Salmonella in Livestock Production in GB 2019 September 2020

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Contents

Glossary ............................................................................................................................... 1

Introduction .......................................................................................................................... 3

Statutory Aspects of Salmonella Control in Great Britain ................................................. 3

Definition of an Isolation and Incident .............................................................................. 5

Serotyping and Phage Typing Methods ........................................................................... 7

Methods Used For Screening Salmonella Vaccine Strains .............................................. 8

Nomenclature ................................................................................................................... 9

Chapter 1: Overview of Salmonella in Livestock and People ............................................. 11

Highlights ....................................................................................................................... 14

Figure 1.1: Isolations of the most common serovars in livestock and people in GB 2019 ....................................................................................................................................... 20

Table 1.1 Salmonella isolations in cattle, sheep, pigs and poultry† on all premises in Great Britain, including statutory and non-statutory results ............................................ 22

Figure 1.2: Isolations of the most common S. Typhimurium phage types (including monophasic strains) in livestock 2019 ............................................................................ 25

Figure 1.3: Isolations of the most common S. Enteritidis phage types in livestock 2019 27

Figure 1.4: Isolations of S. Enteritidis in livestock in GB 2017 - 2019 ............................ 28

Figure 1.5: Isolations of S. Typhimurium in livestock in GB 2017 – 2019 ....................... 29

Figure 1.6: Isolations of S. 4,5,12:i:- in livestock in GB 2017 – 2019 ............................. 30

Figure 1.7: Isolations of S. 4,12:i:- in livestock in GB 2017 – 2019 ................................ 31

Chapter 2: Reports of Salmonella in Cattle ........................................................................ 32

Figure 2.1: Cattle population and number of holdings with cattle in GB 2009- 2019 ...... 35

Table 2.1: Isolations and incidents of Salmonella in cattle on all premises in Great Britain ....................................................................................................................................... 36

Figure 2.2: Isolations of the most common serovars in cattle in GB 2015 – 2019 .......... 38

Figure 2.3: Seasonality of Salmonella Dublin in cattle in Great Britain 2015 - 2019 ....... 39

Figure 2.4: S. Dublin, S. Enteritidis, S. Typhimurium and Salmonella 4,(5),12:i:- as a proportion of all isolations in cattle in Great Britain 1999 – 2019 .................................... 40

Table 2.2: Isolations and incidents of S. Typhimurium in cattle on all premises in Great Britain ............................................................................................................................. 41

Figure 2.5: Top phage types of S. Typhimurium in cattle in GB 2015 - 2019 ................. 42

Figure 2.6: Salmonella Typhimurium DT104 and related strains as a proportion of all isolations of Salmonella Typhimurium and Salmonella 4,(5),12:i:- in cattle in Great Britain 1999 - 2018 ......................................................................................................... 43

Figure 2.7: Salmonella 4,5,12:i:- phage types in cattle in GB 2015 - 2019 ..................... 44

Figure 2.8: Salmonella 4,12:i:- phage types in cattle in GB 2015 – 2019 ....................... 45

Figure 2.9: S. Enteritidis phage types in cattle in GB 2015 – 2019 ................................ 46

Chapter 3: Reports of Salmonella in sheep and goats ....................................................... 47

Sheep ............................................................................................................................. 47

Goats .............................................................................................................................. 49

Figure 3.1: Sheep population and number of holdings with sheep in GB 2010- 2019 .... 50

Table 3.1: Isolations and incidents of Salmonella in sheep on all premises in Great Britain ............................................................................................................................. 51

Table 3.2: Isolations and incidents of Salmonella in goats on all premises in Great Britain ............................................................................................................................. 52

Figure 3.2: Isolations of the most common serovars in sheep in GB 2015 – 2019 ......... 53

Figure 3.3: S. Dublin, S. enterica diarizonae, S. Enteritidis, S. Montevideo, S. Typhimurium and Salmonella 4,(5),12:i:- as a proportion of all isolations in sheep in Great Britain 1999 - 2019 ............................................................................................... 54

Figure 3.4: S. Typhimurium phage types in sheep in GB 2015 - 2019 ........................... 55

Figure 3.5: Salmonella 4,5,12:i:- phage types in sheep in GB 2015 – 2019 ................... 56

Figure 3.6: Salmonella 4,12:i:- phage types in sheep in GB 2015 – 2019 ...................... 57

Chapter 4: Reports of Salmonella in pigs ........................................................................... 58

Figure 4.1: Pig population and number of holdings with pigs in GB 2010 - 2019 ........... 60

Table 4.1: Isolations and incidents of Salmonella in pigs on all premises in Great Britain ....................................................................................................................................... 61

Figure 4.2: Isolations of the most common serovars in pigs in GB 2015 – 2019 ............ 62

Figure 4.3: S. Derby, S. Enteritidis, S. Typhimurium and Salmonella 4,(5),12:i: as a proportion of all isolations in pigs in Great Britain 1999 - 2019 ...................................... 63

Table 4.2: Isolations and incidents of S. Typhimurium in pigs on all premises in Great Britain ............................................................................................................................. 64

Figure 4.4: Isolations of Salmonella Typhimurium phage types in pigs in Great Britain 2015 – 2019 ................................................................................................................... 65

Figure 4.5: Top phage types of S. Typhimurium in pigs in GB 2015 - 2019 ................... 66

Figure 4.6: Salmonella 4,5,12:i:- phage types in pigs in GB 2015 - 2019 ....................... 67

Figure 4.7: Salmonella 4,12:i:- phage types in pigs in GB 2015 - 2019 .......................... 68

Chapter 5: Reports of Salmonella in deer, horses and rabbits ........................................... 69

Table 5.1: Isolations and incidents of Salmonella in deer on all premises in Great Britain ....................................................................................................................................... 71

Table 5.2: Isolations and incidents of Salmonella in rabbits on all premises in Great Britain ............................................................................................................................. 71

Table 5.3: Isolations and incidents of Salmonella in horses on all premises in Great Britain ............................................................................................................................. 72

Figure 5.1: Isolations of the most common serovars in horses in GB 2015 – 2019 ........ 73

Figure 5.2: S. Enteritidis, S. Newport, S. Typhimurium and Salmonella 4,(5),12:i:- as a proportion of all isolations in horses in Great Britain 1999 - 2019 .................................. 74

Table 5.4: Isolations and incidents of S. Typhimurium in horses on all premises in Great Britain ............................................................................................................................. 75

Figure 5.3 Top phage types of S. Typhimurium in horses in GB 2015 - 2019 ................ 76

Figure 5.4: Salmonella 4,5,12:i:- phage types in horses in GB 2015 - 2019 ................... 77

Figure 5.5: Salmonella 4,12:i:- phage types in horses in GB 2015 - 2019...................... 78

Figure 5.6: S. Enteritidis phage types in horses in GB 2015 - 2019 ............................... 79

Chapter 6: Reports of Salmonella in chickens ................................................................... 80

National Control Programme for Salmonella in chickens ............................................... 83

Figure 6.1: Chicken population in GB 2010 – 2019 ........................................................ 92

Table 6.1: Salmonella in chickens on all premises in Great Britain. (Positive flocks from statutory testing; isolations from both statutory and non-statutory testing) ..................... 93

Figure 6.2: The most common serovars in chickens by number of isolations* in GB 2015 – 2019 ............................................................................................................................ 95

Table 6.2: S. Typhimurium in chickens on all premises in Great Britain. (Positive flocks from statutory testing; isolations from both statutory and non-statutory testing) ............. 96

Figure 6.3: Most common phage types of S. Typhimurium in chickens in GB 2015 - 2019† .............................................................................................................................. 97

Figure 6.4: S. Enteritidis phage types in chickens in GB 2015 - 2019† ........................... 98

Figure 6.5: Salmonella 4,5,12:i:- phage types in chickens in GB 2015 - 2019† .............. 99

Figure 6.6: Salmonella 4,12:i:- phage types in chickens in GB 2015 - 2019† ............... 100

Table 6.3: S. Enteritidis in chickens on all premises in Great Britain. (Positive flocks from statutory testing; isolations from both statutory and non-statutory testing) ................... 101

Figure 6.7: Prevalence of Salmonella in breeding chicken flocks tested under NCP in GB 2008 – 2019 ................................................................................................................. 102

Table 6.4: Chicken breeding flocks in GB - number of flocks reported positive with each Salmonella serovar, NCP testing 2012 - 2019* ............................................................ 103

Figure 6.8: Serovars identified in adult chicken breeding flocks in GB 2014 - 2019 reported from NCP testing ............................................................................................ 104

Figure 6.9: Prevalence of Salmonella in laying hen flocks tested under NCP in GB 2009 - 2019 ........................................................................................................................... 105

Table 6.5: Laying hen flocks in GB - number of flocks reported positive with each Salmonella serovar, NCP testing 2015 - 2019* ............................................................ 106

Figure 6.10: The most common serovars identified in adult laying hen flocks in GB 2014 - 2019 reported from NCP testing ................................................................................ 107

Figure 6.11: Prevalence of Salmonella in broiler chicken flocks tested under NCP in GB 2010 - 2019 .................................................................................................................. 108

Table 6.6: Broiler chicken flocks in GB - number of flocks positive for each Salmonella serovar, NCP testing 2015 - 2019* ............................................................................... 109

Table 6.6: Broiler chicken flocks in GB - number of flocks positive for each Salmonella serovar, NCP testing 2015 - 2019* - continued ............................................................ 110

Figure 6.12: The most common serovars identified in broiler chicken flocks in GB 2014 - 2019 reported from NCP testing ................................................................................... 111

Chapter 7: Reports of Salmonella in turkeys .................................................................... 112

National Control Programme for Salmonella in fattening and breeding turkeys ........... 115

Table 7.1: Salmonella in turkeys on all premises in Great Britain. (Positive flocks from statutory testing; isolations from both statutory and non-statutory testing) ................... 118

Figure 7.1: The most common serovars in turkeys by number of isolations* in GB 2015 – 2019 ............................................................................................................................. 120

Figure 7.2: S. Typhimurium phage types in turkeys in GB 2015- 2019† ....................... 121

Figure 7.3: Salmonella 4,5,12:i:- phage types in turkeys in GB 2015 - 2019† ............. 121

Figure 7.4: Salmonella 4,12:i:- phage types in turkeys in GB 2015 - 2019† ................ 122

Figure 7.5: S. Enteritidis phage types in turkeys in GB 2015 - 2019† .......................... 122

Figure 7.6: Prevalence of Salmonella in turkey fattening flocks tested under NCP in GB 2012 - 2019 .................................................................................................................. 123

Figure 7.7: Prevalence of Salmonella in turkey breeder flocks tested under NCP in GB 2012 - 2019* ................................................................................................................. 124

Table 7.2: Turkey fattening flocks in GB - number of flocks reported positive for each Salmonella serovar, NCP testing 2014 - 2018* ............................................................ 125

Figure 7.8: The most common serovars identified in turkey fattening flocks in GB 2014 - 2019 reported from NCP testing ................................................................................... 127

Table 7.3: Turkey breeding flocks in GB - number of adult flocks reported positive for each Salmonella serovar, NCP testing 2015 - 2019* ................................................... 128

Figure 7.9: Serovars identified in adult turkey breeding flocks in GB 2014 - 2019 reported from NCP testing ............................................................................................ 129

Chapter 8: Reports of Salmonella in ducks and geese .................................................... 130

Table 8.1: Isolations and incidents of Salmonella in ducks on all premises in Great Britain ........................................................................................................................... 132

Table 8.2: Isolations and incidents of Salmonella in geese on all premises in Great Britain ........................................................................................................................... 133

Figure 8.1: Isolations of the most common serovars in ducks in GB 2015 – 2019 ....... 134

Figure 8.2: S. Enteritidis, S. Indiana, S. Typhimurium, monophasic variant S. Typhimurium and other serovars as a proportion of all isolations in ducks in GB (1999 - 2019) ............................................................................................................................ 135

Figure 8.3: S. Typhimurium phage types in ducks and geese in GB 2015 – 2019 ....... 136

Figure 8.4: S. Enteritidis phage types in ducks and geese in GB 2015 – 2019 ............ 137

Figure 8.5: Salmonella 4,12:i:- phage types in ducks and geese in GB 2015 - 2019 ... 138

Chapter 9: Reports of Salmonella in other statutory birds ................................................ 139

Game birds ................................................................................................................... 139

Pigeons ........................................................................................................................ 140

Table 9.1: Isolations and incidents of Salmonella in guinea fowl on all premises in Great Britain ........................................................................................................................... 142

Table 9.2: Isolations and incidents of Salmonella in partridges on all premises in Great Britain ........................................................................................................................... 142

Table 9.3: Isolations and incidents of Salmonella in pheasants on all premises in Great Britain ........................................................................................................................... 143

Table 9.4: Isolations and incidents of Salmonella in quail on all premises in Great Britain ..................................................................................................................................... 144

Table 9.5: Isolations and incidents of Salmonella in pigeons on all premises in Great Britain ........................................................................................................................... 144

Figure 9.1: S. Typhimurium phage types in partridges in GB 2015 - 2019 ................... 145

Figure 9.2: S. Typhimurium phage types in pheasants in GB 2015 - 2019 .................. 146

Figure 9.3: S. Typhimurium phage types in quail in GB 2015 - 2019 ........................... 147

Figure 9.4: S. Typhimurium phage types in pigeons in GB 2015 - 2019 ...................... 148

Figure 9.5: Salmonella 4,12:i:- phage types in partridges in GB 2015 - 2019 .............. 149

Chapter 10: Reports of Salmonella in wildlife .................................................................. 150

Wild Mammals .............................................................................................................. 150

Wild Birds ..................................................................................................................... 151

Figure 10.1: Isolations of Salmonella in wild mammals in GB 2015 - 2019 .................. 152

Figure 10.2: Isolations of Salmonella in wild birds in GB 2015 - 2019 .......................... 153

Table 10.1: Isolations and incidents of Salmonella in wild mammals in Great Britain in 2019 ............................................................................................................................. 153

Chapter 11: Salmonella in animal feedingstuffs and products tested under ABPR .......... 154

Figure 11.1: Animal feedingstuffs and ingredients in GB (tests performed under the ABP (Enforcement) Regulations 2013 and Defra Codes of Practice) 2015 - 2019 ............... 157

Figure 11.2: Animal feedingstuffs and ingredients in GB contamination rate 2015 - 2019 ..................................................................................................................................... 158

Table 11.1: Regulated Salmonella serovars in animal feedingstuffs in Great Britain 2017 – 2019 .......................................................................................................................... 159

Table 11.2: Isolations of Salmonella serovars considered to be of special public health importance from products monitored in Great Britain under the Defra Codes of Practice, 2019 ............................................................................................................................. 161

Figure 11.3: Number of isolations of regulated Salmonella serovars in animal feedingstuffs and products associated with the ABPR 2015 - 2019 by type of feedingstuff ................................................................................................................... 162

Figure 11.4: Number of isolations of regulated Salmonella serovars in animal feedingstuffs and products associated with the ABPR 2015 – 2019 ............................ 163

Figure 11.5: Number of isolations of Salmonella in compound animal feedingstuffs 2015 – 2019 .......................................................................................................................... 164

Table 11.3: Serovars of Salmonella isolated from compound ruminant feed in Great Britain in 2019, compared with the previous two years ................................................ 164

Table 11.4: Serovars of Salmonella isolated from compound pig feed in Great Britain in 2019, compared with the previous two years ............................................................... 165

Figure 11.6: Isolations of the most common serovars in compound ruminant feed, cattle and sheep in GB 2019.................................................................................................. 166

Figure 11.7: Isolations of the most common serovars in compound pig feed and pigs in GB 2019 ....................................................................................................................... 167

Table 11.5: Serovars of Salmonella isolated from compound poultry feed in Great Britain in 2019, compared with the previous two years ........................................................... 168

Table 11.6: Serovars of Salmonella isolated from compound feed for other species* feed in Great Britain in 2019, compared with the previous two years ................................... 169

Figure 11.8: Isolations of the most common serovars in compound poultry feed, and positive flocks of chickens and turkeys from NCP testing in GB 2019 ......................... 170

Table 11.7: Salmonella serovars reported from animal feedingstuff ingredients and products associated with the ABPR in GB 2017 – 2019............................................... 171

Table 11.8a: Serovars of Salmonella in feedingstuff ingredients in GB 2017 - 2019 .... 175

Table 11.8b: Serovars of Salmonella in other products associated with the ABPR in GB 2017 - 2019 .................................................................................................................. 179

Table 11.9: Animal By-Products (Enforcement) Regulations, 2013 - domestic protein official testing – contamination rates in GB 2017 – 2019 .............................................. 186

Table 11.10: Animal By-Products (Enforcement) Regulations, 2013 - serovars isolated during 2017 – 2019 from official and private testing of domestic protein and other products associated with the regulations in GB ............................................................ 186

Table 11.11: The Importation of Processed Animal Protein Order, 1981 - imported animal protein contamination rates in Great Britain in 2019, compared with previous years ............................................................................................................................ 187

Figure 11.9: Contamination rate for domestic and imported processed animal protein (batches tested) in GB 2010 - 2019 ............................................................................. 188

Chapter 12: Antimicrobial susceptibility in Salmonella .................................................... 189

Salmonella Dublin ........................................................................................................ 191

Salmonella Typhimurium .............................................................................................. 191

Monophasic Salmonella Typhimurium Serovars .......................................................... 193

Serotypes Other Than Salmonella Dublin and Salmonella Typhimurium ..................... 193

Individual Antimicrobials ............................................................................................... 194

Public Health Considerations ....................................................................................... 195

Table 12.1: Salmonella Dublin: antimicrobial susceptibility monitoring 2009 – 2019 .... 197

Table 12.2: Salmonella Typhimurium: antimicrobial susceptibility monitoring 2009 – 2019 ............................................................................................................................. 198

Table 12.3: Nalidixic acid resistance in Salmonella Typhimurium DT104 from domestic livestock in 2009 - 2019. Number of isolates tested (percentage resistant to nalidixic acid) ............................................................................................................................. 199

Table 12.4: Trimethoprim/sulphonamide resistance in Salmonella Typhimurium (all phage types) from domestic livestock in 2009 – 2019. Number of isolates tested (percentage resistant to trimethoprim/sulphonamide) .................................................. 200

Table 12.5: Trends in trimethoprim/sulphonamide resistance in certain types of Salmonella Typhimurium from pigs over the period 2009 – 2019. Number of isolates tested (percentage resistant to trimethoprim/sulphonamide) ........................................ 201

Figure 12.1: Number of isolates of S. Typhimurium of the eight most frequent phage types subjected to susceptibility testing at APHA 2010 – 2019 ................................... 202

Figure 12.2: Percentage of the eight most common definitive and undefined phage types of Salmonella Typhimurium susceptible to all 16 antimicrobial agents in 2019 ............ 203

Table 12.6: Salmonella other than Salmonella Dublin and Salmonella Typhimurium: antimicrobial susceptibility monitoring 2009 - 2019 ...................................................... 204

Table 12.7: All salmonellas: antimicrobial susceptibility 2019 ...................................... 205

References ...................................................................................................................... 206

Further Publications of Interest .................................................................................... 209

Quality Statement ............................................................................................................ 215

Section A ...................................................................................................................... 215

Section B ...................................................................................................................... 221

Acknowledgements ...................................................................................................... 224

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Glossary ABPR Animal By-Products Regulations

APHA Animal and Plant Health Agency

BSAC British Society for Antimicrobial Chemotherapy

CSBO Control of Salmonella in Broiler Flocks Order

CSPO Control of Salmonella in Poultry Order

CSTO Control of Salmonella in Turkey Flocks Order

DT Definitive Phage Type of S. Typhimurium as described by Anderson et al (1977)

EFSA European Food Safety Authority

HPS Health Protection Scotland

MDR Multi-drug resistant (resistance to four or more of the antimicrobials in the panel tested)

NCP National Control Programme

NOPT Not phage typed

PHE Public Health England

PT Phage type

RDNC Reacts with the phages but does not conform to a recognised pattern of lysis

Rough Rough strains of Salmonella that cannot be serotyped due to autoagglutination

SE Salmonella Enteritidis

SRUC Scotland’s Rural College

STM Salmonella Typhimurium

U Undesignated. A recognised phage designation with a particular pattern of lysis which has not been included in the definitive typing scheme e.g. U302

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UNTY A culture which does not react with any of the phages in the typing scheme

Untypable A culture which is not suitable for typing

Untypable Some cultures may fail to express one or both sets of flagella antigens and consequently cannot be named. In such cases the antigenic structure is reported or isolates are grouped as ‘untypable strains’

Untyped Full information unavailable at the time of data collation

VIDA Veterinary Investigation Diagnosis Analysis

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Introduction This publication presents data on Salmonella reports from livestock species in Great Britain (England, Wales and Scotland) collected and collated by the Animal and Plant Health Agency (APHA) during 2019 and also provides data from previous years for comparative purposes. The data in the first eleven chapters cover reports of Salmonella in livestock, with separate chapters for the main species, reports of Salmonella in wildlife and reports of Salmonella in animal feedingstuffs. The twelfth chapter covers the antimicrobial susceptibility of Salmonella (England and Wales only).

Since 1993, the date of a Salmonella incident has been recorded as the date it was reported to an Officer of the Minister. Under the present system, any Salmonella reports that are confirmed or identified after the publication of the annual report will be incorporated into the revised tables that appear in the following year’s publication. This may result in the number of incidents and/ or isolations differing from that previously given for a particular year. The most recent version of the report should therefore always be used when comparing data from year to year.

Revisions in the way that data have been compiled and presented since 1993 mean that, with the exception of the tables on Salmonella in animal feedingstuffs, data in this report cannot be compared directly with information published prior to 1993. A more detailed comparison can be generated, if required, for any Salmonella serovar, or phage type in the case of S. Enteritidis and S. Typhimurium. Requests for such data should be made to the Department of Epidemiological Sciences, APHA Weybridge who will be happy to assist with requests (Foodbornezoonoses@apha.gov.uk).

Care should be taken when comparing data from one year to another as an increase or decrease in the number of isolations and incidents does not necessarily indicate a similar change in prevalence. This is because the total number of samples examined and their distribution are often not known.

Statutory Aspects of Salmonella Control in Great Britain On 1st March 1989 the Zoonoses Order 1975 was revoked and replaced by the Zoonoses Order 1989. The 1989 Order added horses, deer and pigeons to the range of species from which Salmonella isolations are subject to reporting. Under the 1989 Order, the responsibility for reporting the isolation of a Salmonella was placed on the laboratory carrying out the examination or, in the case of examinations elsewhere, the person carrying out the examination. In practice, reports of Salmonella isolations must be made to a Veterinary Investigation Officer at one of the Veterinary Investigation Centres (previously Regional Laboratories) of the APHA or to a Regional Veterinary Lead in Scotland. A culture of the organism must be made available on request.

From the late 1980s, there have been statutory Salmonella control programmes for certain sectors of the poultry industry in the UK. These controls have been amended over the

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years. The requirement to test poultry for Salmonella on a regular basis under the Poultry Laying Flocks (Testing and Registration etc.) Order 1989 and the Poultry Breeding Flocks & Hatcheries (Registration and Testing) Order 1989 increased the number of examinations carried out from 1989 onwards. These two Orders were revoked in 1993 with the implementation of the Poultry Breeding Flocks and Hatcheries Order (PBFHO) 1993, which brought Salmonella control measures in poultry into line with the European Union Directive 92/117/EEC with the result that the level of monitoring in some poultry sectors altered. Zoonoses Directive (EC) No. 92/117 required Member States to monitor the trends and sources of various zoonotic agents in animals, feed, food and people, analyse them and report the findings to the Commission. In addition, it required Member States to monitor breeding flocks of domestic fowl (Gallus gallus) for Salmonella. If S. Enteritidis or S. Typhimurium was confirmed to be present in a breeding flock then the flock was slaughtered. The monitoring of breeding flocks took place at hatcheries with follow up confirmation in the birds on the farm.

A review of Directive (EC) No. 92/117 was carried out in the late 1990s by the Scientific Committee on Veterinary Measures relating to Public Health, and in its Opinion published in April 2000 it was considered that the measures in place at that time to control food-borne zoonotic infections were insufficient. The Committee went on to propose other risk management options. As a result, in 2003, Member States agreed that the monitoring of specified zoonotic agents should be expanded and harmonised, where beneficial, in a new Directive (EC) No. 2003/99 and that the risk management measures required to control zoonotic infections should be extended in a new Regulation (EC) No. 2160/2003.

The European Council Directive 2003/99/EC currently provides the statutory basis for monitoring of zoonoses and zoonotic agents in the EU. Member States are required to monitor certain zoonoses and to report to the Commission each year the trends and sources of those zoonotic infections. This Directive covers animals, feed, food and the relevance to human infection, as well as trends in antimicrobial resistance in Salmonella, Campylobacter and other indicator organisms.

The Zoonoses Regulation (EC) No. 2160/2003 came into force on 21st December 2003. The aim of this Regulation is to reduce the prevalence of certain zoonotic infections at the primary production level by establishing the level in the Community and setting a target for reduction. As a result, each Member State is required to produce a programme to achieve the target.

In order to implement Regulation (EC) No. 2160/2003, the Poultry Breeding Flocks and Hatcheries Order (PBFHO) 2007 replaced the PBFHO 1993 and set out the requirements for registration and sampling for a new Salmonella National Control Programme (NCP) for chicken breeding flocks. According to the new Order, statutory testing of breeding flocks of domestic fowl during the rearing phase and during the period of production of eggs for hatching takes place on the breeding flock holding only, and an enhanced sampling (boot swabs or composite faeces) and detection method using Modified Semi-Solid Rappaport Vassiliadis culture medium (ISO 6579: Annex D; now incorporated into ISO6579-1/17) is

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used. The modified sampling protocol specified by the PBFHO 2007 is not directly comparable with that required under the PBFHO 1993.

The PBFHO 2007 was in turn revoked and replaced by the Control of Salmonella in Poultry Order (CSPO) 2007 which came into force in January 2008 and included the requirements for the implementation of a NCP in commercial laying flocks, together with that already in place for breeding chicken flocks. In 2009, the Control of Salmonella in Broiler Flocks Order 2009 came into force in England and Wales, and in Scotland the CSPO 2007 was revoked and replaced by the Control of Salmonella in Poultry (Breeding, Laying and Broiler Flocks) (Scotland) Order 2009. This legislation implemented the requirement for a Salmonella National Control Programme in the broiler chicken sector.

In January 2010, the Control of Salmonella in Turkey Flocks Orders 2009 came into force in England and Scotland, and in February 2010 the Control of Salmonella in Turkey Flocks Order 2010 came into force in Wales. This legislation enforces Regulation (EC) No. 2160/2003 and Regulation (EC) No. 1190/2012 and implements the requirement for a Salmonella National Control Programme in the turkey sector. The Order makes provision for the testing of turkey flocks for Salmonella. As with the NCP in chicken flocks, it also prohibits the use of antimicrobials to control non-clinical Salmonella and live Salmonella vaccines that cannot be distinguished from field strains.

The above changes in legislation and subsequent levels of monitoring for Salmonella in the GB commercial chicken and turkey sectors need to be borne in mind when examining long-term data for poultry. It should also be noted that the poultry industry is currently the only food animal production sector that has structured bacteriological surveillance programmes for Salmonella in place. This routine monitoring may be expected to result in larger numbers of Salmonella isolates than the scanning surveillance of diagnostic submissions that applies to other farm livestock. Please refer to Chapter 6 (Chickens) and Chapter 7 (Turkeys) for further information.

Definition of an Isolation and Incident For all species not covered by a National Control Programme, the tables and figures of this publication give precedence to the number of isolations rather than the number of incidents. This is because the number of isolations gives a more representative picture of the number of Salmonella isolates reported in livestock, however incidents are still useful for epidemiological purposes.

Chapters 6 and 7 (chickens and turkeys, respectively, both of which are covered by NCPs) focus on the number of flocks from which the various Salmonella serovars have been reported and show these data together with the number of isolations. Incidents are not reported in this publication for chickens and turkeys.

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Since the implementation of the NCPs for chicken breeding, laying and broiler flocks in 2007, 2008 and 2009, respectively, the data on positive findings of Salmonella in laying, breeding and broiler chicken flocks have been reported as the number of positive flocks, as required by the legislation, as well as the number of positive isolations detected during the year. This is also the case in turkey flocks, for which the NCP was implemented in 2010. The number of reported isolations of Salmonella detected in chickens and turkeys does not equate directly to the overall number of positive flocks that are detected during the year. A flock is counted as positive only once, irrespective of the number of isolations occurring and the number of serovars identified.

As the tables and figures of Chapter 1 present combined data for cattle, chickens, ducks, pigs, sheep and turkeys, incident data are not shown in this chapter.

Chapter 11 (Feeds) and Chapter 12 (Antimicrobial Susceptibility) show only the number of isolations and cultures, respectively.

Isolates, isolations and incidents are defined in the following way:

An isolate is a single culture of a particular Salmonella, and results from a single sample.

An isolation is defined as the report of the first isolate of a given Salmonella (defined by serovar and/ or phage type, if available) from the same group of animals on a given occasion. If two submissions from the same group of animals on different dates give the same serovar, this is reported as two isolations.

An incident comprises the first isolation and all subsequent isolations of the same serovar, or serovar and phage type combination of a particular Salmonella, from an animal, group of animals or their environment on a single premises, within a defined time period (usually 30 days). Subsequent isolations arising from an incident reported in the previous year are included under the year in which they were reported.

In contrast to Salmonella in humans, many isolations of Salmonella from livestock are not associated with clinical disease or occur on farm premises where Salmonella has been isolated from a group of animals rather than an individual. Since 1993, reports of Salmonella from livestock have been separated into isolations and incidents. ‘Isolations’ comprise individual reports of Salmonella made from samples and reported to Officers of the Minister. ‘Incidents’ do not include repeat isolations of a serovar that may result from a number of samplings during the course of an investigation or monitoring activities on a particular premises.

The first such report of any particular serovar or serovar and phage type combination of Salmonella from a particular animal, group of animals or their environment will therefore be recorded as one incident and one isolation. Further reports of the same Salmonella from the same group during the incident investigation will be recorded as further isolations, but not as further incidents unless the isolation is from an epidemiologically distinct group of animals. Examples of this would include a distinct group of the same species on a

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separate part of the same premises. Reports of a different serovar or phage type of Salmonella from the same animals will be recorded as a new incident. Thus two reports of S. Typhimurium, one of DT104 and another of DT193, from the same group of animals would count as one incident and one isolation of S. Typhimurium DT104 and one incident and one isolation of S. Typhimurium DT193, whilst two reports of S. Typhimurium DT12 from the same group of animals on different occasions within a 30 day period would count as one incident but two isolations.

Serovar and phage type combinations where the phage type is RDNC were previously not considered to be incidents. This was changed in 2018 and these serovar and phage type combinations are now recorded as incidents. Serovar and phage type combinations where the phage type is UNTY or NOPT are not considered to be incidents.

Since 2006, any poultry hatchery isolates for which there are no supply flock details available have been treated as isolations only as they cannot be traced back to a specific flock.

The concept of an ‘incident’ is inappropriate when referring to isolations from animal feedingstuffs or human foodstuffs of animal origin, so data for these are only reported in terms of isolations of Salmonella.

All isolates (except some feed and food isolates) that have been identified in England and Wales are required to be sent to an APHA Laboratory for examination and confirmation of Salmonella. Of those samples taken in Scotland, the majority of poultry samples are sent to APHA Lasswade and all mammalian samples are sent to the SAC Consulting (part of SRUC) and confirmed by Health Protection Scotland.

Data from research projects and surveys are excluded from the tables in the species chapters in this publication. The antimicrobial susceptibility chapter (Chapter 12) contains data from routine surveillance and other surveillance projects.

Serotyping and Phage Typing Methods Salmonella isolated from animals and feed is biochemically or serologically confirmed and serotyped by micro, tube and/ or slide agglutination tests. Each culture is tested for the presence of somatic and flagella antigens by agglutination with specific Salmonella antisera. Where homologous antiserum and antigen react, clumps of bacteria form as visible agglutination. Serovars are derived by reference to the White-Kauffmann-Le Minor Scheme. Additional biochemical tests are needed to confirm some serovars. Since 2010, only S. Typhimurium and S. Enteritidis have been routinely phage typed. Cultures are seeded onto special agar plates and a specific set of phages applied to the culture. After incubation, the pattern and degree of lysis is read and a phage type attributed to the culture (Anderson et al 1977, Ward et al 1987). In the case of S. Typhimurium, some phage types are not fully validated as being stable and specific for the serovar. These are referred to as undesignated phage types (U) rather than definitive phage types (DT).

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Serotyping and phage typing of samples received from premises in England and Wales is carried out by the APHA. Mammalian isolates, and some poultry isolates, from Scotland are serotyped and also assessed by HPS using whole genome sequencing. The majority of poultry samples from Scotland are serotyped and phage typed by APHA, using conventional methods.

Some phage types are recorded as RDNC (reacts with the phages but does not conform to a recognised phage type). In previous years, where the same RDNC pattern was regularly reported this would be considered by PHE and assigned a U type number with a definitive type (DT) designated after further validation. As PHE no longer carry out conventional phage typing this activity was not carried out in 2019, resulting in an increased number of RDNC phage types.

Some phage types may be ‘related variants’ although they are still reported as distinct types, e.g. PT4 and PT7 of S. Enteritidis and DT12, DT104, DT104b and U302 of S. Typhimurium. More than one phage type may sometimes be recovered from a group of animals that is sampled by means of environmental samples. This may result from variations in the attachment of phages to organisms that have been exposed to environmental stress.

Monophasic or aphasic group B Salmonella strains, which lack one or both sets of flagella antigens, can be confirmed as variants of S. Typhimurium by obtaining a definitive phage type (DT) for the strain or by monophasic S. Typhimurium-specific PCRs. PCR methods can also be used to confirm the absence of flagella genes (rather than poor expression of flagella proteins) and the presence of a particular genomic island that is characteristic of the monophasic S. Typhimurium DT193/120 variant strains that have emerged since 2006.

A new procedure for simplified presumptive identification of Salmonella Derby from certain known persistently infected turkey fattening farm sources was introduced in 2016 to reduce the cost of serotyping large numbers of such isolates. In this process, slide agglutination testing of such Group B isolates was used to identify S. Derby [4,5,12:f,g:((1,2)], and to exclude the possibility of S. Typhimurium [4,5,12:i:1,2] or S. Agona [4,5,12:f,g,s:1,2]. After confirmation, the isolates were reported as ‘presumptive S. Derby’ as full serotyping had not been carried out. Any non-Group B isolates, isolates which react with Hi or Hs antiserum or isolates for which definitive S. Derby-related antigens could not be confirmed were subjected to full serotyping. The use of this procedure was discontinued for 2019 due to a fall in the number of S. Derby isolates received for serotyping.

Methods Used For Screening Salmonella Vaccine Strains Following the introduction of live vaccines for Salmonella Enteritidis and Salmonella Typhimurium in poultry, additional testing is required to distinguish field strains from vaccine strains.

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Salmonella Enteritidis and relevant S. Typhimurium isolates are compared to the Avipro Vac E and Vac T vaccine strains, which carry antimicrobial resistance markers, using a panel of four relevant antimicrobials in a disc diffusion technique. Both Avipro Vac E and Avipro Vac T are sensitive to erythromycin and resistant to rifampicin to distinguish them from Salmonella field strains. To differentiate between the two Avipro vaccine strains, Vac E has additional high level resistance to streptomycin and Vac T has an additional resistance to nalidixic acid. Avipro Duo comprises a mixture of Avipro Vac E and Vac T.

Salmovac 440 (which used to be called Gallivac SE) vaccine has no resistance markers but contains mutations causing auxotrophism for histidine and adenine. Salmonella Enteritidis isolates are compared to the vaccine strain by growth on minimal media with and without histidine and adenine.

Tests for Vac E and Vac T vaccine strains and Salmovac 440 vaccine tests are carried out at APHA Weybridge.

Vaccine strains are excluded from the text, tables and figures of this report.

Nomenclature The nomenclature used throughout this publication follows that devised by Le Minor and Popoff which divides the bacterial genus Salmonella into two species: Salmonella enterica and Salmonella bongori. The species Salmonella enterica is further divided into six subspecies: enterica, salamae, arizonae, diarizonae, houtenae and indica.

The method of naming serovars of subspecies enterica largely differs from that used for the other five subspecies in that the familiar serovar names are assigned to serovars within subspecies enterica whilst members of the other subspecies are designated by antigenic formulae.

For example, following this method the serovar originally referred to

as Salmonella typhimurium is now known as Salmonella enterica subspecies enterica serovar Typhimurium, which may be shortened to Salmonella Typhimurium and the naming of serovars of subspecies diarizonae is, for example, Salmonella enterica subspecies diarizonae serovar 61:k:1,5,7 (or Salmonella III 61:k:1,5,(7)). For further details of this nomenclature see Grimont & Weill (2007).

The serovar formally known as Salmonella Java has now been reclassified, on the basis of genetic similarity studies, as Salmonella Paratyphi B variant (var.) Java. It is a group B Salmonella and has the same antigenic structure as Salmonella Paratyphi B (4,12:b:1,2). Salmonella Paratyphi B var. Java and Salmonella Paratyphi B are differentiated by the dextro-tartrate test, in which Salmonella Paratyphi B var. Java gives a positive acid reaction, whereas Salmonella Paratyphi B is negative.

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Similarly, Salmonella Pullorum is now designated as S. Gallinarum biovar Pullorum and some other individual serovars have also been consolidated as variants of a single serovar (e.g. S. Orion/ Binza).

The serovar previously reported as S. Binza is now recorded under the updated nomenclature of S. Orion var. 15+. It is for this reason that the tables of this publication show no reports of S. Binza.

The serovar previously reported as S. Newbrunswick is now recorded under the updated nomenclature of S. Give var. 15+.

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Chapter 1: Overview of Salmonella in Livestock and People This chapter provides information on Salmonella isolated from livestock from samples taken from all types of premises, including farms, hatcheries, veterinary practices, zoos and slaughterhouses. An overview of the number of isolations of Salmonella reported from farm animal species is given in Table 1.1 (poultry refers to reports from chickens, turkeys and ducks).

It is important to note that data for the different species are not directly comparable. Most Salmonella reports from cattle, sheep and pigs result from the investigation of clinically diseased animals whereas reports from chickens and turkeys are mostly from statutory surveillance. However, trends over time within species are largely comparable, especially for chickens and turkeys since the introduction of the Salmonella National Control Programmes (NCPs).

For comparison purposes, data have been reproduced here on the number of laboratory reports of human isolations of Salmonella reported in England and Wales to Public Health England (PHE), Colindale and in Scotland to Public Health Scotland (PHS) (Figure 1.1). There are a number of factors that influence the reporting of these data by clinical microbiology laboratories. These are discussed in the Zoonoses Report UK 2017 (PHE 2018)1.

Figure 1.1 shows the most common Salmonella serovars isolated from livestock in Great Britain in 2019 alongside the most common serovars isolated from human cases of salmonellosis in Great Britain. Figures 1.2 and 1.3 provide data for phage types of S. Typhimurium and S. Enteritidis in livestock; human data are not shown in these figures as phage types are not available following the discontinuation of phage typing by PHE with the implementation of whole genome sequencing for routine surveillance of Salmonella. Apart from S. Typhimurium (including monophasic variants) and S. Enteritidis, serovars commonly associated with human cases are reported relatively rarely from British livestock.

In 2019, a total of 9,588 isolations of Salmonella from humans were reported to PHE (representing England and Wales) and PHS; this is 5.5% lower than in 2018 (10,143 isolations) and 3.7% lower than in 2017 (9,961 isolations).

1 https://assets.publishing.service.gov.uk/government/uploads/system/uploads/attachment_data/file/765111/UK_Zoonoses_report_2017.pdf

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Figures showing the relative frequency of the most common Salmonella serovars in each animal species during 2019 (Figure 1.1) should be considered alongside absolute numbers of isolations (Table 1.1). This is because the relative proportions of each serovar may remain similar despite a change in number of isolations, in which case we assume that the change in number of isolations is likely to be constant across serovars. Similarly, if there is a change in serovar relativity, it is only by examining changes in absolute numbers that we can ascertain the size of any increase or decrease.

In 2019, the total number of Salmonella isolation reports from cattle, sheep, pigs and poultry decreased by 13.8% compared with 2018 but increased by 11.3% compared with 2017 (Table 1.1). This was mainly due to a decrease in isolations from ducks and turkeys. Increases in the number of reports were, however, not consistent across serovars; for example, reports of S. Kedougou were two times higher than in 2018, reports of S. Oslo were one-and-a-half times higher, reports of S. Senftenberg increased by 42.9% and reports of S. Montevideo increased by 42.0%. However, reports of S. Derby, Salmonella 13,23:i:-, S. Dublin and S. Mbandaka fell by 58.5%, 36.0%, 18.5% and 12.3%, respectively. In addition, reports of S. Enteritidis were 66.7% higher (50 isolations vs. 30 isolations) during 2019 compared with 2018 but only 11.1% higher than in 2017 (45 isolations), with increases reported mainly from chickens and horses. Reports of S. Typhimurium were 27.1% lower than during 2018 (124 isolations vs. 170 isolations) but almost identical to 2017 (123 isolations).

The most important factor which may bias the number of Salmonella reports from species not covered by NCPs (i.e. species other than chickens and turkeys) is the submission rate. This report presents numerator data but the denominator, in most cases, is unknown and may change over time. However, we use the number of diagnostic submissions to Animal and Plant Health Agency (APHA) and Scotland’s Rural College (SRUC) as a proxy to understand if the denominator may have significantly changed. Most Salmonella reports from cattle, sheep and pigs result from the investigation of clinically diseased animals, and economic factors may exert a strong influence on diagnostic practices, such as whether a veterinary surgeon is consulted and whether samples are submitted for laboratory examination. The Salmonella data from these species is likely to be most influenced by changes in submission rate.

The number of diagnostic submissions to the APHA and SRUC decreased by 8.6% in 2019 compared with 2018. This decrease was seen for all species apart from pigs and miscellaneous species with the greatest falls being in sheep (16.1% decrease) and cattle (8.3% decrease). As the majority of the isolations from species other than poultry relate to clinical investigations (although the Salmonella found may not always be the primary cause of the illness) the current prevalence of subclinical infection in these species of livestock is not known. Most sample submissions from poultry are associated with statutory or voluntary surveillance activities. Although trends in Salmonella reports from species not covered by NCPs can be compared with diagnostic submission rates to APHA/ SRUC, it should be remembered that not all submissions will have been examined for

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Salmonella. Private laboratories also report the isolation of Salmonella and the total number of submissions to these laboratories is unknown.

There were 3,428 isolations of Salmonella in livestock in 2019 which represents a decrease of 9.8% compared with 2018 (3,798 isolations). This comprised 3,204 isolations from species covered by the statutory reporting requirements of the Zoonoses Order 1989 (1,749 isolations from chickens, 467 isolations from cattle, 293 isolations from ducks, 267 isolations from turkeys, 167 isolations from pigs, 126 isolations from horses, 103 isolations from sheep, eleven isolations from pigeons, eight isolations from pheasants, five isolations from partridges, five isolations from quail, two isolations from deer and one isolation from goats) plus 224 isolations from non-statutory species (e.g. cats, dogs and reptiles, which are not reported in detail in this publication).

Relative to 2018, there were more isolations from horses (126 vs. 21 isolations), pigeons (11 vs. 9 isolations) and quail (5 vs. 2 isolations).

The surveillance data for 2019 shows that only 27.2% of the isolations of Salmonella reported to APHA resulted from samples taken due to clinical disease in livestock. This is higher than during 2018 when 24.5% of isolations were from clinical disease investigations but lower than in 2017 when 30.4% of isolations were from clinical disease investigations. This contrasts with data for Salmonella in humans where reports usually originate from cases of clinical disease.

The majority of the isolations reported from chicken and turkey flocks (83.4% and 89.5%, respectively) during 2019 were the result of statutory surveillance activities due to the NCPs that are in place for these sectors (further information on the NCPs is included in Chapter 6 and Chapter 7). This differs from years prior to the introduction of the NCPs when the majority of chicken and turkey isolations originated from voluntary surveillance. Voluntary Salmonella surveillance of healthy flocks is common practice in the duck industry. In 2019, all Salmonella isolations from ducks resulted from voluntary surveillance.

The total number of S. Typhimurium isolations from cattle, sheep, pigs and poultry fell by 27.1% in 2019 (124 isolations) relative to 2018 (170 isolations). There was a decrease in the number of isolations from most sectors relative to the previous year; isolations from ducks fell by 81.8% (2 vs. 11 in 2018), isolations from sheep fell by 73.3% (4 vs. 15), isolations from pigs decreased by 23.1% (50 vs. 65) and isolations from cattle decreased by 15.6% (54 vs. 64) (Figure 1.5). However, isolations of S. Typhimurium in chickens was 55.6% higher in 2019 compared to 2018 (14 vs. 9 isolations in 2018). Isolations of the monophasic strain Salmonella 4,5,12:i:- also decreased (by 21.8%) in 2019, (Figure 1.6). In contrast, isolations of Salmonella 4,12:i:- increased by 7.3% compared with 2018, with an increase in isolations in the pig sector (Figure 1.7). Reports of S. Enteritidis also increased by 66.7% in 2019 compared with 2018 (50 vs. 30 isolations), and by 11.1% compared with 2017 (45 isolations). As in previous years, the majority of S. Enteritidis isolations in 2019 were reported from chickens, but there were also single isolations each from cattle and pigs; the first time that S. Enteritidis has been reported from pigs since 2008. This contrasts with 2018 when isolations of S. Enteritidis came from chicken and

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cattle only, and with 2017 when there were isolations from chickens, cattle, ducks and turkeys (Figure 1.4).

Highlights

Cattle

• Salmonella isolations from cattle in 2019 were 5.3% lower compared to 2018 (467 vs. 492 isolations) (Table 2.1).

• Salmonella Dublin remained the most commonly reported serovar (261 isolations) accounting for 55.9% of total cattle isolations. This was lower than during 2018 in terms of absolute number of isolations (316 isolations in 2018) and proportion of all cattle isolations (64.2% in 2018).

• The second most common serovar in 2019 was S. Mbandaka (78 isolations; 16.7% of total cattle isolations) and the third most common serovar was S. Typhimurium (54 isolations; 11.6% of total cattle isolations). This differs from 2018 when S. Typhimurium was the second most common serovar and S. Mbandaka the third (13.0% and 7.1% of total cattle isolations, respectively). Of the 54 isolations of S. Typhimurium, the most common phage types were DT104 (18 isolations) and UNTY (15 isolations).

• The combined number of reports of the monophasic variants of S. Typhimurium in 2019 was similar to 2018 (14 isolations vs. 13 isolations) and made up a slightly higher percentage of total isolations from cattle (3.0% vs. 2.6% of total cattle isolations). There were seven isolations of Salmonella 4,5,12:i:- and seven isolations of Salmonella 4,12:i:- in 2019.The most common phage type was DT193 (10 isolations; 71.4% of total monophasic variants)

• There was a single isolation of S. Enteritidis (NOPT) compared with three isolations during both 2018 and 2017.

Small ruminants

• Reports of Salmonella from sheep in 2019 were slightly lower than during 2018 (103 isolations vs. 110 isolations) and 2017 (110 isolations) (Table 3.1).

• Salmonella enterica subspecies diarizonae serovar 61:k:1,5,(7) (and variants) remained the most common serovar (59 isolations; 60.2% of total sheep isolations).

• Salmonella Montevideo was the second most commonly reported serovar from sheep during 2019 (16 isolations; 16.3% of total reports from sheep) and S. Dublin was the third most common (6 isolations; 6.1% of total reports from sheep).

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• Salmonella Typhimurium was the fourth most commonly reported serovar from sheep in 2019 (4 isolations; 4.1% of total sheep report), having been the second most common in 2018 (15 isolations; 13.6% of total reports from sheep), together with S. Agama (also 4 isolations). The phage types of S. Typhimurium reported in 2019 were U320 (2 isolations) and single isolations of DT104 and UNTY. There were no isolations of Salmonella 4,5,12:i:- and one isolation of Salmonella 4,12:i:- (not phage typed) in 2019, which was the same as during 2018 and compares with no isolations of either serovar in 2017.

• There was a single isolation from goats in 2019 (Salmonella 16:z10:e,n,x,z15) compared with no reports during 2018 or 2017. Prior to 2019 the last report from goats in GB was in 2016 (one isolation of S. Coeln).

Pigs

• The number of Salmonella isolations from pigs in 2019 was similar to 2018 (167 isolations vs. 169 isolations) and 20.1% higher than during 2017 (139 isolations) (Table 4.1).

• Salmonella Typhimurium (including monophasic variants, 4,[5],12:i:-) were together responsible for 76.0% of all isolations, compared with 79.9% in 2018 and 86.3% in 2017. Compared with 2018, this decrease was largely attributable to a decrease in S. Typhimurium (50 isolations vs. 65 isolations) partially offset by an increase in reports of Salmonella 4,12:i:- (47 isolations vs. 37 isolations).

• The most common phage type of S. Typhimurium was U288 (22 isolations; 44.0% of total S. Typhimurium isolations in pigs). Phage type DT193 was the most common phage type of both Salmonella 4,5,12:i:- and Salmonella 4,12:i:-, with 28 isolations (93.3% of total) and 40 isolations (85.1% of total), respectively.

Deer, Horses and Rabbits

• There were two isolations of Salmonella from deer during 2019 compared with one isolation during 2018 and none during 2017. The serovars reported were single isolations of S. Montevideo and monophasic Salmonella Typhimurium 4,5,12:i:- NOPT; neither of these serovars have previously been reported from deer in GB.

• As in both 2018 and 2017, there were no isolations of Salmonella from rabbits during 2019. The last isolation of Salmonella from rabbits was in 2016 (Salmonella 21:g,t:-) (Table 5.2).

• There were 126 isolations of Salmonella from horses in 2019, which is six times that reported during 2018 (21 isolations) and approximately three times the number in 2017 (39 isolations) (Table 5.3).

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• Salmonella Typhimurium was the most commonly reported serovar from horses during 2019 (34 isolations; 27.0% of total horse isolations) and S. Oslo was the second most common serovar (23 isolations; 18.3% of total horse isolations). Although S. Typhimurium was also the most common serovar during 2018 along with S. Bovismorbificans (33.0% of total horse isolations each), there were only seven isolations. Compared with 2018, reports of S. Bovismorbificans in horses more than doubled in 2019 (19 isolations vs. 7 isolations); however, this serovar fell to be the third most common in 2019 (15.1% of total horse isolations).

• There were six isolations of Salmonella 4,5,12:i:- (all DT193) and 12 isolations of Salmonella 4,12:i:- (all DT193) during 2019 compared to none of either serovar during 2018. The most common phage type of S. Typhimurium was U302 (6 isolations; 17.6% of S. Typhimurium isolations).

Chickens

• Including both NCP and non-statutory surveillance data, there were 1,749 isolations of Salmonella from chickens in 2019. This is a decrease of 4.8% compared with 2018 but an increase of 51.6% compared with 2017 (Table 6.1).

• The most commonly reported serovars were:

– Salmonella 13,23:i:- (436 isolations; 24.9% of total chicken isolations).

– S. Mbandaka (367 isolations; 21.0% of total chicken isolations).

– S. Kedougou (357 isolations; 20.4% of total chicken isolations).

– S. Montevideo (169 isolations; 9.7% of total chicken isolations).

– S. Ohio (75 isolations; 4.3% of total chicken isolations).

• There were 48 isolations of S. Enteritidis in 2019 compared with 27 isolations during 2018 and 25 isolations during 2017 .The most commonly reported phage type in 2019 was PT8 (35 isolations).

• There were 14 isolations of S. Typhimurium compared with nine in 2018; the most commonly reported phage types were DT99 (4 isolations) and RDNC (4 isolations). There were also two isolations of DT193 and single isolations of DT2, DT13, DT35 and DT36. There also were seven isolations of monophasic strains of S. Typhimurium, including four isolations of Salmonella 4,5,12:i:- (all DT193) and three isolations of Salmonella 4,12:i:- (DT193 (x1) and UNTY (x2)), compared with two isolations and eight isolations, respectively, during 2018. There was one further isolation of Salmonella 4,12:i:- from chickens in 2019, but this was not confirmed as monophasic S. Typhimurium by PCR.

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• Information and data are given in Chapter 6 (Reports of Salmonella in Chickens) on the National Control Programmes (NCPs) for Salmonella in breeding flocks, laying hen flocks and broiler flocks. The estimated prevalence of regulated serovars in all three chicken NCPs was well below the EU targets of 1% for breeders, 2% for layers and 1% for broilers (0.00% for breeders, 0.40% for layers and 0.03% for broilers).

Turkeys

• Including both NCP and non-statutory surveillance data, there were 267 isolations of Salmonella from turkeys in 2019. This is a decrease of 46.3% compared with 2018 (497 isolations) and a 46.5% decrease compared with 2017 (499 isolations) (Table 7.1). This is the lowest number of isolations since 2014 (193 isolations) and the second lowest since the implementation of the turkey NCP in 2010.

• As in previous years, the most common serovar reported from turkeys was S. Derby (132 isolations; 49.4% of total turkey isolations). This is a decrease of 67.1% compared with 2018 (401 isolations) and a 62.4% decrease compared with 2017 (351 isolations). All isolates of S. Derby were fully serotyped during 2019. This is in contrast to 2017 and 2018 when due to the large number of S. Derby isolates received from certain sources only partial serotyping was carried out for the majority of isolates.

• There were two isolations of monophasic Salmonella Typhimurium 4,5,12:i:- in 2019; both were phage type DT193. This is much lower than in 2018 (14 isolations). Similarly, there were no isolations of Salmonella Typhimurium 4,12:i:- in 2019, compared to one isolation in 2018, and there were no isolations of S. Typhimurium in 2019 compared with six isolations in 2018.

• Information and data are given in Chapter 7 (Reports of Salmonella in Turkeys) on the National Control Programmes (NCP) for Salmonella in turkeys. The estimated prevalence of regulated serovars for turkey fatteners was 0.0%, which is well below the EU target of 1%. The estimated prevalence of regulated serovars for turkey breeding flocks in GB was 0.73%, which is below the EU target of 1%.

Ducks and Geese

• There were 293 isolations of Salmonella from ducks in 2019 compared with 430 isolations 2018 (31.9% decrease) and 395 isolations in 2017 (25.8% decrease). All of the isolations resulted from voluntary Salmonella monitoring in commercial duck flocks (Table 8.1).

• The most commonly isolated serovars from ducks were S. Indiana (93 isolations; 31.7% of total duck isolations), S. Give var. 15+ (53 isolations; 18.1% of total duck isolations), S. Hadar (39 isolations; 13.3% of total duck isolations) and S. Orion var. 15+ (36 isolations; 12.3% of total duck isolations). There were only two isolations of S.

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Typhimurium (UNTY (x2)) compared with eleven in 2017 and no isolations of S. Enteritidis; the same as during 2018.

• There were no isolations of Salmonella from geese in 2019 compared with four isolations in 2018 and six isolations in 2017 (Table 8.2).

Other Statutory Birds (as specified in the Zoonoses Order)

• There were 18 isolations of Salmonella from game birds in 2019 (guinea fowl, partridges, pheasants and quail), which is almost the same as during 2018 (17 isolations) but a 30.8% decrease compared with 2017 (25 isolations). Compared with 2018, reports from quail increased (5 isolations vs. 2 isolations), reports from pheasants fell (8 isolations vs. 10 isolations) and reports from partridges remained the same (5 isolations).

• The most commonly reported serovar from game birds was S. Senftenberg (9 isolations; 50.0% of total game bird isolations); the second most commonly reported was S. Bredeney (3 isolations; 16.7% of total game bird isolations). Salmonella Typhimurium, which in 2018 was the most commonly reported serovar (8 isolations; 47.1% of total game bird isolations) fell to the third most common serovar in 2019 together with S. Orion var. 15+ (both 2 isolations; 11.1% of total game bird isolations each).

• There were eleven Salmonella isolations from pigeons in 2019, which was 22.2% higher than in 2018 (9 isolations) but 26.7% lower than in 2017 (15 isolations). All eleven isolations were S. Typhimurium; the most common phage type was DT2 with five isolations.

Wildlife

• There were four isolations of Salmonella from wildlife during 2019, all from wild mammals. This is lower than 2018 when there were seven isolations but higher than 2017 when there was only one isolation.

• Salmonella Enteritidis was the only serovar reported, with three isolations of S. Enteritidis PT11 and one isolation of S. Enteritidis UNTY. These were found in hedgehogs.

Feedingstuffs

• During 2019, 1.7% of tests carried out under the Animal By-Products Regulations (ABPR) and Defra Codes of Practice were positive for Salmonella. This is lower than during 2018 when 1.9% of tests were positive for Salmonella but higher than during 2017 when 1.3% of tests were positive for Salmonella.

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• There were 88 isolations of regulated Salmonella serovars from animal feedingstuffs and related products during 2019, 39.7% higher than in 2018 (n=63) and almost three times higher than in 2017 (n=31).

• The most commonly reported serovars from animal feedingstuffs and compound feed during 2019 were S. Tennessee (60 isolations), S. Senftenberg (47 isolations) and S. Ohio (42 isolations).

• There were 245 reports of Salmonella from pet food which was intended to be fed raw during 2019. This is 30.3% higher than 2018 when there were 188 reports and 53.1% higher than 2017 when there were 160 reports. The most common serovars reported during 2019 were S. Indiana (31 isolations), S. Derby (14 isolations), S. Mbandaka (14 isolations) and S. Bovismorbificans (12 isolations).

• The isolation rate of Salmonella from domestic processed animal protein in 2019 was 1.7%, higher than during 2018 when it was 0.5%.

• There were no batches of imported processed animal protein tested during 2019, the same as during 2018 and 2017.

Antimicrobial Susceptibility Testing

• Of the 4,522 Salmonella isolates examined during 2019, 72.2% were susceptible to all 16 antimicrobial drugs tested against. This is slightly lower than in 2018, when 76.5% of isolates were susceptible to all 16 antimicrobials drugs.

• A total of 254 cultures of Salmonella Typhimurium were examined in 2019, of which 49.2% were susceptible to all the antimicrobials tested against. This is a decrease compared with 2018 when 54.4% were susceptible to all antimicrobials tested, but higher than in 2017 when 34.2% were susceptible to all antimicrobials tested.

• 4,010 isolates of serovars other than S. Dublin or S. Typhimurium were tested in 2019 and 71.9% of these were susceptible to all the antimicrobials tested against.

• Resistance to third generation cephalosporins and fluoroquinolones is considered of high importance, since these antimicrobials are used for the treatment of more serious cases of human salmonellosis. The percentage of Salmonella isolates that were resistant to ciprofloxacin in 2019 was 0.4%. Cefotaxime or ceftazidime resistance was not detected in S. Enteritidis from animals in 2019. One single S. Enteritidis isolate (a PT12 from quail) was resistant to ciprofloxacin in 2019. Such findings are important since this serovar is of particular public health significance.

Full details of the above highlights can be found in the individual chapters.

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Figure 1.1: Isolations of the most common serovars in livestock and people in GB 2019

† Public Health England’s SGSS is a live laboratory reporting system therefore numbers are subject to change and may not be directly comparable with data reported in previous years. Since 1 st December 2014, data have been derived from the Second-Generation Surveillance System (SGSS). Data reported prior to 1 st December 2014 were generated using legacy laboratory reporting systems and may not be directly comparable to SGSS generated data.

Dublin55.9%

Mbandaka16.7%

Ty phimurium11.6%

Montev ideo3.9%

4,12:i:-1.5%

4,5,12:i:-1.5%

Newport1.3%

Other serov ars

7.7%

Cattle (n=467)

enterica diarizonae

61:k:1,5,(7) and v ariants

60.2%

Montev ideo15.5%

Dublin5.8%

Agama3.9%

Ty phimurium3.9%

Other serov ars

13.6%

Sheep (n=103)

Ty phimurium29.9%

4,12:i:-28.1%

4,5,12:i:-18.0%

Bov is-morbif icans

7.2%

Kedougou4.8%

Derby3.6%

Newport3.6%

Other serov ars

4.8%

Pigs (n=167)

Other serov ars

36.9%

Enteritidis30.8%

Ty phimurium (including

monophasic strains)18.5%

Newport3.0%

Inf antis2.3%

Agona2.2%

Mikawasima1.7%

Jav a1.6%

Stanley1.6%

Virchow1.5%

People (n=9,588)†

21

Figure 1.1: Isolations of the most common serovars in livestock and people in GB 2019 - continued

** Includes both statutory and non-statutory data ** Includes both statutory and non-statutory data

13,23:i:-24.9%

Mbandaka21.0%

Kedougou20.4%

Montev ideo9.7%

Ohio4.3%

Senf tenberg4.1%

Enteritidis2.7%

Derby2.5%

Agona1.8%

Other serov ars

8.6%

Chickens** (n=1,749)

Derby49.4%

Senf tenberg18.0%

Kedougou16.5%

Agona3.4%

Mbandaka1.9%

Newport1.9%

Anatum1.5%

Kottbus1.5% Other

serov ars6.0%

Turkeys** (n=267)

Indiana31.7%

Giv e v ar. 15+

18.1%Hadar13.3%

Orion v ar. 15+

12.3%

Orion5.1%

Giv e 3.8%

Kottbus3.8%

Oslo3.1%

Bov is-morbif icans

2.7%

Other serov ars

6.1%

Ducks (n=293)

22

Table 1.1 Salmonella isolations in cattle, sheep, pigs and poultry† on all premises in Great Britain, including statutory and non-statutory results

Salmonella 2015 2016 2017 2018 2019 subspecies ENTERICA ENTERICA Africana - - - - 1 Agama 15 10 14 7 12 Agona 9 7 15 17 40 Ajiobo 3 10 3 - - Albany - - - - 2 Albert - - - 2 - Anatum 6 12 11 8 12 Anatum var. 15+ 2 - - - - Bardo - 1 1 1 1 Berta - - 1 - 1 Bovismorbificans 14 24 37 17 20 Braenderup 2 - - - - Bredeney 1 1 - - - Budapest - - - 1 - Butantan 6 2 - - - Coeln 3 1 - 4 2 Cubana - 1 - - - Derby 437 534 370 441 183 Dublin 247 273 302 329 268 Durham 1 2 2 - - Eastbourne - - - - 4 Eboko - - 2 - - Enteritidis 92 4 45 30 50 Fresno - - - - 1 Give 22 10 20 64 11 Give var. 15+ 44 58 72 55 57 Gloucester - 1 - - - Goldcoast 2 1 - - - Hadar 24 24 26 44 39 Havana - 2 2 3 1 Hindmarsh - - 1 - - Idikan 7 2 2 13 17 Indiana 140 107 119 126 101 Infantis 2 7 9 2 2 Isangi - - - 1 - Istanbul - - - 1 -

23

Salmonella 2015 2016 2017 2018 2019 subspecies Javiana 2 - - - - Kedougou 231 242 211 203 409 Kentucky 1 2 3 1 1 Kingston 2 - - 2 4 Kottbus 12 17 50 31 22 Labadi - - 1 - - Lagos - - - - 1 Lexington - 9 27 6 2 Liverpool - 5 1 - - Livingstone 11 22 14 12 11 Lomita - 1 - - - London 3 1 3 - 3 Mapo - - - 1 - Mbandaka 345 245 317 514 451 Meleagridis - - 1 - - Minnesota - - 1 - - Mokola - - 5 1 - Monschaui 4 4 3 4 4 Montevideo 54 132 135 143 203 Muenchen - 1 - - 1 Muenster 1 2 - - - Nagoya - 1 1 - - Nchanga - - - 1 - Newport 38 26 9 24 23 Nima - - - - 1 Nottingham - - 1 9 13 Offa - - - - 1 Ohio 26 11 49 94 76 Oranienburg - - 1 - - Orion 30 37 31 50 19 Orion var. 15+ 27 37 23 50 51 Oslo 1 - 5 6 15 Othmarschen 1 - - - - Panama - 13 3 3 1 Paratyphi B var. Java 2 - 7 - - Poona - 1 - 2 - Pullorum 1 1 1 - - Reading 1 3 2 2 2 Rissen - - - 7 1 Rosslyn - - 2 - - Sandiego - - 1 - - Schwarzengrund 1 - - - - Senftenberg 91 159 260 84 120

24

Salmonella 2015 2016 2017 2018 2019 subspecies Soerenga - 1 - 7 - Stanley - - - 1 1 Stourbridge - - - 1 - Tennessee - - - - 2 Thompson - 1 - - - Typhimurium 70 83 123 170 124 Uganda - - - - 2 Urbana - - 1 - - Virchow 1 - 1 1 - Wangata - - - 2 - 4,5,12:i:- 54 58 50 55 43 4,12:i:- 58 38 52 55 58 13,23:i:- 189 188 179 681 436 ENTERICA DIARIZONAE 61:k:1,5 2 9 1 5 5 61:k:1,5,7 25 11 30 9 10 61:-:1,5 11 16 12 10 11 61:-:1,5,7 10 11 24 37 37 UNSPECIFIED untypable strains 39 30 35 70 52 rough strains 27 7 6 15 5 TOTAL 2450 2519 2736 3535 3046

† Poultry includes chickens, turkeys and ducks.

25

Figure 1.2: Isolations of the most common S. Typhimurium phage types (including monophasic strains) in livestock 2019

† One 4,12:i:- UNTY w as not mST by PCR

* Including both statutory and non-statutory data

UNTY27.9%

DT10426.5%

DT19320.6%

RDNC11.8%

DT22.9%

Other phage ty pes10.3%

Cattle (n=68)

DT19366.9%

U28817.3%

UNTY4.7%

U3023.9%

DT321.6%

DT1201.6% Other phage

ty pes3.9%

Pigs (n=127)

DT19331.8%

DT9918.2%

RDNC18.2%

UNTY†13.6%

Other phage ty pes18.2%

Chickens* (n=22)

U32040.0%

DT10420.0%

NOPT20.0%

UNTY20.0%

Sheep (n=5)

26

Figure 1.2: Isolations of the most common S. Typhimurium phage types (including monophasic strains) in livestock 2019 - continued

* Including both statutory and non-statutory data

UNTY100.0%

Ducks (n=2)

DT193100.0%

Turkeys* (n=2)

27

Figure 1.3: Isolations of the most common S. Enteritidis phage types in livestock 2019

* Including both statutory and non-statutory testing

There were no isolations of S . Enteritidis from sheep, turkeys or ducks during 2019

PT872.9%

PT13a16.7%

PT22.1%

PT42.1%

PT11b2.1%

PT132.1% UNTY

2.1%Chickens* (n=48)

NOPT100.0%

Cattle (n=1)

PT11100.0%

Pigs (n=1)

28

Figure 1.4: Isolations of S. Enteritidis in livestock in GB 2017 - 2019

0

10

20

30

40

50

60

2017 2018 2019

Num

ber

of is

olat

ions

Cattle Chickens* Ducks Pigs Sheep Turkeys*

* Inc. both statutory and non-statutory testing

29

Figure 1.5: Isolations of S. Typhimurium in livestock in GB 2017 – 2019

0

20

40

60

80

100

120

140

160

180

2017 2018 2019

Num

ber

of is

olat

ions

Cattle Chickens* Ducks Pigs Sheep Turkeys*

* Inc. both statutory and non-statutory testing

30

Figure 1.6: Isolations of S. 4,5,12:i:- in livestock in GB 2017 – 2019

0

10

20

30

40

50

60

2017 2018 2019

Num

ber

of is

olat

ions

Cattle Chickens* Ducks Pigs Sheep Turkeys*

* Inc. both statutory and non-statutory testing

31

Figure 1.7: Isolations of S. 4,12:i:- in livestock in GB 2017 – 2019

0

10

20

30

40

50

60

70

2017 2018 2019

Num

ber

of is

olat

ions

Cattle Chickens* Ducks Pigs Sheep Turkeys*

* Inc. both statutory and non-statutory testing

32

Chapter 2: Reports of Salmonella in Cattle The number of cattle on GB agricultural holdings continues to reduce slowly. As of June 2019, the number of cattle and calves recorded was 7,947,348 according to Defra figures. This is a reduction of 1.8% compared with June 2018 (8,091,222 animals) (Figure 2.1).

On the VIDA database there were 20,243 submissions recorded from cattle in 2019, which was a decrease of 6.7% compared with 2018 (21,606). There is no active monitoring for Salmonella in cattle in GB, with nearly all isolations being made from animals with clinical disease. The isolations are made by Government and private laboratories, the latter being required to forward isolates to Government laboratories for confirmation and further identification.

There was a total of 467 Salmonella isolations from cattle in 2019. This is a 5.3% decrease compared to 2018 (492 isolations) (Table 2.1). The four most commonly reported serovars were S. Dublin, S. Mbandaka, S. Typhimurium and S. Montevideo, which have been the most common serovars isolated from cattle every year since 2013. However, the number of S. Dublin isolations was 17.4% lower than in 2018 (261 isolations vs. 316 isolations), and isolations of S. Typhimurium and S. Montevideo also fell. In contrast, isolations of S. Mbandaka more than doubled in number compared to the previous year (78 isolations vs. 35 isolations), making it the second most common serovar to be isolated from cattle in 2019, and continuing the ongoing increase in herd infections in recent years, particularly in dairy herds.

Salmonella Dublin

The most common serovar isolated from cattle in GB was Salmonella Dublin for the 21st successive year. There were 261 isolations of S. Dublin, which is a reduction of 17.4% compared to the previous year (316 isolations). However, this serovar still represented 55.9% of the total of 467 Salmonella isolates from cattle (Figure 2.2). There was a similar seasonal trend to previous years, with a peak in S. Dublin isolations seen in the autumn (Figure 2.3), which probably reflects the tendency for many dairy herds to calve later in the year. However, in recent years this peak has reduced in size, being replaced instead by a broader distribution throughout the year. Alimentary tract disease was the most common presentation of clinical infection, with the majority of S. Dublin isolations arising from cases of enteritis, which were recorded in all ages of cattle. Salmonella Dublin was also isolated from cases of abortions in adult cattle.

Salmonella Typhimurium

There were 54 isolations of Salmonella Typhimurium from cattle in 2019, which is a 15.6% reduction compared to 2018 (64 isolations) and reverses an increasing trend seen in recent years (Table 2.2). As in previous years, DT104 was the most common phage type to be isolated, with a total of 18 isolations attributed to 14 incidents. This is similar to 2018 (17 isolations from 15 incidents).

33

The next most common S. Typhimurium phage ‘type’ was UNTY with 15 isolations, which is similar to 2018 (14 isolations). However, the number of S. Typhimurium UNTY incidents was 50% lower than in the previous year (4 incidents in 2019 vs. 9 incidents in 2018).

The number of S. Typhimurium RDNC isolations fell slightly compared to 2018 (8 vs. 13 in 2018) but was still relatively high compared to earlier years. This is likely, as with UNTY, to reflect the emergence of novel phage types that are not included in the current PHE phage-typing scheme. Such isolations are likely to increase in number over time, since the typing scheme is no longer updated by PHE, who now use sequence-based identification.

There was a single isolation of S. Typhimurium DT189 in 2019, which is the first record of this phage type in GB cattle; unfortunately no presenting signs were available. There was also a single isolation of S. Typhimurium DT204b, which was recorded from a case of enteritis; this serovar was last identified in GB cattle in 2002.

Salmonella Mbandaka

There was a considerable rise in the number of S. Mbandaka isolations in 2019 (78 vs. 35 isolations in 2018). The majority of isolates arising from clinical cases were from adult bovines with signs of enteritis. The reason for this increase is currently unclear, but there may be an association with feed contamination. Products such as soya bean meal, rapeseed products and palm kernel have previously been identified as sources according to existing literature, but S. Mbandaka has now become embedded in many dairy farms, so can also be spread by movements between farms.

Other serovars

Other principal Salmonella serovars isolated from cattle in 2019 were S. Montevideo (3.9% of isolations), Salmonella 4,12:i:- (1.5% of isolations) and Salmonella 4,5,12:i:- (1.5% of isolations) (Figure 2.2). There were seven isolations of Salmonella 4,12:i:- (DT193 (x6) and UNTY (x1); Figure 2.8) and seven isolations of Salmonella 4,5,12:i:- (DT193 (x4) and UNTY (x3); Figure 2.7), compared to seven and six, respectively, in 2018. There was also a single isolation of Salmonella Enteritidis (NOPT) from cattle in 2019, compared to three in 2018 (Figure 2.9).

In 2019, three Salmonella serovars were isolated from cattle for the first time in recent years; these were S. Nottingham which was last isolated from cattle in GB in 2008, S. Uganda which was last isolated from cattle in GB in 2005 and S. Infantis which was last isolated from cattle in GB in 2014. The isolations of S. Nottingham and S. Uganda were all from clinical disease but no presenting signs were available. The single incident of S. Infantis (2 isolations) was from cattle with a clinical history of enteritis, milk drop and abortion. Two further serovars were isolated in 2019 which had never been recorded in GB cattle before; these were S. Bardo and S. Lagos.

34

Reports of non-GB origin

In total there were five reports of Salmonella in cattle of non-GB origin in 2019. This included two reports of S. Dublin in cattle from the Republic of Ireland, one report of S. Dublin in cattle from Denmark, one report of S. Mbandaka in cattle from Germany and one report of S. Montevideo in cattle also originating in Germany. These reports are excluded from the tables and figures of this publication.

35

Figure 2.1: Cattle population and number of holdings with cattle in GB 2009- 2019

36

Table 2.1: Isolations and incidents of Salmonella in cattle on all premises in Great Britain

Salmonella 2015 2015 2016 2016 2017 2017 2018 2018 2019 2019subspecies Isolations Incidents Isolations Incidents Isolations Incidents Isolations Incidents Isolations IncidentsENTERICA ENTERICAAgama 7 6 - - 3 3 4 4 1 1Ajiobo 1 1 - - 1 1 - - - -Anatum 3 2 8 6 7 6 5 5 2 2Anatum var. 15+ 2 2 - - - - - - - -

Bardo - - - - - - - - 1 1Berta - - - - 1 1 - - 1 1Bovismorbificans - - 4 4 2 2 - - - -Branederup 1 1 - - - - - -Bredeney - - 1 1 - - - - - -Butantan 6 3 - - - - - - - -

Coeln 2 2 1 1 - - 4 3 - -

Dublin 238 214 257 226 291 238 316 271 261 223Durham - - 1 1 2 2 - - - -

Eboko - - - - 1 1 - - - -Enteritidis 2 1 - - 3 3 3 2 1 -

Infantis - - - - - - - - 2 1

Kedougou 2 2 - - - - - - - -Kentucky 1 1 - - - - - - - -Kingston 1 1 - - - - - - 2 1Kottbus 2 1 - - 1 1 1 1 3 3

Labadi - - - - 1 1 - - - -Lagos - - - - - - - - 1 1Lomita - - 1 1 - - - - - -

Mbandaka 54 48 38 37 28 24 35 28 78 59Mokola - - - - - - 1 1Montevideo 15 15 23 18 14 11 21 18 18 16Muenster 1 1 1 1 - - - - - -

Newport 5 5 3 3 3 3 4 4 6 6Nottingham - - - - - - - - 3 2

Oslo 1 1 - - - - 1 1 4 3Othmarschen 1 1 - - - - - - - -

.Rissen - - - - - - 1 1 - -

.Stourbridge - - - - - - 1 1 - -

Typhimurium 17 9 21 19 57 33 64 46 54 34

Uganda - - - - - - - - 1 1

Virchow - - - - 1 1 1 1 - -

37

Table 2.1: Isolations and incidents of Salmonella in cattle on all premises in Great Britain - continued

Salmonella 2015 2015 2016 2016 2017 2017 2018 2018 2019 2019subspecies Isolations Incidents Isolations Incidents Isolations Incidents Isolations Incidents Isolations IncidentsENTERICA ENTERICAWangata - - - - - - 1 1 - -

4,5,12:i:- 6 6 6 5 5 5 6 4 7 64,12:i:- 4 4 4 1 8 6 7 5 7 6

ENTERICA DIARIZONAE61:k:1,5,7 1 1 - - 4 4 - - 1 161:-:1,5,7 2 2 - - 3 3 2 2 1 161:k:1,5 - - 1 1 - - - - - -61:-:1,5 2 2 1 1 - - 1 - 1 1

UNSPECIFIEDuntypable strains 2 2 7 7 4 4 9 9 10 10rough strains 2 2 - - 2 2 4 4 1 1

TOTAL 381 336 378 333 442 355 492 412 467 381

38

Figure 2.2: Isolations of the most common serovars in cattle in GB 2015 – 2019

Dublin62.5%

Mbandaka14.2%

Ty phimurium4.5%

Montev ideo3.9%

Agama1.8%

Butantan1.6%

4,5,12:i:-1.6%

enterica diarizonae

61:k:1,5,(7) and v ariants

1.3%

Newport1.3% Other

serov ars7.3%

2015 (n=381)

Dublin68.0%

Mbandaka10.1%

Montev ideo6.1%

Ty phimuirum5.6%

Anatum2.1%

4,5,12:i:-1.6%

Bov is-morbif icans

1.1%

4,12:i:-1.1%

Newport0.8% Other

serov ars3.7%

2016 (n=378)

Dublin65.8%

Ty phimurium12.9%

Mbandaka6.3%

Montev ideo3.2%

4,12:i:-1.8%

Anatum1.6%

enterica diarizonae

61:k:1,5,(7) and v ariants

1.6%

4,5,12:i:-1.1% Other

serov ars5.7%

2017 (n=442)

Dublin64.2%

Ty phimurium13.0%

Mbandaka7.1%

Montev ideo4.3%

4,12:i:-1.4%

4,5,12:i:-1.2%

Anatum1.0%

Other serov ars

7.7%

2018 (n=492)

Dublin55.9%

Mbandaka16.7%

Ty phimurium11.6%

Montev ideo3.9%

4,12:i:-1.5%

4,5,12:i:-1.5%

Newport1.3% Other

serov ars7.7%

2019 (n=467)

39

Figure 2.3: Seasonality of Salmonella Dublin in cattle in Great Britain 2015 - 2019

40

Figure 2.4: S. Dublin, S. Enteritidis, S. Typhimurium and Salmonella 4,(5),12:i:- as a proportion of all isolations in cattle in Great Britain 1999 – 2019

41

Table 2.2: Isolations and incidents of S. Typhimurium in cattle on all premises in Great Britain

2015 2015 2016 2016 2017 2017 2018 2018 2019 2019Isolations Incidents Isolations Incidents Isolations Incidents Isolations Incidents Isolations Incidents

1 1 1 - - - - - - - -2 - - - - - - 1 1 2 212 - - 3 3 - - 5 3 - -19 - - - - - - 1 1 - -41 - - 1 1 - - 1 1 - -46a - - - - 2 2 - - - -104 6 5 10 8 41 24 17 15 18 14189 - - - - - - - - 1 1193 1 1 3 3 2 1 2 2 4 4204b - - - - - - - - 1 1

U302 2 2 3 3 4 2 8 8 1 1

NOPT 7 - - - 2 - 2 - 4 -RDNC - - - - 2 - 13 6 8 7UNTY - - 1 1 4 4 14 9 15 4

TOTAL 17 9 21 19 57 33 64 46 54 34

Phage Types

42

Figure 2.5: Top phage types of S. Typhimurium in cattle in GB 2015 - 2019

43

Figure 2.6: Salmonella Typhimurium DT104 and related strains as a proportion of all isolations of Salmonella Typhimurium and Salmonella 4,(5),12:i:- in cattle in Great Britain 1999 - 2018

44

Figure 2.7: Salmonella 4,5,12:i:- phage types in cattle in GB 2015 - 2019

45

Figure 2.8: Salmonella 4,12:i:- phage types in cattle in GB 2015 – 2019

46

Figure 2.9: S. Enteritidis phage types in cattle in GB 2015 – 2019

47

Chapter 3: Reports of Salmonella in sheep and goats

Sheep There was a small fall in the total GB sheep numbers from 31.77 million in 2018 to 31.59 million in 2019. The 2017 sheep numbers (32.77 million) were the highest recorded since 2008, after numbers had declined from 31.82 million sheep in 2014, to a low of 27.88 million in 2016.

There were 5,151 GB ovine diagnostic submissions in 2019 compared to 6,142 in 2018, a marked fall of 16.1%, continuing a decreasing trend in diagnostic submissions since 2012. It is not clear if this large reduction in submissions may have followed the sheep-related human cases in 2018 and 2019 and associated requirement for Food Chain Information (FCI) declarations.

There were 103 Salmonella isolations from sheep in 2019, which is 6.4% fewer than in 2018 and 2017 (both 110 isolations). However, the number of Salmonella isolations relative to the total number of diagnostic submissions received for all reasons was comparable to the previous year (2.0% in 2019 vs. 1.8% in 2018).

As in all previous years since 2008, the most common Salmonella serovar to be isolated from sheep in 2019 was Salmonella enterica subspecies diarizonae 61:k:1,5(,7) (including associated incompletely typable strains). This was isolated 59 times in 2019, which is similar to the number in 2018 (58 isolations) and 2017 (60 isolations) (Table 3.1). Since 2008 annual isolations of this serovar have ranged widely from 37 to 109. The next most common serovars isolated were S. Montevideo (16 isolations) and S. Dublin (6 isolations), with the number of isolations of each falling within the typical range seen for these serovars since 2008 (typically between four and 36 per year for S. Montevideo and between seven and 17 per year for S. Dublin). Together, these three serovars accounted for approximately 80% of isolations from sheep in 2019 (Table 3.1; Figure 3.2). In contrast to recent years, the number of S. Typhimurium isolations from sheep was relatively low (4 isolations), falling by approximately three-quarters compared to 2018 (15 isolations) and 2017 (16 isolations).

Salmonella enterica subspecies diarizonae

Salmonella enterica subspecies diarizonae serovar 61:k:1,5,(7) (and associated incompletely typable strains) is typically the most common Salmonella serovar reported from sheep, and it contributed to 57.3% of the total number of isolates obtained from sheep samples during 2019 (Figure 3.2). Since 2008, 36.6% to 75.0% of the annual sheep Salmonella isolations have been Salmonella enterica subspecies diarizonae. Abortion was the most frequently described presenting sign in 2019, followed by diarrhoea, and infection is often identified in combination with other diagnoses. This organism is usually considered

48

an incidental finding in healthy sheep, but can be of potential significance when isolated from sheep with concurrent disease, especially chronic rhinitis.

Salmonella Montevideo

Salmonella Montevideo was the second most common serovar isolated from sheep in 2019, (16 isolations; an increase compared to the ten isolations in 2018) and accounting for 15.5% of the total Salmonella isolations this year (Figure 3.2). This serovar has typically represented between 11.9% and 32.1% of the Salmonella isolations from sheep each year since 2008, although it accounted for a slightly lower proportion of isolations in 2018 (9.1%). Salmonella Montevideo is typically associated with abortions in sheep, without other signs of illness in the ewe. It is considered endemic in sheep in GB and is also a regular contaminant of animal feed.

Salmonella Dublin

Salmonella Dublin was the third most common serovar isolated from sheep in 2019. This serovar is typically one of the three most common serovars isolated from sheep each year; this remained the case in 2019, although there were just six isolations, representing 5.8% of total Salmonella isolations (Figure 3.2). The diagnosis of S. Dublin was predominantly associated with abortions during 2019, with other less frequently described signs including “found dead” and diarrhoea.

Salmonella Typhimurium

There were four Salmonella Typhimurium isolations in sheep during 2019 representing 3.9% of Salmonella isolations (Figure 3.2). This is a considerable reduction compared to the unusually high numbers seen in 2018 (15 isolations), 2017 (16 isolations) and 2016 (11 isolations), and a return to the low number of annual S. Typhimurium isolations typically seen prior to this. Diarrhoea is most frequently described in diagnosed cases, often in combination with “found dead” and malaise.

Three of the four S. Typhimurium isolates from sheep in 2019 were phage-typable. There were two isolations (from one incident) of S. Typhimurium U320 – a phage type not previously recorded in sheep in GB (Figure 3.4). The presenting sign for these isolations was “found dead”. In addition there was one isolation of S. Typhimurium DT104. This phage type is generally considered to be the most common S. Typhimurium phage type found in sheep, and has been isolated each year since 2016. However, the number of isolations in 2019 was considerably lower compared to 2018 (6 isolations), 2017 (7 isolations) and 2016 (6 isolations).

One isolate of S. Typhimurium from sheep was classed as UNTY in 2019, indicating that it did not react with any of the phages in the current typing system.

49

There was also a single isolation of monophasic Salmonella 4,12:i:- in sheep in 2019, which was not phage typed (NOPT). This compares to a single isolation of monophasic Salmonella Typhimurium 4,12:i:- DT193 in 2018 (Figure 3.6).

Salmonella Agama

There were four isolations of S. Agama from sheep during 2019, which represented 3.9% of Salmonella isolations (Figure 3.2). While this is double the number of isolations compared to 2018 (2 isolations), it is in keeping with the number of S. Agama isolations from sheep each year since 2010, which has typically ranged between two and ten. Salmonella Agama predominantly presents with abortions in sheep, with variable other signs in a few cases such as “found dead”, diarrhoea, malaise and recumbency.

Other Serovars

There was a single isolation of S. Mbandaka during 2019. The presenting sign was ‘found dead’, and S. Mbandaka septicaemia was diagnosed. This serovar was also isolated once from sheep in 2018, but prior to that had not been recorded in GB sheep since 2010, although it is regularly isolated from GB cattle. There was also one isolation of S. Newport (fully sensitive to all the antimicrobials tested against) from sheep in 2019, for which no presenting signs were available. This serovar, which is often associated with badgers, like S. Agama, has not been isolated from GB sheep since 2015. Salmonella Kingston was also isolated from sheep on one occasion in 2019. This serovar has never been recorded in GB sheep before, and the presenting signs were not available.

Goats The GB goat population has steadily increased from 98,000 in 2013 to 108,819 in 2019.

However, diagnostic submissions from goats fell by 7.9% in 2019 (419 submissions) compared to 2018 (455 submissions), which continues a decreasing trend in the number of submissions seen in recent years.

There was one isolation of Salmonella reported from goats during 2019. The serovar isolated was Salmonella 16:z10:e,n,x,z15 and was from clinical disease (no presenting signs were available). Salmonella is infrequently isolated from goats, with the most recent cases prior to this being single isolations of S. Coeln in 2016, S. Anatum in 2014 and S. Dublin in 2010.

50

Figure 3.1: Sheep population and number of holdings with sheep in GB 2010- 2019

51

Table 3.1: Isolations and incidents of Salmonella in sheep on all premises in Great Britain

Salmonella 2015 2015 2016 2016 2017 2017 2018 2018 2019 2019subspecies Isolations Incidents Isolations Incidents Isolations Incidents Isolations Incidents Isolations IncidentsENTERICA ENTERICAAgama 2 2 7 5 3 2 2 2 4 4

Dublin 7 7 17 12 9 9 13 13 6 6

Eboko - - - - 1 1 - - - -

Indiana 1 1 - - - - - - - -

Kingston - - - - - - - - 1 1

Mbandaka - - - - - - 1 1 1 1Minnesota - - - - 1 1 - - - -Montevideo 8 7 15 14 16 12 10 9 16 13

Newport 2 2 - - - - - - 1 1

Panama - - 5 4 - - - - - -

Typhimurium - - 11 9 16 10 15 7 4 2

Urbana - - - - 1 1 - - - -

4,5,12:i:- 1 1 - - - - - - - -4,12:i:- 2 2 1 1 - - 1 1 1 1

ENTERICA DIARIZONAE61:k:1,5 2 2 8 8 1 1 5 4 5 461:k:1,5,7 24 24 11 11 26 25 9 9 9 961:-:1,5 9 8 15 15 12 11 9 7 10 761:-:1,5,7 8 8 11 11 21 21 35 31 35 31

UNSPECIFIEDuntypable strains - - 7 7 3 3 9 9 10 10rough strains - - - - - - 1 1 - -

TOTAL 66 64 108 97 110 97 110 94 103 90

52

Table 3.2: Isolations and incidents of Salmonella in goats on all premises in Great Britain

Salmonella 2015 2015 2016 2016 2017 2017 2018 2018 2019 2019subspecies Isolations Incidents Isolations Incidents Isolations Incidents Isolations Incidents Isolations IncidentsENTERICA ENTERICACoeln - - 1 1 - - - - - -

UNSPECIFIEDuntypable strains - - - - - - 1 1

TOTAL - - 1 1 - - - - 1 1

53

Figure 3.2: Isolations of the most common serovars in sheep in GB 2015 – 2019

enterica diarizonae

61:k:1,5,(7) and v ariants

65.2%

Montev ideo12.1%

Dublin10.6%

Agama3.0%

Newport3.0%

4,12:i:-3.0%

Other serov ars

3.0%2015 (n=66)

enterica diarizonae

61:k:1,5,(7) and v ariants

41.7%

Dublin15.7%

Montev ideo13.9%

Ty phimurium10.2%

Agama6.5%

Panama4.6%

Other serov ars

7.4%

2016 (n=108)

enterica diarizonae

61:k:1,5,(7) and v ariants

54.5%Montev ideo

14.5%

Ty phimurium14.5%

Dublin8.2%

Agama2.7%

Other serov ars

5.5%2017 (n=110)

enterica diarizonae

61:k:1,5,(7) and v ariants

52.7%Ty phimurium

13.6%

Dublin11.8%

Montev ideo9.1%

Agama1.8%

Other serov ars

10.9%2018 (n=110)

enterica diarizonae

61:k:1,5,(7) and v ariants

57.3%

Montev ideo15.5%

Dublin5.8%

Agama3.9%

Ty phimurium3.9%

Other serov ars

13.6%2019 (n=103)

54

Figure 3.3: S. Dublin, S. enterica diarizonae, S. Enteritidis, S. Montevideo, S. Typhimurium and Salmonella 4,(5),12:i:- as a proportion of all isolations in sheep in Great Britain 1999 - 2019

55

Figure 3.4: S. Typhimurium phage types in sheep in GB 2015 - 2019

56

Figure 3.5: Salmonella 4,5,12:i:- phage types in sheep in GB 2015 – 2019

57

Figure 3.6: Salmonella 4,12:i:- phage types in sheep in GB 2015 – 2019

58

Chapter 4: Reports of Salmonella in pigs There was a small increase in the total GB pig herd in 2019 to 4.40 million from 4.38 million in 2018, compared with 4.32 million in 2017 and 4.27 million in 2016. (Figure 4.1)

There remains no current national scheme for monitoring Salmonella levels on pig farms in GB since the withdrawal of meat juice ELISA testing of slaughter pigs in 2012. Isolates reported to APHA largely result from clinical investigations, but Salmonella infection in pigs is largely subclinical.

There was an increase (14.4%) in total pig submissions to APHA/ SRUC during 2019 to 2,818 from 2,464 in 2018. There was also an increase (12.2%) in diagnostic pig submissions to 1,290 from 1,150 in 2018. The increase in the pig sector submissions did not follow the decreasing trend in total submissions of all farmed species to APHA/ SRUC, which fell by 4.21% compared with 2018.

There were 167 isolations of Salmonella from pigs in 2019. This is very similar to the number of isolations in 2018 (169 isolations). The serovars isolated are detailed in Table 4.1 and Figure 4.2.

Salmonella Typhimurium and monophasic S. Typhimurium 4,(5),12:i:-

Isolations of S. Typhimurium and its monophasic variants together accounted for the majority of isolations of Salmonella from pigs in 2019 (Figure 4.2). This is consistent with previous years, but the overall proportion of pig isolations falling into this category has decreased recently (76.0% in 2019 compared to 79.9% in 2018 and 86.3% in 2017) as isolations of other serovars have increased in frequency.

As in previous years, the most common serovar isolated from pigs in 2019 was S. Typhimurium (50 isolations). However, there was a decrease of 23.1% in the number of S. Typhimurium isolations compared with 2018 (65 isolations). Phage type U288, which is particularly associated with pigs, was the most commonly isolated phage type of S. Typhimurium in 2019 (22 isolations), followed by DT193 (17 isolations). Other S. Typhimurium phage types isolated were U302 (4 isolations), DT32 (2 isolations) and DT104 (1 isolation). Two S. Typhimurium isolates were not phage typed, and two isolates did not conform to any phage types in the current typing scheme (Table 4.2; Figure 4.5).

After S. Typhimurium, the next most common Salmonella serovar isolated from pigs in 2019 was monophasic Salmonella 4,12:i:- (47 isolations). Isolations of this serovar increased by 27.0% compared to 2018 (37 isolations), and almost matched the number of S. Typhimurium isolations in 2019. The majority of these isolates (85.1%) were phage type DT193, which represents the ‘epidemic’ type that has emerged in Europe since 2006, and has dominated amongst monophasic strains of S. Typhimurium in GB pigs since then. There were also two isolations of DT120, one isolation of U302 and the remaining three

59

isolates were not typable against the current phage-typing scheme (UNTY) and one not phage-typed (NOPT) (Figure 4.7).

As in 2018, the third most common serovar isolated from pigs in 2019 was monophasic Salmonella 4,5,12:i:- (30 isolations), although there was a 9.1% decrease in the number of isolations compared to the previous year (33 isolations in 2018). All typable isolates were confirmed as phage type DT193 (28 isolations) and two further isolates were not typable (UNTY) (Figure 4.6).

Other serovars

After S. Typhimurium and its monophasic variants, the next most frequently isolated serovar from pigs in 2019 was S. Bovismorbificans. This was isolated twelve times (7.2 % of all pig isolations), which is more than double the number of isolations compared to the previous year (5 isolations). There was also a large increase in isolations of S. Kedougou compared to previous years; having only been isolated once or twice per year since 2015, this serovar was isolated eight times in 2019 (4.8% of all pig isolations). Salmonella Newport was isolated six times in 2019, which is a slight increase compared to 2018 (4 isolations) and 2017 (no isolations). In contrast, isolations of S. Derby decreased by 50% in 2019 compared to 2018 (6 vs. 12 isolations), although they matched the figure for 2017. Salmonella Panama and S. Reading were each isolated once, which is also a slight decline compared to previous years (see Table 4.1).

Salmonella Uganda was isolated from pigs in 2019 having never previously been recorded from GB pigs (1 isolation). In addition, there was one isolation of S. Enteritidis PT11, which is a phage type of S. Enteritidis that has never before been isolated from GB pigs, and is typically associated with hedgehogs. Furthermore, this is the first time since 2008 that S. Enteritidis of any phage type has been isolated from GB pigs. There was also one isolation of S. Livingstone, which was last recorded in GB pigs in 2006.

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Figure 4.1: Pig population and number of holdings with pigs in GB 2010 - 2019

61

Table 4.1: Isolations and incidents of Salmonella in pigs on all premises in Great Britain

Salmonella 2015 2015 2016 2016 2017 2017 2018 2018 2019 2019subspecies Isolations Incidents Isolations Incidents Isolations Incidents Isolations Incidents Isolations IncidentsENTERICA ENTERICAAgama - - - - 1 1 - - - -

Bardo - - 1 1 1 1 1 1 - -Bovismorbificans 2 2 2 2 1 1 5 3 12 10

Derby 7 6 9 9 6 6 12 12 6 5

Enteritidis - - - - - - - - 1 1

Kedougou 1 1 2 2 1 1 1 - 8 8

Livingstone - - - - - - - - 1 1London 3 2 1 1 3 3 - - 1 1

Muenchen - - 1 1 - - - - - -

Nchanga - - - - - - 1 1 - -Newport 1 1 4 4 - - 4 3 6 6

Panama - - 3 3 3 3 3 3 1 1

Reading 1 1 3 3 2 2 2 2 1 1Rissen - - - - - - 3 2 - -

Sandiego - - - - 1 1 - - - -

Typhimurium 42 36 43 40 41 38 65 47 50 47

Uganda - - - - - - - - 1 1

4,5,12:i:- 39 39 47 44 41 37 33 28 30 274,12:i:- 49* 47 30 29 38 37 37* 28 47 45

UNSPECIFIEDuntypable strains - - - - - - 2 1 2 2

TOTAL 145 135 146 139 139 131 169 131 167 156

* One isolation (U302) not confirmed as monophasic S . Typhimurium by PCR in 2015 and four isolations (UNTY)not confirmed as monophasic S . Typhimuirum nby PCR in 2018

62

Figure 4.2: Isolations of the most common serovars in pigs in GB 2015 – 2019

4,12:i:-33.8%

Ty phimurium29.0%

4,5,12:i:-26.9%

Derby4.8%

London2.1%

Bov is-morbif icans

1.4%Other

serov ars2.1%

2015 (n=145)

4,5,12:i:-32.2%

Ty phimurium29.5%

4,12:i:-20.5%

Derby6.2%

Newport2.7%

Panama2.1%

Reading2.1%

Other serov ars

4.8%

2016 (n=146)

Ty phimurium29.5%

4,5,12:i:-29.5%

4,12:i:-27.3%

Derby4.3%

London2.2%

Panama2.2%

Reading1.4%

Other serov ars

3.6%

2017 (n=139)

Ty phimurium38.5%

4,12:i:-21.9%

4,5,12:i:-19.5%

Derby7.1%

Bov is-morbif icans

3.0%

Newport2.4%

Panama1.8%

Rissen1.8%

Other serov ars

4.1%

2018 (n=169)

Ty phimurium29.9%

4,12:i:-28.1%

4,5,12:i:-18.0%

Bov is-morbif icans

7.2%

Kedougou4.8%

Derby3.6%

Newport3.6%

Other serov ars

4.8%

2019 (n=167)

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Figure 4.3: S. Derby, S. Enteritidis, S. Typhimurium and Salmonella 4,(5),12:i: as a proportion of all isolations in pigs in Great Britain 1999 - 2019

64

Table 4.2: Isolations and incidents of S. Typhimurium in pigs on all premises in Great Britain

2015 2015 2016 2016 2017 2017 2018 2018 2019 2019Isolations Incidents Isolations Incidents Isolations Incidents Isolations Incidents Isolations Incidents

32 - - - - - - 2 2 2 2104 1 1 1 1 1 1 1 1 1 1193 7 6 6 6 11 11 18 17 17 17195 1 1 - - - - - - - -

U288 22 22 25 25 24 24 28 20 22 21U302 6 4 6 6 - - 5 5 4 4U308 2 2 - - - - - - - -U311 - - - - 1 1 - - - -

NOPT 3 - 3 - 3 - 8 - 2 -RDNC - - - - - - - - 1 1UNTY - - 2 2 1 1 3 2 1 1

TOTAL 42 36 43 40 41 38 65 47 50 47

Phage Types

65

Figure 4.4: Isolations of Salmonella Typhimurium phage types in pigs in Great Britain 2015 – 2019

66

Figure 4.5: Top phage types of S. Typhimurium in pigs in GB 2015 - 2019

67

Figure 4.6: Salmonella 4,5,12:i:- phage types in pigs in GB 2015 - 2019

68

Figure 4.7: Salmonella 4,12:i:- phage types in pigs in GB 2015 - 2019

69

Chapter 5: Reports of Salmonella in deer, horses and rabbits Isolations of Salmonella from deer, horses and rabbits are reportable as these species may be reared for human consumption.

Deer

There were 36,142 farmed deer registered in Great Britain at the June 2019 Agricultural Census, which was an increase of 14.4% compared with 2018 (31,583 animals). There were two isolations of Salmonella from deer during 2019 compared with one isolation during 2018 and no isolations during 2017 (Table 5.1). The serovars reported were single isolations of S. Montevideo and Salmonella Typhimurium 4,5,12:i:- NOPT; both reports were from clinical disease. The report of S. Montevideo was from an adult animal presenting with wasting and diarrhoea, however the presenting signs and age were not available for the report of Salmonella 4,5,12:i:-. Neither S. Montevideo nor Salmonella 4,5,12:i:- have previously been reported from deer in GB.

Rabbits

There were no isolations of Salmonella from rabbits during 2019, the same as during 2018 and 2017 (Table 5.2). The last isolation from rabbits was in 2016 (Salmonella 21:g,t:-) and prior to that there was a single isolation in 2012 (S. Monschaui).

Horses

The number of horses recorded as being kept in Great Britain at the June 2019 Agricultural Census was 241,520, which is a slight increase (359 animals) compared to 2018 (241,161 animals).

There were 126 isolations of Salmonella from horses in 2019, which is almost six times more than during 2018 (22 isolations) and just over three times more than during 2017 (39 isolations) (Table 5.3). This is the highest number of isolations reported since Salmonella in horses became reportable in 1989; the previous highest number was during 2007 when 67 isolations were reported. Some of these reports relate to increased monitoring in veterinary hospitals and rescue centres.

The most commonly reported serovars from horses during 2019 were S. Typhimurium (34 isolations; 27.0% of total horse isolations), S. Oslo (23 isolations; 18.3% of total horse isolations) and S. Bovismorbificans (19 isolations; 15.1% of total horse isolations). In contrast, during 2018 the most commonly reported serovars were S. Typhimurium and S. Bovismorbificans (both 7 isolations; 33.3% of total isolations) followed by S. Anatum and S. Newport (both 2 isolations; 9.5% of total isolations). The number of isolations of S. Typhimurium during 2019 was just over four times the number of isolations in 2018 (8

70

isolations) and almost three time that in 2017 (13 isolations). There were also 18 isolations of monophasic variants of Salmonella Typhimurium in 2019, including 12 isolations of Salmonella 4,12:i:- (all DT193) and six isolations of Salmonella 4,5,12:i:- (all DT193). This compares with no isolations of either of these monophasic variants during 2018 and only five in total during 2017 (Table 5.3).

Horses are considered to be a common reservoir of S. Typhimurium. The 34 isolations of S. Typhimurium reported from horses during 2019 comprised nine different phage types (excluding UNTY and RDNC) (Table 5.4 and Figure 5.3). The most common phage type reported was U302 with six isolations, followed by DT40 and DT193 which were each isolated four times. There was also a single isolation of S. Typhimurium DT135, which was last reported from horses in GB in 2010, and two isolations of S. Typhimurium U188, which has never previously been reported from horses in GB. The isolations of DT135 and U188 all arose from clinical disease cases for which no presenting signs were available.

Salmonella Oslo was the second most common serovar to be isolated from horses in 2019. There were 23 isolations of S. Oslo attributed to seven incidents, which is considerably more than when it was last isolated in 2016 (2 isolations from 2 incidents). This serovar has been associated with equine hospitals and rescue centres, which may act as a focus of contamination. There was also an almost three-fold increase in the number of S. Bovismorbificans isolations from horses in 2019 compared to 2018 (19 vs. 7 isolations). This serovar is mainly associated with pigs, and isolations from pigs were also higher in 2019 compared to previous years.

The number of S. Newport isolations from horses in 2019 was six-fold higher than during 2018 (12 vs. 2 isolations); all isolations resulted from clinical disease investigations. Most of the isolates (10/12) were fully susceptible to all the antimicrobials tested against, but one was resistant to ampicillin and the other was resistant to tetracycline. In some parts of the country, S. Newport can be associated with badgers.

There were five isolations of S. Enteritidis in 2019, which is more than in each of the proceeding three years (1 isolation in both 2018 and 2017 and 2 isolations in 2016). The phage types were PT13a (x3), PT11 (x1), and PT21 (x1) (Figure 5.6); all resulted from clinical disease. Phage type PT21 has never previously been reported from horses in GB. As with cattle, the phage types of S. Enteritidis found in horses are often a closer match with human strains than with those identified from British poultry.

There was also a single isolation of S. Hessarek and five isolations of S. Kingston from horses in 2019; neither of these serovars has previously been reported from horses in GB. All of these isolations were the result of clinical disease investigations, but the associated clinical signs were not available.

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Table 5.1: Isolations and incidents of Salmonella in deer on all premises in Great Britain

Table 5.2: Isolations and incidents of Salmonella in rabbits on all premises in Great Britain

Salmonella 2015 2015 2016 2016 2017 2017 2018 2018 2019 2019subspecies Isolations Incidents Isolations Incidents Isolations Incidents Isolations Incidents Isolations IncidentsENTERICA ENTERICADublin - - - - - - 1 1

Montevideo - - - - - - - - 1 1

Newport - - 1 1 - - - - - -

4,5,12:i:- - - - - - - - - 1 1

UNSPECIFIEDrough strains - - 1 1 - - - - - -

TOTAL - - 2 2 - - 1 1 2 2

Salmonella 2015 2015 2016 2016 2017 2017 2018 2018 2019 2019subspecies Isolations Incidents Isolations Incidents Isolations Incidents Isolations Incidents Isolations IncidentsENTERICA ENTERICA21:g,t:- - - 1 1 - - - - - -

TOTAL - - 1 1 - - - - - -

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Table 5.3: Isolations and incidents of Salmonella in horses on all premises in Great Britain

Salmonella 2015 2015 2016 2016 2017 2017 2018 2018 2019 2019subspecies Isolations Incidents Isolations Incidents Isolations Incidents Isolations Incidents Isolations IncidentsENTERICA ENTERICAAgama 3 3 7 7 6 5 - - 1 1Ajiobo - - 2 2 - - - - - -Anatum 2 2 - - - - 2 2 - -Ank 2 2 - - - - - - - -

Bovismorbificans - - 2 2 - - 7 6 19 11Braenderup - - - - 1 1 - - - -

Coeln - - - - 1 1 - - 2 2

Dublin - - - - - - - - 1 1Durham - - - - 1 1 - - - -

Enteritidis 8 8 2 2 1 1 1 1 5 5

Hadar - - - - 1 1 - - - -Hessarek - - - - - - - - 1 1

Infantis - - - - 3 2 - - - -

Kingston - - - - - - - - 5 4Kottbus - - 2 2 - - - - - -

London - - - - - - 1 1 - -

Mbandaka - - - - - - - - 3 2Montevideo 1 1 - - - - - - - -

Newport 5 5 7 7 2 2 2 2 12 8

Oslo - - 2 2 - - - - 23 7

Paratyphi B var. Java - - - - 2 2 - - - -

Teddington - - - - 2 2 - - - -Typhimurium 17 15 17 11 13 10 8 5 34 23

4,5,12:i:- 5 5 5 4 2 2 - - 6 14,12:i:- 3 3 1 1 3 3 - - 12 7

UNSPECIFIEDuntypable strains 1 1 1 1 1 1 1 1 2 2

TOTAL 47 45 48 41 39 34 22 18 126 75

73

Figure 5.1: Isolations of the most common serovars in horses in GB 2015 – 2019

Ty phimurium36.2%

Enteritidis17.0%

Newport10.6%

4,5,12:i:-10.6%

Agama6.4%

4,12:i:-6.4%

Anatum4.3%

Ank4.3%

Other serov ars

4.3%2015 (n=47)

Ty phimurium35.4%

Agama14.6%

Newport14.6%

4,5,12:i:-10.4%

Ajiobo4.2%

Bov is-morbif icans

4.2%

Enteritidis4.2%

Kottbus4.2%

Oslo4.2%

Other serov ars

4.2%

2016 (n=48)

Ty phimurium33.3%

Agama15.4%

Inf antis7.7%

4,12:i:-7.7%

Newport5.1%

Paraty phi B v ar. Jav a

5.1%

Teddington5.1%

4,5,12:i:-5.1%

Other serov ars

15.4%2017 (n=39)

Ty phimurium36.4%

Bov is-morbif icans

31.8%

Anatum9.1%

Newport9.1%

Other serov ars

13.6%

2018 (n=22)

Ty phimurium27.0%

Oslo18.3%Bov is-

morbif icans15.1%

Newport9.5%

4,12:i:-9.5%

Other serov ars

20.6%

2019 (n=126)

74

Figure 5.2: S. Enteritidis, S. Newport, S. Typhimurium and Salmonella 4,(5),12:i:- as a proportion of all isolations in horses in Great Britain 1999 - 2019

75

Table 5.4: Isolations and incidents of S. Typhimurium in horses on all premises in Great Britain

2015 2015 2016 2016 2017 2017 2018 2018 2019 2019Isolations Incidents Isolations Incidents Isolations Incidents Isolations Incidents Isolations Incidents

1 1 1 3 3 - - - - 2 18 - - 1 1 - - - - 3 312 - - - - 1 1 1 1 - -40 - - - - 2 2 - - 4 241 3 3 - - 2 2 1 1 3 356 1 1 1 1 - - - - - -66a 1 1 - - - - - - - -104 - - 4 3 2 2 - - 3 3132 1 1 - - - - - - - -135 - - - - - - - - 1 1193 5 4 2 2 1 1 - - 4 2195 1 1 - - - - - - - -

U188 - - - - - - - - 2 2U302 2 2 - - 1 1 - - 6 3U310 1 1 - - - - - - - -U320 - - - - - - 1 1 - -U323 - - 2 1 - - - - - -

UNTY - - - - 1 1 1 1 1 1NOPT - - 1 - - - - - - -RDNC 1 - 3 - 3 - 4 1 5 2

TOTAL 17 15 17 11 13 10 8 5 34 23

Phage Types

76

Figure 5.3 Top phage types of S. Typhimurium in horses in GB 2015 - 2019

77

Figure 5.4: Salmonella 4,5,12:i:- phage types in horses in GB 2015 - 2019

78

Figure 5.5: Salmonella 4,12:i:- phage types in horses in GB 2015 - 2019

79

Figure 5.6: S. Enteritidis phage types in horses in GB 2015 - 2019

80

Chapter 6: Reports of Salmonella in chickens According to the June Agricultural Census, the total number of chickens held in Great Britain was 151.8 in 2019, comprising approximately 45.7million breeding and laying hens, and 106.1 million broiler chickens (Figure 6.1). This is similar to 2018 when there were 152.4 million chickens.

Two different systems of reporting are used in this chapter, which should be taken into account when interpreting the results.

• The first part of this chapter describes isolations of Salmonella, including samples originating from statutory surveillance, voluntary surveillance, investigations into clinical disease and investigations carried out under the Zoonoses Order. If two submissions from the same group of animals on different dates give the same serovar, this is reported as two isolations.

• The second part of this chapter describes results obtained within the National Control Programmes (NCPs) i.e. results from statutory surveillance. The Salmonella serovars considered to be of public health significance under EU regulations (the regulated serovars) form a very small proportion of the total isolations reported. Results from the NCPs are reported to the European Commission in a way that ensures that every flock with a Salmonella-positive result is counted only once. Numbers of positive flocks reported within the NCP are, therefore, expected to differ from the number of reported isolations. For example, some flocks may be positive for more than one serovar, in which case they are still only counted once as positive flocks for the NCP. This also applies if there is a long interval between positive tests from the same flock.

There was a total of 5,549 chicken diagnostic and monitoring submissions received by APHA and SRUC laboratories in 2019. This was an increase of 1.5% compared to 2018. However, APHA does not have information on the number of non-statutory submissions submitted to private laboratories that do not result in a positive culture of Salmonella, as these are not reportable under the Zoonoses Order.

There were 1,749 isolations of Salmonella from chickens in 2019 (Table 6.1), which represents a slight decrease by 4.8% compared with 2018 (1,838 isolations). This follows a substantial increase of 59.3% reported in 2018, which was primarily in the broiler sector and possibly partly linked to the ban on the use of formaldehyde-based products in animal feed production across the European Union since January 2018.

As previously described, the total number of isolations includes samples from statutory surveillance, voluntary surveillance, diagnostic submissions and investigations of clinical disease. It should, however, be noted that there is substantial statutory surveillance of Salmonella in chickens and turkeys, unlike in all other food animal species.

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The total number of isolations in 2019 was distributed among the following categories according to the reason for submission:

• Statutory surveillance: 1,459 (83.4%)

• Voluntary surveillance: 290 (16.6%)

The percentage of Salmonella isolations reported through statutory surveillance in 2019 (83.4% of total chicken isolations) was higher than during 2018 (74.5% of total chicken isolations).

Forty-one different Salmonella serovars were isolated in 2019, accounting for 1,729 of the 1,749 isolations. Twenty isolations involved untypable Salmonella cultures (including one rough strain). Table 6.1 shows all of the Salmonella serovars isolated from chickens between 2015 and 2019; Figure 6.2 shows the relative percentages of the most common serovars isolated from chickens between 2015 and 2019.

The top eight serovars to be isolated from chickens in 2019 were the same as in 2018 (Figure 6.2). In 2019, for the second time, the most common Salmonella serovar isolated from chickens was Salmonella 13,23:i:-. This serovar was first isolated in broiler chickens during 2009, when it was isolated just once. Salmonella 13,23:i:- was subsequently isolated 132 times in 2013 (10.9% of all isolations) and has remained one of the most commonly isolated serovars from chickens ever since, consistently amounting to more than one hundred isolates each year. However, there was a dramatic rise in Salmonella 13,23:i:- isolations in 2018, with more than a three-fold increase compared to 2017 (681 vs. 179 isolations in 2017). In 2019, the number of isolations dropped to 436, but this is still more than double the number of isolations in 2017. There is increasing evidence that Salmonella 13,23:i:- strains represent a monophasic variant of S. Idikan with a mutation that prevents expression of the phase 2 flagella antigens. This serovar is associated with contaminated feed mills and can also become established and persistent in hatcheries and on poultry farms.

Prior to 2018, S. Mbandaka, which is thought to be largely feed-related, had been the most common serovar isolated from chickens for several years. The number of S. Mbandaka isolations increased rapidly in 2012 (214 vs. 57 isolations in 2011), and it then remained the most common serovar isolated until 2018. Both the absolute number and the relative percentage of S. Mbandaka decreased in 2019 (367 isolations vs. 472 in 2018; 21.0% of all isolations vs. 25.7% 2018). Despite this decrease, S. Mbandaka remained the second most common serovar isolated from chickens in 2019.

Even with an 81.2% increase in the number of isolations compared to 2018, S. Kedougou remained the third most common serovar isolated from chickens in 2019 (357 isolations; 20.8%). Similarly, isolations of S. Montevideo increased by 49.6% compared to the previous year, and this continued to be the fourth most common serovar (169 isolations; 9.7%).

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Isolations of S. Derby almost doubled in 2018 (26 in 2018 vs.14 in 2017) and this increasing trend continued in 2019 with the number of isolations rising to 44. Salmonella Agona, a feed-related serovar, also increased more than five-fold compared to the previous year (31 in 2019 vs. 6 in 2018).

The number of S. Senftenberg isolations remained at lower levels following a dramatic reduction in 2018 compared to recent years. There were 72 isolations in 2019 (4.1% of all isolations), compared to 56 isolations in 2018 and 238 in 2017. Salmonella Senftenberg is often related to hatchery contamination, and the reduction may be associated with hatchery improvements.

There were fourteen S. Typhimurium isolations from chickens in 2019, accounting for 0.8% of all Salmonella isolations. This is a slight increase on previous years, when there has been between five and nine isolations of S. Typhimurium annually since 2015. As shown in Table 6.2 and Figure 6.3, four S. Typhimurium isolations in 2019 were phage type DT99, two were DT193 and there was one isolation of each phage type DT2, DT13, DT35 and DT36. Four isolations were RDNC. Many of these strains are likely to be associated with wild birds.

Monophasic strains of S. Typhimurium were first reported from chickens in 2010, when both Salmonella 4,5,12:i:- and Salmonella 4,12:i:- were isolated. In 2019, there were four isolations of monophasic Salmonella Typhimurium 4,5,12:i:-, all of which were phage type DT193 (Figure 6.5). There were also three isolations of monophasic Salmonella Typhimurium 4,12:i:-; one was phage type DT193 and two were UNTY (Figure 6.6). This represents a reduction in monophasic Typhimurium in poultry since 2018, when a large number of cases, in East Anglia in particular, were considered likely to be associated with dust-bowl contamination from outdoor pig farms.

During 2015, the number of S. Enteritidis isolations from chickens spiked to 79 (8.5% of all Salmonella isolations), the majority of which had been linked to a S. Enteritidis outbreak in broiler chickens associated with a single hatchery. In 2016, only four S. Enteritidis isolations were reported, which was in line with pre-outbreak years. The number of isolations increased again in 2017 (25 isolations; 2.2% of all isolations) and remained at a similar level in 2018 (27 isolations; 1.5% of all isolations). The 27 isolations of S. Enteritidis in 2018 involved ten separate flocks; seven broiler flocks, (linked to a smaller hatchery outbreak) and three adult laying hen flocks. The number of S. Enteritidis isolations increased considerably in 2019 to 48 (2.7% of all chicken isolations), involving 16 separate flocks. However, there was a shift in the type of flocks involved compared to 2018, with the majority in 2019 being from adult laying flocks (14 flocks) and fewer from broiler flocks (2 flocks). The 14 adult laying flocks were from five separate holdings and were potentially linked by the use of common packing centres, which may have facilitated transmission of infection from highly contaminated farms to others.

Salmonella Enteritidis phage types isolated from chickens in 2019 are shown in Table 6.3 and Figure 6.4. There was a shift in the phage types identified in 2019 compared to 2018, with large increases in the number of PT8 (35 vs. 6 in 2018) and PT13a (8 vs. 1 in 2018).

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In contrast, there was a large decrease in isolations of PT4 compared to in 2018 (1 vs. 13 in 2018). In addition, there was a single isolation each of PT2, PT11b and PT13. Salmonella Enteritidis PT2 and PT11b had never been isolated from chickens in GB before, and PT13 was last isolated from chickens in GB in 2007. One isolation in 2019 did not react with any of the phages in the current typing scheme (UNTY). Phage types of S. Enteritidis can be variable and genotyping evidence suggested that these isolates were likely to be variants of PT8.

In 2019, S. Muenchen, S. Nima and S. Offa were isolated from chickens in GB for the first time. Other unusual serovars included S. Reading (from laying hens), which was last isolated from chickens in GB in 2011, S. London (from broilers) and S. Tennessee (from laying hens), both of which had not been isolated from chickens in GB since 2014.

National Control Programme for Salmonella in chickens The Zoonoses Regulation EC No. 2160/20032, which came into force on 21st December 2003, aims to reduce the prevalence of certain zoonotic infections at the primary production level, by requiring the implementation of species-specific Salmonella National Control Programmes (NCPs). There are three Salmonella NCPs for chickens (Gallus gallus) in GB; for breeding flocks, laying flocks and broiler flocks.

For all the NCPs, the results are reported in terms of positive flocks. A flock is counted as positive only once regardless of the number of separate isolations reported from that flock or the number of different serovars identified. If more than one positive flock is identified on a holding within the year, these are counted separately.

National Control Programme for Salmonella in breeding flocks of chickens

The NCP for breeding flocks of chickens implements the monitoring and controls that are required in order to meet the target for reduction in Salmonella prevalence that has been set in Regulation (EU) No. 200/20103 and Regulation (EU) No. 517/20114 (amended in 2019 by Regulation (EU) 2019/2685). The target is for a maximum of 1% of adult breeding flocks testing positive for regulated Salmonella serovars annually. The regulated serovars are S. Enteritidis, S. Typhimurium, monophasic strains of Salmonella Typhimurium with the antigenic formula Salmonella 1,4,[5],12:i:-6, S. Infantis, S. Virchow and S. Hadar.

2 https://eur-lex.europa.eu/legal-content/en/ALL/?uri=CELEX:32003R2160

3 https://eur-lex.europa.eu/LexUriServ/LexUriServ.do?uri=OJ:L:2010:061:0001:0009:EN:PDF 4 http://eur-lex.europa.eu/LexUriServ/LexUriServ.do?uri=OJ:L:2011:138:0045:0051:EN:PDF

5 https://eur-lex.europa.eu/legal-content/EN/TXT/?qid=1596624302456&uri=CELEX:32019R0268 6 The somatic antigen 1 can only be determined after lysogeny so is not normally tested for. The somatic antigen 5 may or may not be present in different strains of S. Typhimurium or its monophasic variants

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The NCP for Salmonella in breeding flocks includes all holdings with 250 or more birds. The NCP in GB is enforced by separate, equivalent Control of Salmonella in Poultry Orders (CSPO) in England7, Scotland8 and Wales9. The EC target for reduction is only concerned with regulated serovars in adult breeding flocks; however, the CSPO sets out sampling and recording requirements for both in-rear and adult flocks, and APHA monitors the results from testing in both age categories.

Positive breeding flocks identified in the NCP in 2019

In 2019, thirteen adult breeding flocks, on eight separate holdings, tested positive for Salmonella under the statutory testing programme. No adult breeding flock tested positive for a regulated Salmonella serovar. Seven broiler parent flocks from three holdings tested positive for Salmonella 13,23:i:-, two broiler parent flocks on one holding tested positive for S. Ohio, one broiler grandparent flock tested positive for S. Kottbus, one layer parent flock tested positive for S. Nottingham, one broiler grandparent flock tested positive for Salmonella 6,7:-:enz15 and one broiler parent flock tested positive for Salmonella 3,19:z27:- (Table 6.4).

The number of adult breeding flocks found positive for Salmonella in 2019 (13 flocks) was the highest since 2009 (when there were 19 positive flocks), and although very similar to 2018 (12 positive flocks), it is more than double the number of positive flocks compared to 2017 (6 positive flocks). In general, there has been an increasing trend in the proportion of adult breeding flocks found positive for Salmonella since 2013 (Figure 6.7).

No immature (in-rear) breeding flocks tested positive for any Salmonella serovar during 2019. This is fewer than in 2018 (2 positive flocks) but the same as in 2017, and is in line with the low numbers of positive immature breeding flocks identified in previous years.

No breeding flocks were identified with regulated Salmonella serovars in 2019, which was the same as in 2018, 2017, 2015, 2013 and 2012. In 2016 and 2011, a single broiler parent flock tested positive for S. Typhimurium each year, and a single broiler parent flock tested positive for monophasic S. Typhimurium 4,12:i:- in 2014.

A comparison of the serovars identified in adult breeding flocks that tested positive under the NCP between 2012 and 2019 is shown in Table 6.4 and Figure 6.8; data for years prior to this are available in the Salmonella in Livestock Production reports from the relevant year.

The increase in the number of positive adult breeding flocks seen since 2017 is largely attributable to an increase in the number of flocks testing positive for the partially typeable serovar Salmonella 13,23:i:-, which is a monophasic variant of S. Idikan and is a resident strain in some hatcheries and feed mills and often becomes persistent on affected poultry

7 http://www.legislation.gov.uk/uksi/2007/3574/contents/made

8 http://www.legislation.gov.uk/ssi/2008/266/contents/made

9 http://www.legislation.gov.uk/wsi/2008/524/contents/made

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farms. Seven flocks from three different holdings tested positive for this serovar in 2019. This is slightly fewer than in 2018, when nine flocks tested positive, but remains high compared to 2017 when just two flocks tested positive. There was, however, a 50% reduction in the number of different holdings testing positive for this serovar in 2019 compared to the previous year (3 holdings in 2019 versus 6 holdings in 2018). There has been a concurrent increase in the number of broiler flocks of Gallus gallus testing positive for this serovar in recent years.

Apart from Salmonella 13,23:i:-, which has been identified in adult breeding flocks every year since 2013, there is no clear trend in the occurrence of different Salmonella serovars year-on-year. Only one of the five other Salmonella serovars identified in breeding flocks during 2019 has been reported from NCP testing in adult breeding chickens in the last 10 years, namely S. Kottbus in 2010.

In GB, a total of 1,246 adult breeding flocks were subject to routine annual official sampling tests under the NCP during 2019. Using this figure as the denominator population, the estimated prevalence of Salmonella spp. in adult breeding flocks within the NCP was 1.04% (13/1,246) in 2019. This is comparable to prevalence in 2018 (1.06%), but higher than in 2017 (0.49%) and all other years since 2009 (Table 6.4, Figure 6.7).

The estimated prevalence of regulated serovars in adult breeding flocks in GB during 2019 was 0.00% (0/1,246). This is well below the definitive target of 1% and maintains the low prevalence observed since the introduction of the NCP. For comparison, the prevalence in 2018 and 2017 was also 0.00% (Table 6.4, Figure 6.7).

National Control Programme for Salmonella in laying hen flocks

Commercial laying flocks are subject to statutory Salmonella testing programmes in order to fulfil the requirements of Regulation (EC) No. 2160/200310 and Regulation (EU) No. 517/201111 (amended in 2019 by Regulation (EU) 2019/26812). The target is for a maximum of 2% of adult laying hen flocks testing positive for regulated Salmonella serovars annually. The regulated serovars are S. Enteritidis, S. Typhimurium, and monophasic strains of S. Typhimurium (Regulation (EU) No. 517/2011).

The NCP for Salmonella in laying flocks includes all commercial egg laying holdings with 350 or more birds. The NCP is enforced by separate, equivalent Control of Salmonella in Poultry Orders (CSPO) in England13, Scotland14 and Wales15. The EC target for reduction is only concerned with regulated serovars in adult laying flocks; however, the CSPO sets

10 http://eur-lex.europa.eu/LexUriServ/LexUriServ.do?uri=OJ:L:2003:325:0001:0015:EN:PDF

11 http://eur-lex.europa.eu/LexUriServ/LexUriServ.do?uri=OJ:L:2011:138:0045:0051:EN:PDF

12 https://eur-lex.europa.eu/legal-content/EN/TXT/?qid=1596624302456&uri=CELEX:32019R0268 13 http://www.legislation.gov.uk/uksi/2007/3574/contents/made 14 http://www.legislation.gov.uk/ssi/2008/266/contents/made 15 http://www.legislation.gov.uk/wsi/2008/524/contents/made

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out sampling and recording requirements for both in-rear and adult flocks, and APHA monitors the results from testing in both age categories.

Positive laying flocks identified in the NCP in 2019

During 2019, a total of 48 adult laying hen flocks, originating from 34 separate holdings, tested positive for Salmonella under the statutory testing programme. This is 28.4% lower than the number of flocks testing positive in 2008 when the NCP was first implemented (67 positive flocks), but is an increase of 84.6% compared to 2018 (26 positive flocks) (Table 6.5 and Figure 6.9).

There were seven in-rear (immature) flocks positive for Salmonella in 2019. This is a 75.0% increase compared to 2018 (4 positive flocks) but a slight reduction compared to 2017 (8 positive flocks). Compared to 2008, the number of in-rear positive flocks has fallen by 50.0% (7 vs. 14 positive flocks in 2008). There has been a general declining trend over this time, although the number of in-rear flocks testing positive for Salmonella in 2009 and 2010 was considerably higher (38 and 30 positive flocks, respectively).

A total of sixteen adult flocks, from seven separate holdings, tested positive for a regulated Salmonella serovar during 2019. This represents a four-fold increase compared to 2018 (4 positive flocks) (Table 6.5 and Figure 6.9). Fourteen flocks were positive for S. Enteritidis in 2019 (PT8 (x11), PT13a (x2), PT11b (x1) and PT2 (x1)), including one flock that tested positive for two different phage types (PT13a and PT11b). These are all considered, on the basis of whole genome sequencing, to be variants of PT8. In addition, one flock was positive for S. Typhimurium (DT35) and one flock was positive for monophasic S. Typhimurium 4,5,12:i:- (DT193). This is the first time since 2015 that an adult laying flock has tested positive for any monophasic strain of S. Typhimurium (1 flock tested positive for S. 4,12:i:- DT193 in 2015).

The increase in prevalence of regulated serovars in adult laying flocks in 2019 was largely driven by an increase in the number of flocks testing positive for S. Enteritidis, with fourteen adult flocks from five separate holdings testing positive. This is the highest since the implementation of the NCP in 2008 (when 49 flocks tested positive) and is more than four times higher than the number of flocks testing positive for S. Enteritidis in 2018 (3 flocks). This increase was influenced by the occurrence of risk-based enhanced sampling by APHA and BEIC on some positive premises which were linked by use of common egg packing centres. These centres may have been responsible for dissemination of infection between farms after packing eggs from a highly infected flock.

No in-rear (immature) laying flocks tested positive for regulated serovars during 2019. This compares to one in-rear flock testing positive in 2018 (for S. Typhimurium RDNC), which was the first time since 2010 that a regulated serovar had been detected in NCP samples from an immature flock.

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A comparison of the serovars identified in adult laying flocks in the NCP between 2015 and 2019 is shown in Table 6.5 and Figure 6.10; data for years prior to this are available in the Salmonella in Livestock Production reports from the relevant year.

In total, twenty-one different non-regulated serovars were isolated from adult laying hens in 2019. The most common was S. Kedougou, a feed-related serovar, which was isolated from four flocks. This serovar has not been isolated from adult laying flocks via NCP sampling since 2016, when a single flock tested positive. All four positive flocks in 2019 were located on a single holding and were identified at the same time.

Three adult flocks on three different holdings tested positive for S. Newport in 2019. This is the same number of flocks that tested positive in 2018, a slight increase compared to 2017 (2 flocks), but still 50% fewer than in 2014 (6 flocks) when the highest number of flocks tested positive for this serovar since the implementation of the NCP in 2008.

Three adult flocks on three different holdings tested positive for S. Agama in 2019. This is a slight increase compared to 2018 (1 positive flock), but similar to the number of positive flocks in preceding years (4 flocks in 2017 and 3 flocks in 2016). This serovar, which, like S. Newport, is associated with badgers, has been isolated from at least one adult laying flock in all but one year (2011) since the implementation of the NCP.

Two adult flocks on two different holdings tested positive for S. Anatum in 2019. Two further flocks on a different holding tested positive for S. Montevideo, which is usually feed-related. Prior to 2019, neither of these serovars had been isolated from laying chickens as a result of NCP sampling since 2015.

One adult flock tested positive for the partially typeable serovar S. 13,23:i:- in 2019. This is a reduction compared to 2018, when the number of flocks testing positive was much higher than in any previous year since the implementation of the NCP (5 flocks from 4 different holdings tested positive in 2018). This serovar has been resident in feed production for several years and continues to be commonly isolated from breeding chickens, hatcheries and broilers in GB.

One adult flock tested positive for S. Rissen in 2019. This is similar to 2018, when two flocks on a single holding tested positive. This serovar is commonly associated with rapeseed feed ingredients and pigs and prior to 2018 had only been isolated in NCP samples once since the implementation of the NCP in 2008 (1 flock tested positive in 2014).

The predominant serovar detected in immature (in-rear) flocks of laying hens in 2019 was S. Senftenberg, which was isolated from four flocks and is particularly associated with some hatcheries. Other serovars detected in immature flocks were S. Montevideo (1 positive flock), S. Nottingham (1 positive flock) and Salmonella 13,23:i:- (1 positive flock).

Using the number of NCP-eligible adult flocks of laying hens in production in GB during 2019 as the denominator population, the estimated prevalence of Salmonella spp. in laying

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flocks was 1.20% (48/4,014) in 2019. This compares with 0.63% in 2018 and 0.72% in 2017. The estimated prevalence of regulated Salmonella serovars in adult laying flocks was 0.40% (16/4,014) in 2019. This is a four-fold increase compared to 2018 (0.10%) but still falls well below the definitive EU target of below 2%.

Overall, the prevalence of Salmonella in adult laying hens in GB remains considerably lower than in 2004 and 2005 when the EU baseline survey was carried out. Whilst the results of the baseline survey are not directly comparable to the NCP monitoring results, due to different sampling methods and denominator data, this nevertheless demonstrates continued successful control of Salmonella in the egg industry.

National Control Programme for Salmonella in broiler flocks

Commercial broiler flocks are subject to statutory Salmonella testing programmes in order to fulfil the requirements of Regulation (EC) No. 2160/200316 and Regulation (EU) No. 200/201217 (amended in 2019 by Regulation (EU) 2019/26818). The target is set for a maximum of 1% of broiler flocks testing positive for regulated Salmonella serovars annually. The regulated serovars are S. Enteritidis, S. Typhimurium, and monophasic strains of S. Typhimurium (Regulations (EU) No. 200/2012 and (EU) No. 517/201119).

The NCP for Salmonella in broiler flocks includes all commercial broiler holdings with 2000 or more birds. The NCP is enforced by separate, equivalent Control of Salmonella in Broiler Orders (CSBO) in England20, Scotland21 and Wales22.

Positive flocks identified in the NCP for broiler flocks in 2019

During 2019, a total of 1,472 broiler flocks tested positive for Salmonella under NCP testing. This is the highest number of positive flocks identified in any year since the broiler sector NCP was implemented, representing an increase of 14.7% compared to 2018 (1,283 positive flocks) and continuing the general increasing trend observed since 2014 (430 positive flocks in 2014, 557 positive flocks in 2015, 561 positive flocks in 2016, and 702 positive flocks in 2017) (Table 6.6 and Figure 6.11).

Seventeen broiler flocks tested positive for regulated serovars in 2019. This was the same as in 2018; an increase compared to 2017 (3 positive flocks) and 2016 (5 positive flocks), but a 67.3% decrease compared to 2015, when more positive flocks were detected than in any previous year since the implementation of the NCP (52 positive flocks) (Table 6.6 and

16 http://eur-lex.europa.eu/LexUriServ/LexUriServ.do?uri=OJ:L:2003:325:0001:0015:EN:PDF

17 http://eur-lex.europa.eu/LexUriServ/LexUriServ.do?uri=OJ:L:2012:071:0031:0036:EN:PDF

18 https://eur-lex.europa.eu/legal-content/EN/TXT/?qid=1596624302456&uri=CELEX:32019R0268

19 http://eur-lex.europa.eu/LexUriServ/LexUriServ.do?uri=OJ:L:2011:138:0045:0051:EN:PDF 20 http://www.legislation.gov.uk/uksi/2009/260/pdfs/uksi_20090260_en.pdf 21 http://www.legislation.gov.uk/ssi/2009/229/contents/made 22 http://www.legislation.gov.uk/wsi/2009/441/contents/made

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Figure 6.11). The large number of positive broiler flocks in 2015 was primarily due to an outbreak of S. Enteritidis in broiler chickens linked to a single hatchery.

Ten flocks, from seven separate holdings, tested positive for S. Typhimurium (DT99 (x4), RNDC (x3), DT193 (x1), DT36 (x1) and DT2 (x1)) in 2019. These phage types are largely associated with wild birds, especially when isolates are fully sensitive to antibiotics. This is more than double the number of positive flocks compared to 2018 (4 positive flocks), and the highest since 2013 when ten flocks also tested positive for this serovar (Table 6.6). In contrast, the number of flocks testing positive for S. Enteritidis fell from seven flocks (linked to a hatchery outbreak) in 2018 to two flocks, on two separate holdings, in 2019 (PT8 (x1), PT13 (x1)). This is in line with the low number of flocks testing positive for S. Enteritidis in 2017 (1 positive flock) and 2016 (0 positive flocks), and is a substantial reduction compared to 2015, when an outbreak of S. Enteritidis involving 50 flocks was linked to a single hatchery (Table 6.6). Fortunately, S. Enteritidis and S. Typhimurium can be readily eliminated from hatcheries as they do not persist with incubation, unlike several non-regulated serovars.

Three flocks, from two separate holdings, tested positive for monophasic S. Typhimurium 4,12:i:- (UNTY (x2) and DT193 (x1)) in 2019. This is in keeping with the generally low numbers of flocks that are positive for this serovar each year, and a reduction compared to 2018 (5 positive flocks) (Table 6.6).

Two flocks, from two separate holdings, tested positive for monophasic S. Typhimurium 4,5,12:i:- (both DT193) in 2019. This is a slight increase compared to 2018 (1 positive flock) and 2017 (no positive flocks), but is substantially lower than in 2014, when eight flocks tested positive for this serovar (the highest since the NCP was first implemented). One of the flocks positive for Salmonella 4,5,12:i:- in 2019 was identified through official post-restocking sampling, suggesting the carry-over of infection from a previous turkey flock on the same premises in 2018. There was no repeat of the large number of monophasic Typhimurium cases reported from East Anglia in 2018, which is likely to be associated with less hot and dusty conditions on outdoor pig farms and vaccination of many ‘at risk’ broiler and turkey farms.

A comparison of the serovars identified in broiler flocks in the NCP between 2015 and 2019 is shown in Table 6.6 and Figure 6.12; data for years prior to this are available in the Salmonella in Livestock Production reports from the relevant year.

As in 2018, the partially typable serovar Salmonella 13,23:i:- was the most frequently isolated serovar from broiler flocks in 2019 (418 positive flocks). This serovar has been commonly observed in broiler flocks since 2013, prior to which it was only isolated from a single flock in 2009. An initial surge of reports in 2013 (118 positive flocks) was followed by a decrease until 2015 (60 positive flocks). However, reports of this serovar have since risen considerably year-on-year and while there were slightly fewer positive flocks in 2019 compared to 2018 (418 vs. 445), numbers remain more than three-fold higher than in 2017 (129 positive flocks). Salmonella 13,23:i:- is a resident strain in some hatcheries and in feed production, which can also become persistent on poultry farms. There has been a

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concurrent increase in the number of breeder and egg laying flocks of Gallus gallus testing positive for this serovar in recent years (although a slight decline was seen in all sectors in 2019).

Salmonella Mbandaka was the second most frequently reported serovar from broiler flocks in 2019 (334 positive flocks). This was the most frequently isolated serovar in the broiler NCP between 2013 and 2015 and has been commonly detected since the NCP was first implemented in 2009. The number of positive flocks in 2019 was slightly lower than in 2018 (334 vs. 350), but still represents a 76% increase compared to 2017. Salmonella Mbandaka is a feed-related serovar, typically associated with soya products and can colonise the pellet cooling systems in feed mills. It can also become resident in hatcheries.

Salmonella Kedougou was the third most frequently reported serovar from broiler flocks in 2019 (331 positive flocks). As with S. Mbandaka, S. Kedougou has been commonly observed since the implementation of the broiler NCP; however, the number of positive flocks observed in 2019 is the highest since the NCP began and represents a 75.1% increase compared to 2018, when there were 189 positive flocks. Salmonella Kedougou is also a feed-related serovar, which can be found in oilseed meal ingredients, and may become resident within cooling systems in feed mills.

The number of flocks positive for S. Montevideo more than doubled in 2019 compared to the previous year (144 positive flocks compared to 69 positive flocks in 2018). Increasing numbers of flocks have tested positive for this serovar each year since 2015, when 19 flocks tested positive. Salmonella Montevideo, like the other common feed associated serovars mentioned above, appears to be an efficient environmental persister and is able to colonise cooling systems for heat processed feed ingredients and finished feed, as well as hatcher cabinets and feeding systems on farms.

The number of flocks positive for S. Derby almost doubled in 2019 compared to the previous year (29 positive flocks compared to 18 positive flocks in 2018), and is the highest ever reported. This serovar was uncommon prior to 2016, but fourteen flocks tested positive in 2016 and this increase in occurrence has been sustained ever since. This serovar is most commonly associated with pigs and turkeys, with the increase over the last four years appearing to largely relate to hatchery contamination.

There were also notable increases in the number of flocks positive for S. Agona and S. Idikan in 2019 compared to previous years, with the highest numbers of positive flocks being identified for each of these serovars since the start of the NCP. Salmonella Agona, usually associated with feed contamination, increased more than six-fold in 2019 (29 positive flocks) compared to 2018 (4 positive flocks), and the number of flocks testing positive for S. Idikan almost doubled (15 vs. 8 positive flocks in 2019 and 2018, respectively). These serovars are associated with imported vegetable protein feed ingredients.

Nine serovars were also reported from broiler flocks for the first time in NCP samples during 2019: S. Coeln, S. Kingston, S. London, S. Muenchen, S. Offa, Salmonella

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3,10:e,h:-, Salmonella 61:-:1,5,7 (each reported in 1 flock), S. Eastbourne and Salmonella 13,23:-:l,w (each reported in 2 flocks).

There was a notable reduction in the number of flocks positive for three serovars in 2019. There was a 21% decrease in the number of S. Ohio-positive flocks in 2019 (69 flocks) compared to 2018 (87 flocks), although this serovar (also associated with contaminated feed) is still frequently detected in broiler flocks. Following sharp increases compared to previous years in the number of flocks positive for Salmonella 4,12:d:- and S. Orion in 2018 (17 and 13 positive flocks, respectively), the number of flocks positive for each of these serovars decreased in 2019 (7 flocks positive for Salmonella 4,12:d:- and 3 flocks positive for S. Orion), returning to the lower levels seen prior to this spike.

An estimated 48,849 broiler flocks were tested in GB according to the requirements of the Salmonella NCP during 2019. Using this as the denominator population, the estimated prevalence of Salmonella-positive broiler flocks was 3.01% (1,472/48,849). This is similar to the prevalence in 2018 (2.98%), but approximately double the prevalence seen in 2017, and the highest it has been since the implementation of the NCP in 2009 (Table 6.6; Figure 6.11). As highlighted above, many of the serovars displaying increased occurrence in broilers are associated with feed. It is therefore possible that a ban on the use of formaldehyde-based products in animal feed production, which came into force across the European Union in January 2018, may have contributed to the increase in number of Salmonella-positive broiler flocks that began in 2018 and has continued in 2019.

The estimated prevalence of regulated Salmonella serovars in broiler flocks in GB during 2019 was 0.03% (17/48,849). This is similar to 2018 (0.04%), slightly higher than in 2017 and 2016 (0.01% in both years), but a substantial reduction compared to 2015 (0.14%) when the highest prevalence was observed since the implementation of the NCP (Table 6.6, Figure 6.11). The prevalence of regulated Salmonella serovars in broiler chickens in 2019 falls well below the definitive EU target of below 1% and is consistent with the ongoing maintenance of a low prevalence of regulated serovars in this sector.

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Figure 6.1: Chicken population in GB 2010 – 2019

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Table 6.1: Salmonella in chickens on all premises in Great Britain. (Positive flocks from statutory testing; isolations from both statutory and non-statutory testing)

Salmonella 2015 2015 2016 2016 2017 2017 2018 2018 2019 2019subspecies Flocks Isolations Flocks Isolations Flocks Isolations Flocks Isolations Flocks IsolationsENTERICA ENTERICAAfricana - - - - - - - - 1 1Agama 6 6 3 3 5 10 1 1 7 7Agona 6 7 7 6 7 8 4 6 29 31Ajiobo 1 1 - - 1 2 - - - -Anatum 1 2 4 4 - 1 1 1 5 5

Bovismorbificans - - - - 2 2 - - - -Braenderup 1 1 - - - - - - - -Budapest - - - - - - 1 1 - -Butantan - - 2 2 - - - - - -

Coeln 1 1 - - - - - - 1 1Cubana - - 1 1 - - - - - -

Derby - - 14 24 12 14 18 26 30 44Dublin 1 1 - - 1 2 - - 1 1Durham - - 1 1 - - - - - -

Eastbourne - - - - - - - - 3 3Enteritidis 50 79 1 4 6 25 10 27 16 48

Fresno - - - - - - - - - 1

Give 1 1 - - 1 2 4 8 - -Give var. 15+ - - 1 1 1 2 - - 4 4Goldcoast 3 2 1 1 - - - - - -

Hadar - - 1 1 - - - - - -Havana - - 2 2 2 2 3 3 1 1

Idikan 3 7 - 2 2 2 9 13 16 17Indiana 24 29 3 3 1 1 3 3 7 7Infantis - 1 5 7 7 8 1 2 - -Isangi - - - - - - 1 1 - -

Javiana - 2 - - - - - - - -

Kedougou 124 138 163 180 138 150 190 197 335 357Kentucky - - 1 2 3 3 - 1 1 1Kingston 1 1 - - - - 1 1 1 1Kottbus 1 1 2 2 - 1 5 6 2 4

Lexington - - - - 1 1 - - - -Liverpool - - - 5 1 1 - - - -Livingstone 4 11 11 22 8 14 9 12 7 10London - - - - - - - - 2 2

Mbandaka 212 279 148 193 190 272 353 472 335 367Meleagridis - - - - - 1 - - - -Mokola - - - - 1 5 - - - -

94

Table 6.1: Salmonella in chickens on all premises in Great Britain. (Positive flocks from statutory testing; isolations from both statutory and non-statutory testing) (continued)

Salmonella 2015 2015 2016 2016 2017 2017 2018 2018 2019 2019subspecies Flocks Isolations Flocks Isolations Flocks Isolations Flocks Isolations Flocks IsolationsENTERICA ENTERICAMontevideo 20 31 31 93 51 105 69 113 146 169Muenchen - - - - - - - - 1 1Muenster - - 1 1 - - - - - -

Nagoya - - 1 1 1 1 - - - -Newport 3 4 13 14 5 5 7 8 5 5Nima - - - - - - - - 1 1Nottingham - - - - - 1 4 9 4 9

Offa - - - - - - - - 1 1Ohio 25 26 13 11 45 48 87 94 71 75Oranienburg - - - - - 1 - - - -Orion 2 2 - - 3 4 13 14 3 4Orion var. 15+ - 1 2 2 3 3 11 15 12 14Oslo - - - - 5 5 2 2 2 2

Panama - - 1 1 - - - - - -Paratyphi B var. Java - 2 - - 3 7 - - - -Poona - - 1 1 - - 1 2 - -Pullorum - 1 - 1 - 1 - - - -

Reading - - - - - - - - 1 1Rissen - - - - - - 2 2 1 1Rosslyn - - - - - 2 - - - -

Schwarzengrund 1 1 - - - - - - - -Senftenberg 15 68 47 155 93 238 19 56 33 72Soerenga - - 1 1 - - 1 1 - -Stanley - - - - - - 1 1 1 1

Tennessee - - - - - - - - 2 2Thompson - - 1 1 - - - - - -Typhimurium 1 6 4 7 2 5 5 9 11 14

4,5,12:i:- - - 1 1 - 1 1 2 3 44,12:i:- 2 3 - 2 3* 4* 5 8 3 3

13,23:i:- 62 189 104 188 131 179 459 681 426 436

ENTERICA DIARIZONAE61:-:1,5,7 - - - - - - - - 1 1

UNSPECIFIEDuntypable strains 14 19 4 4 10 13 26 33 16 19rough strains 3 5 - - 1 2 4 7 1 1

TOTAL 585†† 929 596††† 950 736‡ 1154 1321‡‡ 1838 1533∆ 1749

* Two were not S . Typhimurum or monophasic S . Typhimurium by PCR†† Three flocks were positive for more than one serovar in 2015 ††† Five flocks were positive for more than one serovar in 2016‡ Ten flocks were positive for more than one serovar in 2017 ‡‡ Ten flocks were positive for more than one serovar in 2018∆ 16 flocks were positive for more than one serovar in 2019

95

Figure 6.2: The most common serovars in chickens by number of isolations* in GB 2015 – 2019

* Derived from statutory and non-statutory testing.

Mbandaka30.0%

13,23:i:-20.3%

Kedougou14.9%

Enteritidis8.5%

Senf tenberg7.3%

Montev ideo3.3%

Indiana3.1%

Ohio2.8%

Liv ingstone1.2%

Other serov ars

8.5%

2015 (n=929)

Mbandaka20.3%

13,23:i:-19.8%

Kedougou18.9%

Senf tenberg16.3%

Montev ideo9.8%

Derby2.5%

Liv ingstone2.3%

Newport1.5%

Ohio1.2%

Other serov ars

7.4%

2016 (n=950)

Mbandaka23.6%

Senf tenberg20.6%13,23:i:-

15.5%

Kedougou13.0%

Montev ideo9.1%

Ohio4.2%

Enteritidis2.2%

Derby1.2%

Liv ingstone1.2%

Other serov ars

9.4%

2017 (n=1,154)

13,23:i:-37.1%

Mbandaka25.7%

Kedougou10.7%

Montev ideo6.1%

Ohio5.1%

Senf tenberg3.0%

Enteritidis1.5%

Derby1.4%

Orion v ar. 15+0.8%

Other serov ars

8.5%

2018 (n=1,838)

13,23:i:-24.9%

Mbandaka21.0%

Kedougou20.4%

Montev ideo9.7%

Ohio4.3%

Senf tenberg4.1%

Enteritidis2.7%

Derby2.5%

Agona1.8%

Other serov ars

8.6%

2019 (n=1,749)

96

Table 6.2: S. Typhimurium in chickens on all premises in Great Britain. (Positive flocks from statutory testing; isolations from both statutory and non-statutory testing)

2015 2015 2016 2016 2017 2017 2018 2018 2019 2019Flocks Isolations Flocks Isolations Flocks Isolations Flocks Isolations Flocks Isolations

1 - - - 1 - 1 - - - -2 - - - 1 1 2 - - 1 113 - - - - - - - - - 135 - - - - - - - - 1 136 - - - - - - - - 1 141b 1 1 - - - - - - - -85 - - 1 1 - - - - - -99 - - - - - - - - 4 4104 - - 3 4 1 1 - - - -132 - 3 - - - - - - - -135 - 1 - - - - - - - -193 - 1 - - - 1 1 1 1 2

NOPT - - - - - - - 1 - -RDNC - - - - - - 4 7 3 4

TOTAL 1 6 4 7 2 5 5 9 11 14

Phage types

97

Figure 6.3: Most common phage types of S. Typhimurium in chickens in GB 2015 - 2019†

† Flocks from statutory testing; isolations from both statutory and non-statutory testing.

98

Figure 6.4: S. Enteritidis phage types in chickens in GB 2015 - 2019†

† Flocks from statutory testing; isolations from both statutory and non-statutory testing.

99

Figure 6.5: Salmonella 4,5,12:i:- phage types in chickens in GB 2015 - 2019†

† Flocks from statutory testing; isolations from both statutory and non-statutory testing.

100

Figure 6.6: Salmonella 4,12:i:- phage types in chickens in GB 2015 - 2019†

† Flocks from statutory testing; isolations from both statutory and non-statutory testing

101

Table 6.3: S. Enteritidis in chickens on all premises in Great Britain. (Positive flocks from statutory testing; isolations from both statutory and non-statutory testing)

2015 2015 2016 2016 2017 2017 2018 2018 2019 2019Flocks Isolations Flocks Isolations Flocks Isolations Flocks Isolations Flocks Isolations

1 - - - - 1 1 - - - -2 - - - - - - - - 1 14 - 1 - 3 2 5 5 13 - 16a 3 3 - - - - - - - -7 - - - - - - 1 2 - -8 - - - - - 15 3 6 12 359b - 2 - - - - - - - -11b - - '- - - - - - 1 113 - - - - - - - - 1 113a - - - - 3 3 - 1 2 821 44 67 1 1 - - - - - -21b 1 1 - - - - - - - -35 1 3 - - - - - - - -62 - - - - - - - 2 - -

NOPT 1 1 - - - 1 1 2 - -UNTY - 1 - - - - - 1 - 1

TOTAL 50 79 1 4 6 25 10 27 16* 48

* One flock tested positive for both PT11b and PT13a but is included only once in the total

Phage types

102

Figure 6.7: Prevalence of Salmonella in breeding chicken flocks tested under NCP in GB 2008 – 2019

0.00%

1.00%

2.00%

3.00%

4.00%

5.00%

2008 2009 2010 2011 2012 2013 2014 2015 2016 2017 2018 2019

Pro

porti

on o

f pos

itive

flo

cks

Year

Figure 6.7: Prevalence of Salmonella in breeding chicken flocks tested under NCP in GB 2008 - 2019

Target forregulatedserovars

Prevalenceofregulatedserovars

PrevalenceofSalmonellaspp.

103

Table 6.4: Chicken breeding flocks in GB - number of flocks reported positive with each Salmonella serovar, NCP testing 2012 - 2019*

2012 2013 2014 2015RANK SEROVAR N RANK SEROVAR N RANK SEROVAR N RANK SEROVAR N

1 Dublin 1 1 13,23:i:- 7 1 13,23:i:- 3 1 Agona 3Mbandaka 1 2 Indiana 2 2 4,12:i:- 2 2 Indiana 1

3 Kedougou 1 3 Derby 1 Senftenberg 1Senftenberg 1 Kedougou 1 13,23:i:- 1

Llandoff 1Mbandaka 1Senftenberg 1

Prevalence of regulated serovars = 0.00% Prevalence of regulated serovars = 0.00% Prevalence of regulated serovars = 0.17% Prevalence of regulated serovars = 0.00%

2016 2017 2018 2019RANK SEROVAR N RANK SEROVAR N RANK SEROVAR N RANK SEROVAR N

1 13,23:i:- 6 1 Agona 2 1 13,23:i:- 9 1 13,23:i:- 72 Mbandaka 1 13,23:i:- 2 2 Kedougou 1 2 Ohio 2

Nagoya 1 2 Senftenberg 1 Mbandka 1 3 Kottbus 1Newport 1 9,12:z29:1,5 1 O rough:g,m,t:- 1 Nottingham 1Poona 1 6,7:-:enz15 1Typhimurium 1 3,19:z27:- 1

Prevalence of regulated serovars = 0.09% Prevalence of regulated serovars = 0.00% Prevalence of regulated serovars = 0.00% Prevalence of regulated serovars = 0.00%

* For details of chicken breeding flocks reported positive in 2007 - 2011, see the 2013 edition of Salmonella in Livestock Production in GB.

Prevalence of all serovars = 0.44%Prevalence of all serovars = 0.86%Prevalence of all serovars = 0.16% Prevalence of all serovars = 0.75%

Prevalence of all serovars = 1.04%Prevalence of all serovars = 1.06%Prevalence of all serovars = 1.01% Prevalence of all serovars = 0.49%

104

Figure 6.8: Serovars identified in adult chicken breeding flocks in GB 2014 - 2019 reported from NCP testing

13,23:i:-30.0%

4,12:i:-20.0%

Derby10.0%

Kedougou10.0%

Llandof f10.0%

Mbandaka10.0%

Senf tenberg10.0%

2014 (10 positive flocks)

Agona50.0%Indiana

16.7%

Senf tenberg16.7%

13,23:i:-16.7%

2015 (6 positive flocks)

13,23:i:-54.5%Mbandaka

9.1%

Nagoy a9.1%

Newport9.1%

Poona9.1%

Ty phimurium9.1%

2016 (11 positive flocks)

13,23:i:-33.3%

Agona33.3%

Senf tenberg16.7%

9,12:z29:1,516.7%

2017 (6 positive flocks)

13,23:i:-75.0%

Kedougou8.3%

Mbandaka8.3%

O rough:g,m,t:-

8.3%

2018 (12 positive flocks)

13,23:i:-53.8%

Ohio15.4%

Kottbus7.7%

Nottingham7.7%

6,7:-:enz157.7%

3,19:z27:-7.7%2019 (13 positive flocks)

105

Figure 6.9: Prevalence of Salmonella in laying hen flocks tested under NCP in GB 2009 - 2019

0.00%

1.00%

2.00%

3.00%

4.00%

5.00%

2009 2010 2011 2012 2013 2014 2015 2016 2017 2018 2019

Pro

porti

on o

f pos

itive

flo

cks

Year

Figure 6.9: Prevalence of Salmonella in laying hen flocks tested under NCP in GB 2009 - 2019

Target forregulatedserovars

Prevalenceofregulatedserovars

PrevalenceofSalmonellaspp.

106

Table 6.5: Laying hen flocks in GB - number of flocks reported positive with each Salmonella serovar, NCP testing 2015 - 2019*

2015 2016 2017 2018 2019RANK SEROVAR N RANK SEROVAR N RANK SEROVAR N RANK SEROVAR N RANK SEROVAR N

1 Agama 5 1 Agona 4 1 Enteritidis 6 1 13,23:i:- 5 1 Enteritidis 142 Mbandaka 3 Anatum 4 2 Agama 4 2 Enteritidis‡‡ 3 2 Agama 43 Kedougou 2 2 Agama 3 3 Kentucky 3 New port 3 3 Kedougou 44 Agona 1 3 New port 2 Paratyphi B var. Java 3 3 Mbandaka 2 New port 3

Anatum 1 4 Cubana 1 4 Orion 2 Rissen 2 4 Anatum 2Ajiobo 1 Indiana 1 5 Ajiobo‡ 1 Senftenberg 2 Montevideo 2Coeln 1 Infantis 1 Derby 1 4 Agama 1 Nottingham 2Dublin 1 Kedougou 1 Dublin 1 Budapest 1 Tennessee 2Indiana 1 Livingstone 1 Give var. 15+ 1 Idikan 1 5 Africana 1Kingston 1 Mbandaka 1 Liverpool 1 Indiana 1 Derby 1Montevideo 1 Panama 1 Livingstone 1 Kingston 1 Dublin 1Schw arzengrund 1 Senftenberg†† 1 Mokola‡ 1 Nottingham 1 Idikan 13,19:-:- 1 Soerenga 1 Nagoya 1 O rough:g,m:-‡‡ 1 Kottbus 14,12:i:- 1 3,19:-:-†† 1 New port 1 Soerenga 1 London 113,23:i:- 1 Oslo 1 Oslo 1 Mbandaka 1

4,5,12:b:- 1 Typhimurium 1 Nima 1Reading 1Rissen 1Senftenberg 1Typhimurium 14,5,12:b:- 14,5,12:i:- 113,23:i:- 1

* For details of laying hen flocks reported positive in 2008, 2009, 2010, 2011, 2012 and 2013 see the 2013 edition of Salmonella in Livestock Production in GB

†† 1 flock tested positive for both S . Senftenberg and Salmonella 3,19:-:-. This flock was only counted once in the overall annual figure to calculate the prevalence.

‡ 1 flock tested positive for both S . Ajiobo and S . Mokola. This flock was counted only once in the overall annual figure to calculate the prevalence.

‡‡ 1 flock tested positive for both S . Enteritidis and S . O rough:g,m:-. This flock was counted only once in the overall annual figure to calculate the prevalence.

Prevalence all serovars = 1.20%

Prevalence regulated serovars = 0.40%

Prevalence all serovars = 0.60% Prevalence all serovars = 0.58% Prevalence all serovars = 0.72% Prevalence all serovars = 0.63%

Prevalence regulated serovars = 0.03%

Prevalence regulated serovars = 0.00%

Prevalence regulated serovars = 0.15%

Prevalence regulated serovars = 0.10%

107

Figure 6.10: The most common serovars identified in adult laying hen flocks in GB 2014 - 2019 reported from NCP testing

** 1 flock positive for 2 serovars (this is counted only once in the total)

*** 1 flock positive for 2 serovars (this is counted only once in the total) † 1 flock positive for 2 serovars (this is counted only once in the total)

†† 1 flock positive for 2 serovars (this is counted only once in the total)

Newport16.7%

Agama13.9%

Montev ideo11.1%

Dublin8.3%Liv ingstone

8.3%

Enteritidis5.6%

Nottingham5.6%

Other serov ars

30.6%

2014 (35 positive flocks**)

Agama22.7%

Mbandaka13.6%

Kedougou9.1%

Other serov ars

54.5%

2015 (22 positive flocks)

Agona17.4%

Anatum17.4%

Agama13.0%

Newport8.7%

Other serov ars

43.5%

2016 (22 positive flocks***)

Enteritidis20.7%

Agama13.8%

Kentucky10.3%Paraty phi B

v ar. Jav a10.3%

Orion6.9%

Other serov ars

37.9%

2017 (28 positive flocks†)

13,23:i:-18.5%

Enteritidis11.1%

Newport11.1%

Mbandaka7.4%Rissen

7.4%

Senf tenberg7.4%

Other serov ars

37.0%

2018 (26 positive flocks††)Enteritidis

29.2%

Agama8.3%

Kedougou8.3%Newport

6.3%Anatum4.2%

Montev ideo4.2%

Nottingham4.2%

Tennessee4.2%

Other serov ars

31.3%

2019 (48 positive flocks)

108

Figure 6.11: Prevalence of Salmonella in broiler chicken flocks tested under NCP in GB 2010 - 2019

0.00%

1.00%

2.00%

3.00%

4.00%

5.00%

2010 2011 2012 2013 2014 2015 2016 2017 2018 2019

Pro

porti

on o

f pos

itive

flo

cks

Year

Figure 6.11: Prevalence of Salmonella in broiler chicken flocks tested under NCP in GB 2010 - 2019

Target forregulatedserovars

Prevalenceof regulatedserovars

PrevalenceofSalmonellaspp.

109

Table 6.6: Broiler chicken flocks in GB - number of flocks positive for each Salmonella serovar, NCP testing 2015 - 2019*

2015 2016 2017 2018 2019RANK SEROVAR N RANK SEROVAR N RANK SEROVAR N RANK SEROVAR N RANK SEROVAR N1 Mbandaka†† 209 1 Kedougou ‡ 162 1 Mbandaka 190 1 13,23:i:-** 445 1 13,23:i:- ∆ 4182 Kedougou†† 122 2 Mbandaka ‡ 146 2 Kedougou‡‡ 138 2 Mbandaka** 350 2 Mbandaka ∆ 3343 13,23:i:- 60 3 13,23:i:- 98 3 13,23:i:-‡‡ 129 3 Kedougou** 189 3 Kedougou ∆ 3314 Enteritidis 50 4 Senftenberg 46 4 Senftenberg‡‡ 92 4 Ohio 87 4 Montevideo ∆ 1445 Ohio 25 5 Montevideo 31 5 Montevideo 51 5 Montevideo 69 5 Ohio ∆ 696 Indiana 22 6 Derby 14 6 Ohio‡‡ 45 6 Derby 18 6 Senftenberg 327 Montevideo 19 7 Ohio 13 7 Derby 11 7 Senftenberg 17 7 Agona ∆ 298 Senftenberg†† 14 8 Livingstone 10 8 Infantis 7 4,12:d:- 17 8 Derby ∆ 299 6,7:z10:- 11 New port 10 Livingstone‡‡ 7 8 Orion 13 9 Idikan 1510 Livingstone†† 4 9 Infantis 4 9 4,12:d:- 6 9 Orion var. 15+ ** 11 10 Orion var. 15+ ∆ 1211 Goldcoast 3 10 Agona 3 10 Agona 5 10 Livingstone 9 11 Typhimurium ∆ 10

Idikan 3 Typhimurium 3 11 New port 4 11 Idikan 8 12 Indiana 7New port 3 11 Butantan 2 Oslo 4 12 Enteritidis** 7 Livingstone 7

12 Agona 2 Havana 2 12 Orion var. 15+ 3 13 Structure only 6 4,12:d:- ∆ 7Orion 2 Indiana 2 13 Bovismorbif icans 2 Kottbus 5 13 Give var. 15+ 46,7:rough:- 2 Kottbus 2 Havana 2 14 4,12:i:- 5 14 Agama 3

13 O rough:g,s,t:- 1 Orion var. 15+ 2 Idikan‡‡ 2 Agona 4 Anatum ∆ 3Agama 1 12 Durham 1 Typhimurium 2 Give 4 Eastbourne 3Braenderup 1 Enteritidis 1 14 4,12:i:- *** 2 New port 4 Orion ∆ 3Give 1 Give var. 15+ 1 Agama 1 15 Typhimurium 4 4,12:i:- ∆ 3Kottbus 1 Goldcoast 1 Give 1 Havana 3 6,7:z10:- 3Typhimurium 1 Hadar 1 Indiana 1 Nottingham 3 15 Enteritidis 24,12:d:- 1 Kentucky 1 Lexington 1 16 6,7:z10:-** 3 New port 24,12:i:- 1 Muenster 1 Orion 1 Indiana 2 Oslo 26,7:-:- 1 Thompson 1 O rough:d:enz15 1 17 O rough:z10:e.n.z15 2 4,5,12:i:- 2

4,5,12:i:- 1 4,12:i:- 1 Anatum 1 13,23:-:l,w 24,12:d:- 1 6,7:z10:- 1 Infantis 1 16 Coeln 16,7:z10 1 6,7:-:- 1 Isangi 1 Havana 16,7:-:enz15 1 Oslo 1 Kentucky 1

Poona 1 Kingston 1Stanley 1 London 14,5,12:i:- 1 Muenchen 1

Nottingham ∆ 1O rough:z10:e,n,z15 1Offa 1Stanley 13,10:e,h:- 128:-:- 161:-:1,5,7 1

* For details of broiler flocks reported positive in 2009 - 2014 see the 2014 edition of Salmonella in Livestock Production in GB. *** Not S . Typhimurium or monophasic S . Typhimurium

Prevalence of regulated serovars = 0.01%

Prevalence of regulated serovars = 0.04%

Prevalence of all serovars = 1.40% ≠ Prevalence of all serovars = 3.01%Prevalence of regulated serovars = 0.03%

Prevalence of all serovars = 1.55% Prevalence of all serovars = 1.50% Prevalence of all serovars =2.98%Prevalence of regulated serovars = 0.14%

Prevalence of regulated serovars = 0.01%

110

Table 6.6: Broiler chicken flocks in GB - number of flocks positive for each Salmonella serovar, NCP testing 2015 - 2019* - continued

≠ Following further cleansing of the returns from private and Government testing laboratories for all broiler flocks tested within 3 weeks before slaughter the denominator and hence the prevalence for 2016 has been updated. Therefore figures presented here differ to the previously published prevalence estimate for Salmonella spp. in 2016.

†† One flock tested positive for both S . Kedougou and S . Mbandaka, one flock tested positive for both S. Livingstone and S. Senftenberg and another flock tested postive for both S. Mbandaka and S. Senftenberg. Each flock was counted only once in the overall figure to calculate prevlalence.‡ One flock tested positive for both S . Kedougou and S . Mbandaka. This flock was counted only once in the overall figure to calculate prevalence.‡‡ Five flocks tested positive for both S . Kedougou and S . Ohio, one flock tested positive for both S . Livingstone and S . Senftenberg, one flock tested positive for both S . Senftenberg and S . 13,23:i:-, one flock tested positive for both S . 13,23:i:- and S . Kedougou, and another flock tested positive for both S . Senftenberg and S . Idikan. Each flock was counted only once in the overall figure to calculate prevalence.

** Three flocks tested positive for both S . Mbandaka and S . 13,23:i:-, two flocks tested positive for both S . Kedougou and S . 13,23:i:-, one flock tested positive for both S . 6,7:z10:- and S . 13,23:i:-, one flock tested positive for both S . Mbandaka and S . Enteritidis, one flock tested positve for both S . 13,23:i:- and S. Enteritdis and one flock tested positive for both S . 13,23:i:- and S . Orion var. 15+. Each flock was counted only once in the overall figure to calculate prevalence.

∆ Three flocks tested positive for both S .Kedougou and S . Ohio, three flocks tested positive for both S . 13,23:i:- and S . Kedougou, two flocks tested positive for both S . Mbandaka and S . Montevideo, two flocks tested positive for both S . Anatum and S . Derby, one flock tested positive for both S . 13,23:i:- and S . Agona, one flock tested positive for both S . 13,23:i:- and S . Mbandaka, one flock tested positive for for both S . Orion var. 15+ and S . Orion, one flock tested positive for both S . 4,12:d:- and S . Montevideo, one flock tested positive for both S . 4,12:i:- and S . Kedougou and one flock testedpositive for S . Typhimurium, S . 13.23:i:- and S . Nottingham. Each flock was counted only once in the overall figure to calculate prevalence.

111

Figure 6.12: The most common serovars identified in broiler chicken flocks in GB 2014 - 2019 reported from NCP testing

* 4 flocks positive for 2 serovars (these are counted only once in the total) * 3 flocks positive for 2 serovars (these are counted only once in the total)

* 8 flocks positive for 2 serovars (these are counted only once in the total)

* 9 flocks positive for 2 serovars (these are counted only once in the total) * 15 flocks positive for 2 serovars and 1 flock was positive for 3 serovars (these are counted only once in the total)

* 1 flock positive for 2 serovars (this is counted only once in the total)

Mbandaka25.8%

Kedougou19.1%

13,23:i:-18.4%

Montev ideo9.4%

Ohio9.4%

Other serov ars

17.7%

2014 (430 positive flocks*)

Mbandaka37.3%

Kedougou21.8%

13,23:i:-10.7%

Enteritidis8.9%

Ohio4.5%

Indiana3.9%

Montev ideo3.4%

Other serov ars

9.5%

2015 (557 positive flocks*)

Kedougou28.8%

Mbandaka26.0%

13,23:i:-17.4%

Senf tenberg8.2%

Montev ideo5.5%

Derby2.5%

Ohio2.3%

Other serov ars

9.3%

2016 (561 positive flocks*)

Mbandaka26.8%

Kedougou19.4%13,23:i:-

18.2%

Senf tenberg13.0%

Montev ideo7.2%

Ohio6.3%

Derby1.5%

Other serov ars

7.6%

2017 (702 positive flocks*)

13,23:i:-34.4%

Mbandaka27.1%

Kedougou14.6%

Ohio6.7%

Montev ideo5.3%

Derby1.4%

Senf tenberg1.3%

4,12:d:-1.3%

Other serov ars

7.7%

2018 (1,283 positive flocks*)

13,23:i:-28.1%

Mbandaka22.4%

Kedougou22.2%

Montev ideo9.7%

Ohio4.6%

Senf tenberg2.1%

Derby1.9%

Agona1.9%

Other serov ars

6.9%

2019 (1,472 positive flocks*)

112

Chapter 7: Reports of Salmonella in turkeys According to the June Agricultural Census, there were 3.91 million turkeys in Great Britain in 2019 compared with 4.06 million in 2018, 4.08 million in 2017 and 4.02 million in 2016.

In January 2010, the National Control Programme (NCP) to control Salmonella in turkeys was implemented across the European Union. Breeding turkey farms with more than 250 adult birds on the holding and fattening turkey farms with more than 500 birds are eligible for Salmonella testing under the NCP. Since 2010, Salmonella reports from turkeys have largely originated from samples taken under the NCP, so data cannot be compared with previous years.

As described in Chapter 6 for chickens, two different systems of reporting are also used in this chapter and results should be interpreted accordingly.

• The first part of this chapter describes all isolations of Salmonella, including samples originating from statutory surveillance, voluntary surveillance, investigations into clinical disease and investigations carried out under the Zoonoses Order. If two submissions from the same group of birds on different dates give the same serovar, this is reported as two isolations.

• The second part of this chapter describes results obtained within the National Control Programmes (NCPs), i.e. results from statutory surveillance only. Results from the NCPs are reported to the European Commission in a way that ensures that every flock with a Salmonella-positive result is counted only once.

Numbers of positive flocks reported within the NCP are expected to differ from the number of reported isolations. Some flocks may be positive for more than one serovar, in which case, they are still only counted once as positive flocks under the NCP, but are counted as more than one isolation.

There were 407 turkey diagnostic and monitoring submissions made to APHA and SRUC laboratories in 2019; compared to 364 submissions in 2018, representing an increase of 11.8%. In comparison, during 2009, before the introduction of the NCP for Salmonella in turkeys, the number of submissions was substantially lower, with 240 submissions. However, APHA does not have information on the number of non-statutory submissions submitted to private laboratories that do not result in a positive culture of Salmonella, as these are not reportable under the Zoonoses Order.

A total of 267 Salmonella isolations were reported from turkeys in 2019 (Table 7.1), which represents a 46.3% reduction from 497 isolations in 2018. This is the fewest isolations since 2014 when there were 193 isolations and the second lowest number of isolations since the implementation of the turkey NCP in 2010.

In 2009, before the introduction of the NCP, only 88 isolations were reported. The considerable increase in isolations in subsequent years can be explained by more

113

sensitive and regular statutory testing of turkey flocks under the NCP. This has led to the identification of positive flocks that otherwise might not have been detected through voluntary surveillance alone. After a peak in isolation numbers in 2012 (789 isolations), numbers steadily declined until 2014 (193 isolations). Subsequently there was a substantial increase in the number of isolations in 2015 (619 isolations) and 2016 (607 isolations), mainly due to an increase in isolations of S. Derby. Since then, the overall number of isolations from turkeys has declined each year (499 isolations in 2017, 497 isolations in 2018, and 267 isolations in 2019), and this reduction is primarily attributable to a decrease in S. Derby isolations.

The total number of isolations in 2019 was distributed between the following categories according to the reason for submission:

• Statutory surveillance: 239 (89.5%)

• Voluntary surveillance: 28 (10.5%)

• Investigations of clinical disease: 0 (0.0%)

• Investigations under the Zoonoses Order: 0 (0.0%)

Sixteen different serovars of Salmonella were isolated in 2019, accounting for 261 of the 267 isolations. The remaining six isolations involved untypable and rough Salmonella isolates.

Table 7.1 shows the absolute numbers of all Salmonella serovars isolated from turkeys, from 2015 to 2019, and Figure 7.1 shows the relative percentages of the most common serovars. Salmonella Derby has been the most commonly isolated serovar from turkeys since 2007 and this continued to be the case in 2019. Despite a dramatic reduction by 67.1% in S. Derby isolations, from 401 in 2018 to 132 in 2019, this serovar still accounted for 49.4% of all isolations from turkeys. This reduction is in large part due to a change in testing procedure of presumptive S. Derby isolations in 2019 compared to 2018. From 2016 to 2018, the majority of presumptive S. Derby isolations were partially serotyped due to the high number of isolations received from certain turkey premises in those years. This partial serotyping, slide agglutination method, still allowed for any serovars which are regulated under EU legislation (i.e. S. Enteritidis, S. Typhimurium and monophasic strains of S. Typhimurium) and serovars other than S. Derby to be identified and fully typed. However, all presumptive S. Derby isolates were grouped with fully serotyped S. Derby isolates in those years. The partial serotyping of presumptive S. Derby isolates was not carried out during 2019 as the number of isolations of this serovar received from turkey holdings was lower than in previous years.

Salmonella Senftenberg remained the second most common serovar to be isolated from turkeys in 2019. The number of isolations increased compared to 2018 (48 isolations vs. 28 isolations in 2018), as did the relative proportion of turkey isolates that were S. Senftenberg (18% of all turkey isolations vs. 5.6% in 2018). Salmonella Senftenberg is a

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hatchery-related serovar, but is also able to colonise feed mills. Isolations of S. Senftenberg have fluctuated each year from 2010 onwards, accounting for between three and 28 isolations each year, with 48 isolations in 2019 being the highest number of isolations recorded in a year.

Salmonella Kedougou, a feed-related serovar, was the third most common serovar reported in turkeys in 2019 (44 isolations; 16.5% of all isolations). There was an eight-fold increase in the number of isolations compared to 2018 (5 isolations). However, prior to 2018, there had been at least 33 isolations of S. Kedougou each year since 2010.

Salmonella Agona was isolated on nine occasions in 2019 (3.4% of all isolations), which is similar to 2018 (11 isolations). Salmonella Mbandaka and S. Newport were both isolated five times (1.9% of all isolations each), which is also similar to the previous year (6 isolations of S. Mbandaka and 5 isolations of S. Newport in 2018).

Salmonella Kottbus and S. Newport had been among the most common serovars isolated in turkeys since at least 2004 and seemed to have become established in the turkey industry. However, since 2015, S. Kottbus reporting levels have been low, being isolated four times in 2019. Salmonella Newport isolations remained at the same low level as reported in 2018, with five isolations.

The prevalence of S. Typhimurium, which was the most commonly reported serovar in 2006, accounting for 20.7% of isolations at the time, has reduced considerably over the last decade. Since 2010, the number of isolations has remained relatively low and peaked in 2011 and 2018 with six isolations. In 2019 there were no isolations of S. Typhimurium from turkeys. Figure 7.2 shows the S. Typhimurium phage types identified in turkeys each year from 2015.

Monophasic strains of S. Typhimurium, namely Salmonella 4,5,12:i:- and Salmonella 4,12:i:-, are typically associated with pigs and were first reported from turkeys in 2011. The number of monophasic strains of S. Typhimurium isolated from turkeys was relatively low until 2014, with a maximum of five isolations per year; isolations peaked in 2014 with a total of 20 isolations. Since 2014, the number of monophasic S. Typhimurium isolations decreased, until 2018 when there was a threefold increase from five in 2017 to 15 isolations in 2018. This reduced considerably in 2019 to two isolations of Salmonella 4,5,12:i:- (both phage type DT193) from two turkey breeder flocks from the same premises. Salmonella 4,12:i:- was not isolated from turkeys in 2019 (Figures 7.3 and 7.4).

As in 2018 there were no isolations of S. Enteritidis in 2019, in contrast to 2017 when there was a spike in the number of isolations with 16 reports (3.2% of all isolations). This serovar was not reported from turkeys between 2004 and 2016, with the exception of 2015, when six isolations were reported, all of which were linked to an outbreak of S. Enteritidis PT21 in broiler chickens. However, in 2017 a mixture of phage types were isolated (shown in Figure 7.5), the majority of which seemed to be linked to an outbreak in a hatchery and showed variability in phage type within the same genotype.

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In 2019 there were three serovars isolated from turkeys in GB for the first time; S. Albany was isolated twice, S. Coeln and S. Eastbourne were both isolated once.

National Control Programme for Salmonella in fattening and breeding turkeys The NCP for Salmonella in fattening and breeding turkeys came into effect on 1st January 2010 and has been implemented to comply with Regulation (EC) No. 2160/2003 and Regulation (EC) No. 1190/201223. These regulations aim to protect public health, through a reduction in levels of Salmonella in turkey flocks.

All holdings with 250 or more breeding turkeys and turkey fattening farms with 500 or more fattening turkeys are included in the NCP, unless exempted according to Regulation (EC) No. 2160/2003 under Article 1.3, i.e. fattening birds produced for private domestic consumption, or where there is direct supply of small quantities of products to the final consumer, or, to local retail establishments directly supplying the primary products to the final consumer.

The NCP is implemented via the Control of Salmonella in Turkey Flocks Order 2009 (CSTO) which came into force in England on the 1st January 201024. There is separate national legislation for Scotland25 and Wales26 although there has been close collaboration throughout the development of the legislative proposals and implementation.

Positive flocks identified in the NCP for fattening turkeys in 2019

In GB there were 173 fattening turkey flocks, originating from 71 individual holdings, which were positive for Salmonella spp. in 2019. This is a decrease from 2018, when there were 296 Salmonella-positive flocks from 78 different holdings.

There were no turkey fattening flocks positive for S. Typhimurium or monophasic strains of S. Typhimurium in 2019. This is the first time that there has been no turkey fattening flocks positive for either S. Typhimurium or monophasic strains of S. Typhimurium since the NCP for Salmonella in turkeys started in 2010. In addition, no turkey fattening flocks were positive for S. Enteritidis in 2019, which was also the case in 2018. This was therefore also

23 http://eur-lex.europa.eu/LexUriServ.do?uri=OJ:L:2001:0029:0034:EN:PDF 24 http://www.legislation.gov.uk/uksi/2009/3271/contents/made 25 http://www.opsi.gov.uk/legislation/scotland/ssi2009/ssi_20090417_en_1 26 http://www.opsi.gov.uk/legislation/wales/wsi2010/wsi_20100065_en_1

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the first year since the NCP began that no regulated serovars were isolated from turkey fattening flocks.

A total of 173 flocks tested positive for Salmonella serovars other than S. Enteritidis and S. Typhimurium (including monophasic strains). A comparison of the serovars identified in turkey fattening flocks in the NCP between 2015 and 2019 are shown in Table 7.2 and Figure 7.8 shows the relative percentages of the most common serovars from 2014 to 2019.

Salmonella Derby continued to be the most commonly isolated serovar from turkey fattening flocks in 2019, despite a dramatic reduction from 259 in 2018 to 105 in 2019. Twenty-eight flocks were positive for S. Kedougou in 2019, which is a more than five-fold increase compared to 2018, making it the second most common serovar in turkey fattening flocks in 2019.

Twenty-one flocks were positive for S. Senftenberg, which is almost double the number compared to 2018. Salmonella Agona was isolated from five flocks, a slight decrease compared to seven flocks in 2018. Four flocks were positive for S. Anatum, four flocks were positive for S. Kottbus, and three flocks were positive for the partially typable strain Salmonella 13,23:i:-.

A total of 2,325 turkey fattening flocks were in production in GB in 2019 and were included in the NCP. Therefore, the estimated prevalence for regulated serovars was 0.00% (0/2,325), which is well below the EU target of a maximum of 1% of flocks positive for regulated serovars. The estimated prevalence of Salmonella spp. was 7.44% (173/2,325) in 2019.

Figure 7.6 shows the change in prevalence of turkey fattening flocks testing positive for Salmonella serovars since 2012. With no regulated serovars reported from fattening turkey flocks in 2019, the prevalence of regulated serovars decreased from 0.33% in 2018 to 0.00% in 2019. The prevalence of turkey fattening flocks positive for Salmonella spp. decreased again in 2019 to 7.44%, when compared to 12.13% in 2018, and 15.10% in 2017. The prevalence of Salmonella spp. has remained higher than the level seen in 2014 (3.69%), with the increase mainly attributed to the number of flocks positive for S. Derby.

Positive flocks identified in the NCP for breeding turkeys 2019

A total of 17 adult turkey breeding flocks tested positive for Salmonella serovars in 2019, a slight reduction compared to 22 flocks in 2018. For the second successive year and the second time since the start of the NCP for turkeys in 2010, regulated serovars were isolated from turkey breeding flocks in GB. Two flocks were positive for monophasic S. Typhimurium 4,5,12:i:- DT193, a serovar typically associated with pigs. These two flocks were located on the same turkey breeding premises from which monophasic S. Typhimurium 4,5,12:i:- DT193 was isolated in 2018, and whole genome sequencing confirmed that the same strain was involved. No other flocks were positive for regulated serovars in 2019.

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Fifteen adult turkey breeding flocks tested positive for S. Senftenberg in 2019, during official annual sampling at the same hatchery. This is a slight increase compared with twelve positive flocks in 2018. Salmonella Senftenberg is a known hatchery contaminant, which is not commonly found in breeding birds. Therefore, it is likely that the number of positive flocks reported exceeds the true number of breeding flocks positive at farm level, and represents hatchery contamination rather than truly positive breeding flocks.

For comparison, the serovars identified in the turkey breeder NCP between 2012 and 2019 are shown in Table 7.3 and Figure 7.9 shows the relative percentages of the serovars in the turkey breeder NCP from 2014 to 2019.

A total of 273 adult breeding flocks were in production in GB in 2019 and were included in the NCP. Therefore, the estimated prevalence for regulated serovars was 0.73% (2/273) which is below the EU target of 1% of flocks positive. The estimated prevalence for Salmonella spp. was 6.23% (17/273), which is a slight decrease compared with 7.91% in 2018. Figure 7.7 shows the change in prevalence of turkey breeder flocks testing positive for Salmonella serovars since 2012.

In 2019 three immature turkey breeding flocks tested positive for S. Derby, which had not been observed in breeding flocks since 2016. This was the first time samples from immature turkey flocks had been positive for any Salmonella serovar since 2013, when S. Senftenberg was isolated from two NCP operator samples.

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Table 7.1: Salmonella in turkeys on all premises in Great Britain. (Positive flocks from statutory testing; isolations from both statutory and non-statutory testing)

Salmonella 2015 2015 2016 2016 2017 2017 2018 2018 2019 2019subspecies Flocks Isolations Flocks Isolations Flocks Isolations Flocks Isolations Flocks IsolationsENTERICA ENTERICAAgama - - - 1 - - - - -Agona - 2 4 10 3 7 7 11 5 9Albany - - - - - - - - 1 2Albert - - - - - - 1 1Anatum - - - - - - 2 2 4 4

Bovismorbificans 1 2 5 5 19 27 3 4 - -

Coeln - - - - - - - - - 1

Derby 213 430 339* 501* 257* 351* 259* 401* 105 132

Eastbourne - - - - - - - - 1 1Enteritidis 1 6 - - 4 16 - - - -

Give var. 15+ - 1 - - - - - - - -Gloucester - - 1 1 - - - - - -

Hindmarsh - - - - 1 1 - - - -

Indiana - - 6 7 1 1 - - 1 1Infantis - - - - 1 1 - - - -

Kedougou 36 89 33 56 36 58 5 5 28 44Kottbus 4 5 - - - 1 1 1 4 4

Mbandaka - 2 - 1 - 1 4 6 - 5Montevideo - - - 1 - - - - - -

Newport 6 26 1 5 - - - 5 1 5Nottingham - - - - - - - - 1 1

Ohio - - - - - 1 - - - 1Orion - - - - - 1 - - - -Orion var. 15+ - 1 - - - - - 1 - 1

Senftenberg 1 22 3 3 8 22 24 28 36 48Soerenga - - - - - - - 6 - -

Typhimurium - 2 2 3 - - 4 6 - -

Wangata - - - - - - 1 1 - -

4,5,12:i:- 8 8 3 4 2 3 9 14 2 24,12:i:- - - 1 1 1 2 1 1 - -

UNSPECIFIEDuntypable strains - 9 1 6 2 5 - 2 4 5rough strains 6 13 3 3 - 1 2 2 - 1

TOTAL 272†† 619 401††† 608 330** 499 317*** 497 190∆ 267* Including presumptive S. Derby (266 flocks; 388 isolations in 2016, 187 flocks; 266 isolations in 2017 and 172 flocks; 230 isolations in 2018)

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Table 7.1: Salmonella in turkeys on all premises in Great Britain. (Positive flocks from statutory testing; isolations from both statutory and non-statutory testing)

†† Five f locks tested positive for tw o different Salmonella serovars in 2015. These f locks are included in the table under both serovars but only once in the overall total.††† One f lock tested positive for tw o different Salmonella serovars in 2016. This f lock is included in the table under both serovars but only once in the overall total.** Five f locks tested positive for tw o different Salmonella serovars in 2017. These f locks are included in the table under both serovars but only once in the overall total.

*** Five f locks tested positive for tw o different Salmonella serovars in 2018. These f locks are included in the table under both serovars but only once in the overall total.

∆ Three f locks tested positive for tw o different Salmonella serovars in 2019. These are included in the table under both seerovars but only once in the overall total.

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Figure 7.1: The most common serovars in turkeys by number of isolations* in GB 2015 – 2019

† Including presumptive S . Derby

* Derived from statutory and non-statutory testing.

† Including presumptive S . Derby

† Including presumptive S . Derby

Derby69.5%

Kedougou14.4%

Newport4.2%

Senf tenberg3.6%

4,5,12:i:-1.3%

Enteritidis1.0% Kottbus

0.8% Other serov ars

5.3%

2015 (n=619)

Derby †82.5%

Kedougou9.2%

Agona1.6%

Indiana1.2%

Bov is-morbif icans

0.8%

Newport0.8%

4,5,12:i:-0.7%

Other serov ars

3.1%

2016 (n=607)

Derby †70.3%

Kedougou11.6%

Bov is-morbif icans

5.4%

Senf tenberg4.4%

Enteritidis3.2%

Agona1.4%

4,5,12:i:-0.6%

4,12:i:-0.4% Other

serov ars2.6%

2017 (n=499)

Derby †80.7%

Senf tenberg5.6%

4,5,12:i:-2.8%

Agona2.2%

Mbandaka1.2%

Soerenga1.2%

Ty phimurium1.2% Other

serov ars5.0%

2018 (n=497)

Derby49.4%

Senf tenberg18.0%

Kedougou16.5%

Agona3.4%

Mbandaka1.9%

Newport1.9%

Anatum1.5%

Kottbus1.5%

Other serov ars

6.0%

2019 (n=267)

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Figure 7.2: S. Typhimurium phage types in turkeys in GB 2015- 2019†

Figure 7.3: Salmonella 4,5,12:i:- phage types in turkeys in GB 2015 - 2019†

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Figure 7.4: Salmonella 4,12:i:- phage types in turkeys in GB 2015 - 2019†

Figure 7.5: S. Enteritidis phage types in turkeys in GB 2015 - 2019†

† Flocks from statutory testing; isolations from both statutory and non-statutory testing

0

1

2

3

4

5

Flocks Isolations Flocks Isolations Flocks Isolations Flocks Isolations Flocks Isolations

2015 2016 2017 2018 2019

Num

ber o

f pos

itive

floc

ks/is

olat

ions

DT193

† Flocks from statutory testing; isolations from both statutory and non-statutory testing

0

2

4

6

8

10

12

14

16

18

Flocks Flocks Flocks Flocks Flocks

2015 2016 2017 2018 2019

Num

ber o

f pos

itive

floc

ks/is

olat

ions PT4

PT8

PT13a

PT21

NOPT

RDNC

123

Figure 7.6: Prevalence of Salmonella in turkey fattening flocks tested under NCP in GB 2012 - 2019

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Figure 7.7: Prevalence of Salmonella in turkey breeder flocks tested under NCP in GB 2012 - 2019*

* The absolute number of breeder flocks eligible for NCP testing and positive for Salmonella is relatively small and should thus be borne in mind when interpreting the trends in this figure.

0.00%

2.00%

4.00%

6.00%

8.00%

10.00%

12.00%

14.00%

16.00%

18.00%

20.00%

2012 2013 2014 2015 2016 2017 2018 2019

Pro

porti

on o

f pos

itive

floc

ks

Year

Figure 7.7: Prevalence of Salmonella in turkey breeder flocks tested under NCP in GB 2012 - 2019*

Target forregulatedserovars

Prevalence ofregulatedserovars

Prevalence ofSalmonella spp.

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Table 7.2: Turkey fattening flocks in GB - number of flocks reported positive for each Salmonella serovar, NCP testing 2014 - 2018*

2015 2016 2017 2018 2019RANK SEROVAR N RANK SEROVAR N RANK SEROVAR N RANK SEROVAR N RANK SEROVAR N

1 Derby† 209 1 Derby†† ∆ 336 1 Derby††† ∆ 257 1 Derby** ∆ 259 1 Derby *** 1052 Kedougou† 36 2 Kedougou 33 2 Kedougou††† 36 2 Senftenberg 12 2 Kedougou *** 283 4,5,12:i:- 8 3 Indiana 6 3 Bovismorbificans††† 19 3 Agona 7 3 Senftenberg 214 Newport 6 4 Bovismorbificans 5 4 Enteritidis 4 4 Kedougou** 5 4 Agona *** 5

O Rough:f,g:-† 6 5 Agona 4 5 Agona 3 5 Typhimuirum** 4 5 Anatum 45 Kottbus 4 6 O rough:e,h:1,6 3 Senftenberg 3 6 Bovismorbificans 3 Kottbus 46 Bovismorbificans 1 4,5,12:i:- 3 6 4,5,12:i:- 2 4,5,12:i:-** 3 6 13,23:i:- 3

Enteritidis 1 7 Typhimurium 2 7 Hindmarsh 1 7 Anatum 2 7 Albany 1Senftenberg 1 8 Gloucester 1 Indiana††† 1 8 O rough:f,g:-** 2 Eastbourne 1

Newport 1 Infantis 1 Albert 1 Indiana 1Senftenberg 1 4,12:i:- 1 Kottbus 1 Newport 14,5:12:b:- 1 4,12:rough:- 1 Wangata 1 Nottingham 14,12:i:- 1 13,23:i- 1 4,12:i:- 1 3,10:e,h:- 1

Prevalence all serovars = 10.20% Prevalence all serovars = 17.44% Prevalence all serovars = 15.10%

* For details of turkey fattening flocks reported positive in 2010, 2011, 2012, 2013 and 2014 see the 2015 edition of Salmonella in Livestock Production in GB

∆ Including presumptive S . Derby (266 flocks in 2016, 187 flocks in 2017 and 172 flocks in 2018)

Prevalence regulated serovars = 0.26%

Prevalence regulated serovars = 0.33%

Prevalence regulated serovars = 0.33%

Prevalence regulated serovars = 0.00%

Prevalence regulated serovars = 0.34%

Prevalence all serovars = 7.44%Prevalence all serovars = 12.13%

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Table 7.2: Turkey fattening flocks in GB - number of flocks reported positive for each Salmonella serovar, NCP testing 2014 - 2018* (continued)

† Four flocks tested positive for both S . Derby and S . O Rough:f,g:- and one flock tested positive for both S . Derby and S . Kedougou. Each flock was counted only once in the overall figure to calculate prevalence.

†† One flock tested tested positive for S . Derby and presumptive S . Derby. This is included ony once in the overall total to calculate prevalence.

††† Two flocks tested positive for S . Derby and S . Kedouogu, two flocks tested positive for presumptive S . Derby and S . Bovismorbificans and one flock tested positive for S . Derby and S . Indiana. Each flock was counted only one in the overall figure to calculate prevalence.

** One flock tested positive for S . Derby and S . Kedouogu and one flock tested positive for S . Derby and S . O rough:f,g:-, one flock tested positive for S . Derby and S . 4,12:i:-, one flock tested positive for S . Derby and S . Typhimurium, and one flock tested positive for S . Derby and S . 4,5,12:i:-. Each flock was counted only once in the overall figure to calculate prevalence.

*** Two flocks tested positive for both S . Agona and S . Derby and one flock tested positive for both S . Derby and S . Kedougou. Each flock was counted only once in the overall figure to calculate prevalence.

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Figure 7.8: The most common serovars identified in turkey fattening flocks in GB 2014 - 2019 reported from NCP testing

* 1 flocks positive for 2 serovars (this is counted only once in the total) * 5 flocks positive for 2 serovars (these are counted only once in the total)

* 1 flock positive for 2 serovars (this are counted only once in the total) * 5 flocks positive for 2 serovars (these are counted only once in the total)

∆ including presumptive S . Derby (266 flocks) ∆ including presumptive S . Derby (187 flocks)

* 5 flocks positive for 2 serovars (these are counted only once in the total) * 3 flocks positive for 2 serovars (these are counted only once in the total)

∆ including presumptive S . Derby (172 flocks)

Derby32.5%

Kottbus23.1%

Kedougou22.2%

4,5,12:i:-10.3%

Newport6.8%

Other serov ars

5.1%

2014 (116 positive flocks*)

Derby76.8%

Kedougou13.2%

4,5,12:i:-2.9%

Newport2.2%

O rough:f ,g:-2.2%

Other serov ars

2.6%

2015 (272 positive flocks*)

Derby ∆84.6%

Kedougou8.3%

Indiana1.5%

Bov is-morbif icans

1.3%

Agona1.0% Other

serov ars3.3%

2016 (396 positive flocks*)

Derby ∆77.9%

Kedougou10.9%

Bov is-morbif icans

5.8%

Enteritidis1.2%

Agona0.9%

Senf tenberg0.9% Other

serov ars2.4%

2017 (325 positive flocks*)

Derby ∆86.0%

Senf tenberg4.0%

Agona2.3%

Kedougou1.7%

Ty phimurium1.3%

Other serov ars

4.7%

2018 (296 positive flocks*)

Derby59.7%

Kedougou15.9%

Senf tenberg11.9%

Agona2.8%

Anatum2.3%

Kottbus2.3%

Other serov ars

5.1%

2019 (173 positive flocks*)

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Table 7.3: Turkey breeding flocks in GB - number of adult flocks reported positive for each Salmonella serovar, NCP testing 2015 - 2019*

2012 2013 2014 2015 2016RANK SEROVAR N RANK SEROVAR N RANK SEROVAR N RANK SEROVAR N RANK SEROVAR N

1 Derby 4 1 Kedougou 2 1 Senftenberg 11 1 Derby 4 1 Derby† 32 Mbandaka 1 2 Derby 1 2 Dublin 1 2 Senftenberg 2

Prevalence all serovars = 1.95% Prevalence all serovars = 1.40% Prevalence all serovars = 4.91%

† Including presumptive S . Derby (1 flock)

2017 2018 2019RANK SEROVAR N RANK SEROVAR N RANK SEROVAR N

1 Senftenberg 5 1 Senftenberg 12 1 Senftenberg 152 4,5,12:i:- 6 2 4,5,12:i:- 23 Mbandaka 4

Prevalence all serovars = 2.09%

* For details of turkey breeding flocks reported positive in 2010 and 2011 see the 2015 edition of Salmonella in Livestock Production in GB

Prevalence all serovars = 7.91% Prevalence all serovars = 6.23%

Prevalence regulated serovars = 0.00%

Prevalence regulated serovars = 2.16%

Prevalence regulated serovars = 0.73%

Prevalence all serovars = 2.24%

Prevalence regulated serovars = 0.00%

Prevalence regulated serovars = 0.00%

Prevalence regulated serovars = 0.00%

Prevalence regulated serovars = 0.00%

Prevalence regulated serovars = 0.00%

Prevalence all serovars = 2.04%

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Figure 7.9: Serovars identified in adult turkey breeding flocks in GB 2014 - 2019 reported from NCP testing

† One flock positive for presumptive S . Derby

Senf tenberg100.0%

2014 (11 positive flocks)

Derby80.0%

Dublin20.0%

2015 (5 positive flocks)

Derby †60.0%

Senf tenberg40.0%

2016 (5 positive flocks)

Senf tenberg100.0%

2017 (5 positive flocks)

Senf tenberg54.5%

4,5,12:i:-27.3%

Mbandaka18.2%

2018 (22 positive flocks)

Senf tenberg88.2%

4,5,12:i:-11.8%

2019 (17 positive flocks)

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Chapter 8: Reports of Salmonella in ducks and geese Ducks

During 2019 there were 293 isolations of Salmonella from ducks in GB, which is 31.9% fewer than during 2018 (430 isolations) and 25.8% fewer than during 2017 (395 isolations) (Table 8.1). Reports from ducks made up 9.6% of total Salmonella isolations from livestock species (cattle, sheep, pigs, chickens, turkeys and ducks) in 2019 which is slightly lower than in 2018 (12.2%), 2017 (14.4%) and 2016 (13.4%). Whilst there is a voluntary Duck Assurance Scheme in place in Great Britain, there are no statutory monitoring requirements for Salmonella in ducks or geese. There has been increased voluntary surveillance activity within the duck industry in recent years, but this appears to have decreased during 2019.

Salmonella Indiana remained the most commonly reported serovar from ducks during 2019 (93 isolations). Although there were fewer isolations compared to 2018 (123 isolations) and 2017 (117 isolations), this serovar accounted for a slightly higher proportion of total isolations from ducks in 2019 (31.7%) compared to previous years (28.6% in 2018 and 29.6% in 2017) (Figure 8.1).

Salmonella Give var. 15+ has been the second most common serovar reported from ducks each year since 2014, with the exception of 2018 when it was the third most common (Figure 8.1). During 2019, there were 53 isolations (18.1% of total isolations) which is a similar number to 2018 (55 isolations; 12.8% of total isolations) but lower than 2017 (70 isolations; 17.7% of total isolations).

The increase in isolations of S. Give from ducks that was seen in 2018 (56 isolations) was not sustained during 2019 and isolations of this serovar instead declined in number (11 isolations) to a level more similar to that seen prior to 2018 (Table 8.1; Figure 8.1).

The number of S. Hadar isolations fell slightly compared with 2018 (39 isolations vs. 44 isolations) but was still higher than during both 2017 (26 isolations) and 2016 (23 isolations).

Isolations of S. Kottbus fell for the second year running (11 isolations in 2019 vs. 24 isolations in 2018 and 47 isolations in 2017) and were now at their lowest level since 2015 (4 isolations). The number of S. Orion isolations in 2019 also more than halved compared to 2018 (15 vs. 36 isolations) resulting in the lowest number of isolations seen in ducks since 2011 (2 isolations). As in 2018, there were no isolations of S. Mbandaka; prior to 2018 there were reports of S. Mbandaka from ducks in GB each year from 2006.

There were only two isolations of S. Typhimurium from ducks in 2019 (both were phage type UNTY). This is fewer than in the preceding two years (11 isolations in 2018 and 5 isolations in 2017) and represents <1% of total Salmonella isolations from ducks in GB.

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Isolations of S. Typhimurium from ducks have decreased substantially since 2011 when there were 56 isolations representing 77.8% of total isolations. It is thought that this overall reduction may be associated with the inception of the duck assurance scheme in 2010.

There were no isolations of Salmonella 4,12:i:- from ducks during 2019 compared with one isolation (DT120) in 2018 and no isolations in either 2017 or 2016. Salmonella 4,5,12:i:- has not been isolated from ducks since 2010.

There were no isolations of S. Enteritidis from ducks in 2019, the same as during 2018 and compared with one isolation (PT9b) in 2017 (Figure 8.4). There were also no isolations of S. Newport compared with three isolations in 2018 and one isolation in 2017.

Geese

There were no isolations of Salmonella from geese in 2019 compared with four isolations in 2018, six isolations in 2017 and four isolations in 2016 (Table 8.2).

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Table 8.1: Isolations and incidents of Salmonella in ducks on all premises in Great Britain

Salmonella 2015 2015 2016 2016 2017 2017 2018 2018 2019 2019subspecies Isolations Incidents Isolations Incidents Isolations Incidents Isolations Incidents Isolations IncidentsENTERICA ENTERICAAjiobo 1 1 - - - - - - - -Albert - - - - - - 1 1 - -Anatum 1 1 - - - - - - 1 1

Bovismorbificans 10 8 13 12 5 5 8 8 8 5Bredeney 1 1 - - - - - - - -

Derby - - - - - - 2 2 1 1

Enteritidis 5 4 - - 1 1 - - - -

Give 21 18 10 10 18 16 56 20 11 9Give var. 15+ 43 35 57 49 70 53 55 36 53 41

Hadar 24 21 23 21 26 20 44 34 39 36

Indiana 110 90 97 76 117 88 123 95 93 79Infantis 1 1 - - - - - - - -Istanbul - - - - - - 1 1 - -

Kedougou 1 1 4 4 2 2 - - - -Kottbus 4 4 15 10 47 23 24 17 11 9

Lexington - - 9 2 26 12 6 5 2 2

Mapo - - - - - - 1 1 - -Mbandaka 10 10 13 10 16 12 - - - -Monschaui 4 4 4 4 3 3 4 4 4 4

Newport - - - - 1 1 3 3 - -

Orion 28 28 37 31 26 18 36 22 15 13Orion var. 15+ 25 24 35 28 20 18 34 32 36 32Oslo - - - - - - 3 3 9 8

Panama - - 4 4 - - - - - -

Rissen - - - - - - 1 1 - -

Senftenberg 1 - 1 - - - - - - -

Typhimurium 3 2 2 1 5 5 11 5 2 2

Vichow 1 1 - - - - - - - -

4,12:i:- - - - - - - 1 1 - -

UNSPECIFIEDuntypable strains 9 9 6 6 11 11 15 13 6 5rough strains 7 7 4 4 1 1 1 1 2 2

TOTAL 310 270 334 272 395 289 430 305 293 249

133

Table 8.2: Isolations and incidents of Salmonella in geese on all premises in Great Britain

Salmonella 2015 2015 2016 2016 2017 2017 2018 2018 2019 2019subspecies Isolations Incidents Isolations Incidents Isolations Incidents Isolations Incidents Isolations IncidentsENTERICA ENTERICAIndiana - - - - - - 2 2 - -

Kottbus - - - - - - 1 1 - -

4,12:i:- - - 4 1 6 3 1 - - -

TOTAL - - 4 1 6 3 4 3 - -

134

Figure 8.1: Isolations of the most common serovars in ducks in GB 2015 – 2019

Indiana35.5%

Giv e v ar. 15+

13.9%Orion 9.0%

Orion v ar. 15+

8.1%

Hadar7.7%

Giv e6.8%

Bov is-morbif icans

3.2%

Mbandaka3.2%

Enteritidis1.6%

Kottbus1.3%

Monschaui1.3%

Other serov ars

8.4%

2015 (n=310)

Indiana29.0%

Giv e v ar. 15+

17.1%Orion 11.1%

Orion v ar. 15+

10.5%

Hadar6.9%

Kottbus4.5%

Bov is-morbif icans

3.9%

Mbandaka3.9%

Giv e 3.0%

Lexington2.7%

Other serov ars

7.5%

2016 (n=334)

Indiana29.6%

Giv e v ar. 15+

17.7%Kottbus11.9%

Hadar6.6%

Lexington6.6%

Orion6.6%

Orion v ar. 15+

5.1%

Giv e4.6%

Mbandaka4.1%

Other serov ars

7.3%2017 (n=395)

Indiana28.6%

Giv e13.0%

Giv e v ar. 15+

12.8%

Hadar10.2%

Orion8.4%

Orion v ar. 15+

7.9%

Kottbus5.6%

Ty phimuirum2.6%

Bov is-morbif icans

1.9%

Other serov ars

9.1%

2018 (n=430)

Indiana31.7%

Giv e v ar. 15+

18.1%Hadar13.3%

Orion v ar. 15+

12.3%

Orion5.1%

Giv e 3.8%

Kottbus3.8%

Oslo3.1%

Bov is-morbif icans

2.7%

Other serov ars

6.1%2019 (n=293)

135

Figure 8.2: S. Enteritidis, S. Indiana, S. Typhimurium, monophasic variant S. Typhimurium and other serovars as a proportion of all isolations in ducks in GB (1999 - 2019)

136

Figure 8.3: S. Typhimurium phage types in ducks and geese in GB 2015 – 2019

137

Figure 8.4: S. Enteritidis phage types in ducks and geese in GB 2015 – 2019

138

Figure 8.5: Salmonella 4,12:i:- phage types in ducks and geese in GB 2015 - 2019

139

Chapter 9: Reports of Salmonella in other statutory birds Other statutory birds comprise guinea fowl, partridges, pheasants, pigeons and quail. A total of 29 isolations of Salmonella were reported from these species during 2019, which is similar to 2018 (26 isolations) but 27.5% lower than 2017 (40 isolations).

Game birds The total number of VIDA submissions from game birds (pheasants, guinea fowl, partridges and quail) to APHA/SRUC fell by 23.7% to 187 submissions in 2019, compared to 245 in 2018. As in previous years, the greatest number of submissions were from pheasants, although this fell compared with 2018 (150 vs. 193 submissions). There were also 52 submissions from grouse, which was a decrease of 26.8% compared with 2018 (71 submissions) and 21 submissions from partridges, which was almost half that reported during 2018 (41 submissions). In contrast, submissions from quail increased compared with 2018 (8 vs. 3 submissions), and there was one submission from guinea fowl, which was the same as the previous year. A further seven submissions were from birds reported as ‘other game’, which is the same as during 2018.

There is no statutory Salmonella monitoring of game birds in Great Britain and the majority of submissions in 2019 were for diagnostic purposes (83.7%), which is similar to 2018 (87.2%).

The number of Salmonella isolations from game birds during 2019 was very similar to 2018 (18 isolations vs. 17 isolations) but 30.8% lower than in 2017 (25 isolations). The number of isolations from pheasants fell slightly compared with 2018 (8 isolations vs. 10 isolations), but the number of isolations from quail more than doubled (5 isolations vs. 2 isolations).There were also five isolations from partridges and no isolations from guinea fowl, which is the same as during both 2018 and 2017.

Salmonella Senftenberg was the most commonly reported serovar in 2019 (9 isolations; 50.0% of total isolations from game bird isolations) and S. Bredeney, which has never previously been reported from game birds, was the second most common (3 isolations 16.7% of total game birds); all three isolations of S. Bredeney were from voluntary surveillance in quail. There was only one isolation of S. Typhimurium (DT2 from pheasants; Figure 9.2) during 2019 compared with eight isolations in 2018 and six isolations in 2017. Salmonella 4,12:i:- was reported during 2019 (1 isolation from partridges) having never previously been reported from game birds in GB. There was also one isolation of S. Enteritidis from game birds this year (PT9b from quail). Salmonella Enteritidis was last isolated from game birds in 2017 (1 isolation of phage type UNTY from pheasants).

140

Guinea Fowl

There were no isolations of Salmonella from guinea fowl in 2019, the same as in 2018 and 2017. The last isolation from guinea fowl was in 2015 (S. Indiana) (Table 9.1).

Partridges

Five isolations of Salmonella were reported from partridges during 2019, the same as during both 2018 and 2017 (Table 9.2). There were three isolations of S. Senftenberg, two from voluntary surveillance and one from clinical disease (no presenting signs were available) and single isolations each of S. Soerenga and monophasic Salmonella Typhimurium 4,12:i:- DT193 from voluntary surveillance. Salmonella 4,12:i:- has never previously been reported from partridges in GB. There were no reports of S. Typhimurium from partridges during 2019 compared with two isolations during 2018.

Pheasants

The number of isolations of Salmonella from pheasants fell by 20.0% compared with 2018 (8 isolations vs. 10 isolations) and by 60.0% compared with 2017 (20 isolations); this is the lowest number of isolations from pheasants since 2011 when there were nine isolations (Table 9.3). The serovars reported were S. Senftenberg (5 isolations), S. Orion var. 15+ (2 isolations) and S. Typhimurium DT2 (1 isolation) (Table 9.3 and Figure 9.2). All isolations were from voluntary surveillance with the exception of a single isolation of S. Senftenberg which was from clinical disease (the presenting sign was recorded as ‘other’).

There were no isolations of S. Pullorum from pheasants during 2019, compared with one isolation in 2018. This serovar is likely to be present at a low level in the game bird population.

Quail

There were five isolations of Salmonella from quail in 2019 compared with two isolations in 2018 and none in 2017; the serovars reported were S. Bredeney (3 isolations), S. Enteritidis PT9b (1 isolation) and S. Senftenberg (1 isolation), all of which were from voluntary surveillance. None of these serovars have previously been reported from quail in GB (Table 9.4).

Pigeons There were 52 submissions from pigeons to APHA/SRUC in 2019 which is 73.3% higher than during 2018 (30 submissions) and 57.6% higher than in 2017 (33 submissions), but similar to 2016 (54 submissions).

There were eleven Salmonella isolations from pigeons in 2019 (Table 9.5) which is 22.2% higher than in 2018 (9 isolations) but a decrease of 26.7% compared with 2017 (15

141

isolations). All eleven isolations were S. Typhimurium, which is consistently the most commonly isolated serovar from pigeons. The phage types reported were DT2 (5 isolations), DT99 (3 isolations) and DT193 (3 isolations). Phage type DT193 was last isolated from pigeons in GB in 2017 (1 isolation) but prior to this was last reported from pigeons in 2013 (1 isolation) (Figure 9.4). Monophasic Salmonella Typhimurium 4,12:i:-, which was reported during 2018 for the first time since 2013, was not reported from pigeons during 2019.

142

Table 9.1: Isolations and incidents of Salmonella in guinea fowl on all premises in Great Britain

Table 9.2: Isolations and incidents of Salmonella in partridges on all premises in Great Britain

Salmonella 2015 2015 2016 2016 2017 2017 2018 2018 2019 2019subspecies Isolations Incidents Isolations Incidents Isolations Incidents Isolations Incidents Isolations IncidentsENTERICA ENTERICAIndiana 1 1 - - - - - - - -

TOTAL 1 1 - - - - - - - -

Salmonella 2015 2015 2016 2016 2017 2017 2018 2018 2019 2019subspecies Isolations Incidents Isolations Incidents Isolations Incidents Isolations Incidents Isolations IncidentsENTERICA ENTERICADerby 1 1 - - - - - - - -

Kedougou - - 1 1 - - - - - -

Newport - - 1 1 - - - - - -

Orion var. 15+ - - 4 4 1 1 1 1 - -Orion var. 15+ 34+ 2 2 - - - - - - - -

Senftenberg 1 1 1 1 3 3 1 1 3 3Soerenga - - - - 1 1 1 1 1 1

Typhimurium 2 2 - - - - 2 - - -

4,12:i:- - - - - - - - - 1 1

TOTAL 6 6 7 7 5 5 5 3 5 5

143

Table 9.3: Isolations and incidents of Salmonella in pheasants on all premises in Great Britain

Salmonella 2015 2015 2016 2016 2017 2017 2018 2018 2019 2019subspecies Isolations Incidents Isolations Incidents Isolations Incidents Isolations Incidents Isolations IncidentsENTERICA ENTERICADublin - - 1 1 - - - - - -

Enteritidis - - - - 1 1 - - - -

Give var. 15+ 1 - - - - - - - - -

Indiana 1 1 - - - - - - - -

Kedougou - - 2 2 - - - - - -

Orion 1 1 3 2 1 1 - - - -Orion var. 15+ 8 5 3 1 2 2 1 1 2 2Orion var. 15+ 34+ 1 1 - - - - - - - -

Pullorum 2 2 - - - - 1 1 - -

Senftenberg 1 1 - - 8 6 4 4 5 5

Tennessee 1 1 2 2 - - - -Typhimurium 17 15 3 2 6 4 4 2 1 1

UNSPECIFIEDuntypable strains - - 1 1 - - - - - -rough strains 1 1 - - - - - - - -

TOTAL 34 28 13 9 20 16 10 8 8 8

144

Table 9.4: Isolations and incidents of Salmonella in quail on all premises in Great Britain

Table 9.5: Isolations and incidents of Salmonella in pigeons on all premises in Great Britain

Salmonella 2015 2015 2016 2016 2017 2017 2018 2018 2019 2019subspecies Isolations Incidents Isolations Incidents Isolations Incidents Isolations Incidents Isolations IncidentsENTERICA ENTERICABredeney - - - - - - - - 3 2

Enteritidis - - - - - - - - 1 1

Infantis 1 1 - - - - - - - -

Senftenberg - - - - - - - - 1 1

Typhimurium 3 2 3 2 - - 2 2 - -

TOTAL 4 3 3 2 - - 2 2 5 4

Salmonellasubspecies Isolations Incidents Isolations Incidents Isolations Incidents Isolations Incidents Isolations IncidentsENTERICA ENTERICADerby - - 1 1 - - - - - -Dublin - - 1 1 - - - - - -

Panama - - 1 1 - - - - - -

Senftenberg - - 1 1 - - - - - -

Typhimurium 23 21 24 24 15 14 7 6 11 11

4,12:i:- - - - - - - 2 2 - -

TOTAL 23 21 28 28 15 14 9 8 11 11

2015 2016 2017 2018 2019

145

Figure 9.1: S. Typhimurium phage types in partridges in GB 2015 - 2019

146

Figure 9.2: S. Typhimurium phage types in pheasants in GB 2015 - 2019

147

Figure 9.3: S. Typhimurium phage types in quail in GB 2015 - 2019

148

Figure 9.4: S. Typhimurium phage types in pigeons in GB 2015 - 2019

149

Figure 9.5: Salmonella 4,12:i:- phage types in partridges in GB 2015 - 2019

150

Chapter 10: Reports of Salmonella in wildlife There is no routine monitoring of Salmonella in wild birds or wild mammals, therefore isolates usually originate from clinical cases or occasionally from small-scale surveys. Salmonella is not necessarily the primary cause of disease when identified in wild birds. Salmonella is voluntarily reportable for most species of wildlife, unless the species is covered by the Zoonoses Order, although in practice, very few wildlife submissions are received by APHA for Salmonella testing.

Wild Mammals There were three isolations of S. Enteritidis PT11 from hedgehogs (Erinaceus europaeus) in 2019. The hedgehogs were in different rescue centres at the time of death. The rescue centres were not linked. The isolates were fully sensitive to the standard APHA antibiotic susceptibility testing panel. Salmonella Enteritidis PT11 is the most common Salmonella isolation from hedgehogs. It is widespread in hedgehogs in England (Keymer and others, 1991) and appears to be endemic in this species (Robinson & Routh, 1999).

The first of these S. Enteritidis PT11 isolations was from a uterine swab from an adult hedgehog. The animal had died during hibernation at a rescue centre and was submitted for postmortem examination which revealed a pyometra with small abscesses within the lymph nodes associated with the reproductive tract and an enlarged spleen. The second isolation was from the lung and liver from an immature hedgehog confirming a Salmonella septicaemia. The animal had been submitted for postmortem examination with a short history of diarrhoea prior to death. Cryptosporidium spp. was isolated from the faeces. The third isolation was from a liver swab from an immature hedgehog. Multiple immature hedgehogs in the same group had diarrhoea.

There was also a single isolation of S. Enteritidis PT183 from a hedgehog in 2019. No additional information is available regarding this case. Salmonella Enteritidis PT183 is an emerging phage type isolated from hedgehogs from rescue centres in Scotland. It is associated with relatively distinctive pathology in the animal, in that the mesenteric lymph nodes are very enlarged. The human Salmonella authority in Scotland have recorded a small number of similar phage types from humans in Scotland.

In addition to the above, S. Newport was isolated from the carcase of a free-living racoon dog (Nyctereutes procyonoides). The carcase was a macerated road traffic victim found by the police near Matlock Derbyshire. This is one of a number of raccoon dogs (up to 20 individuals) believed to have escaped or been illegally released in the area. This isolation is not included in the tables or figures of this chapter.

151

Wild Birds No Salmonella was isolated from any wild bird species submitted to APHA Diseases of Wildlife Scheme during 2019.

Our partners in the Great Britain Wildlife Disease Surveillance Partnership (GWDSP) Garden Wildlife Health (GWH) carry out the majority of disease surveillance in garden birds and hedgehogs and report Salmonella isolations separately. The GWH is a collaborative project between Zoological Society of London (ZSL), the British Trust for Ornithology (BTO), Froglife and the Royal Society for the Protection of Birds (RSPB), and it is part funded by Defra, Welsh Government and the Animal and Plant Health Agency (APHA) Diseases of Wildlife Scheme (DoWS).

152

Figure 10.1: Isolations of Salmonella in wild mammals in GB 2015 - 2019

153

Figure 10.2: Isolations of Salmonella in wild birds in GB 2015 - 2019

Table 10.1: Isolations and incidents of Salmonella in wild mammals in Great Britain in 2019

Enteritidis PT11 Enteritidis PT11 Enteritidis PT183 Enteritidis PT183Isolations Incidents Isolations Incidents

Hedgehog 3 3 1 1

TOTAL 3 3 1 1

Species

154

Chapter 11: Salmonella in animal feedingstuffs and products tested under ABPR The total number of animal feedingstuffs and ingredients tested during 2019 (32,063) fell by 10.7% compared with 2018 (35,903 tests) and by 26.2% compared to 2017 (43,441 tests) (Figure 11.1). There was an increase in the number of tests performed on five product types compared with 2018: pig extrusions (26 tests vs. 0 tests in 2018), protein concentrates (77 vs. 28 tests), poultry extrusions (196 vs. 128 tests), non-oilseed meal vegetable products (3,194 vs. 2,827 tests) and processed animal protein for feedingstuffs use (9,321 vs. 9,267 tests). The number of tests of minerals/vitamins was almost the same as in 2018 (264 isolations vs. 263 isolations) and all other product types showed a decrease in the number of tests compared with 2018. The greatest fall was in processed animal protein from GB premises (11,381 vs. 14,694 tests); there were also sizeable declines in the number of tests conducted on ruminant concentrates (1,119 vs. 1,372 tests) and oilseed meals and products (3,356 vs. 3,875 tests). The percentage of total positive tests decreased to 1.7% compared with 1.9 % in 2018 but showed an increase compared to 1.3% in 2017 (Figure 11.2).

There were 713 isolations of Salmonella from feedingstuffs (91 from compound feeds and 622 from feed ingredients or other associated products) during 2019. This was an increase of 13.7% compared with 2018 (627 isolations) and just over one-and-a-half times that reported during 2017 (470 isolations).

The number of regulated serovars reported from animal feedingstuffs and products tested under the ABPR increased by 39.7% in 2019 compared with 2018 (88 isolations vs. 63 isolations) and was almost three times that reported during 2017 (31 isolations) (Table 11.1). In 2019, these comprised 35 reports of S. Typhimurium, 20 reports of Salmonella 4,12:i:-, eleven reports of S. Infantis, eleven reports of Salmonella 4,5,12:i:-, seven reports of S. Enteritidis and four reports of S. Hadar. See Tables 11.1 and 11.2 for further details.

Compared with 2018, there was an increase in the number of Salmonella isolations from several different feedingstuffs and products controlled under the Animal By-Products Regulations (ABPR)27 including pet food intended to be fed raw (245 vs. 188), feedmill environment (123 vs. 104) and rendering plant material (35 vs. 0) (Tables 11.8a and 11.8b). In contrast, isolations of Salmonella from mixed oil seeds and meat meal fell (4 vs. 26 and 2 vs. 28), respectively. There was only one isolation of Salmonella 13,23:i:- from

27 http://www.legislation.gov.uk/uksi/2011/881/pdfs/uksi_20110881_en.pdf

155

compound poultry feed during 2019; this serovar is very common in broiler flocks and breeding flocks which suggests that there may not be a link with feed.

During 2019, reports from sunflower seed (8 isolations) were double that in 2018 (4 isolations) and much higher than during 2017 (1 isolation) and the number of reports from compost (12 isolations) increased by 71.4% compared to 2018 and 2017 (both 7 isolations). See Tables 11.8a and 11.8b for details.

The total number of Salmonella isolations reported from compound ruminant, pig and poultry feed and animal feedingstuff ingredients and products is listed in Tables 11.3, 11.4, 11.5 and 11.7, respectively. Salmonella was also isolated from compound feed intended for feeding to several non-statutory species including cats, dogs and fish. Table 11.6 gives details of the serovars isolated.

The most commonly reported serovar from compound ruminant feed during 2019 was S. Senftenberg, with three reports (30.0% of isolations from compound ruminant feed). There were also seven further serovars reported, each of which made up 10% of total isolations (1 isolation each) from compound ruminant feed (Table 11.3). Salmonella Senftenberg was not reported from cattle or sheep during 2019 (Figure 11.6).

There were only four isolations of Salmonella from compound pig feed during 2019; single isolations of S. Derby, S. Senftenberg, S. Tennessee and Salmonella 13,23:i:- (25% of total each). Salmonella Senftenberg, S. Tennessee and Salmonella 13,23:i:- were not reported from pigs in 2019, but there were six isolations of S. Derby from pigs (Figure 11.7). Salmonella Derby was not reported from compound pig feed during 2018 or 2017 (Table 11.4).

There were 48 reports of Salmonella from compound poultry feed during 2019 which was similar to 2018 when there were 46 reports, but 60.0% higher than in 2017 (30 reports) (Table 11.5). Twenty-one different serovars were reported, the most common being S. Senftenberg (8 reports; 16.7% of isolations from compound poultry feed), S. Ohio (6 reports; 12.5% of isolations), and S. Kedougou and S. Tennessee (5 reports each; 10.4% of total isolations each). A comparison of the serovars recovered from compound poultry feed and the most common serovars found in chickens and turkeys tested under the NCP is shown in Figure 11.8. Many of the serovars reported from compound poultry feed were also seen in poultry, and especially in the breeding and production meat sectors. These included S. Kedougou (in broiler chicken flocks, layer chicken flocks and turkey flocks), S. Ohio (in breeding chicken flocks and broiler chicken flocks), and S. Senftenberg (in turkey flocks). There is a more direct relationship between feed contamination and poultry isolates than for other livestock species, for which breeding animals and animal movements are the predominant sources. The voluntary and statutory monitoring programmes for poultry will also detect subclinical infection, which is the usual situation in poultry.

During 2019 there were 245 reports of Salmonella from pet food which was intended to be fed raw (Table 11.8b). This is higher than in 2018 (188 reports) and 2017 (160 reports).

156

The most common serovars reported during 2019 were S. Indiana (31 isolations), S. Derby (14 isolations), S. Mbandaka (14 isolations) and S. Bovismorbificans (12 isolations). In comparison the most common serovars during 2018 and 2017 was S. Indiana (20 isolations and 33 isolations, respectively). The range of serovars found in raw meat pet foods often reflects that found in the animal species whose meat is used in the recipe.

Regulated serovars originating from raw pet food during 2019 accounted for 43.2% of total regulated serovars from all feedingstuffs and products associated with the ABPR. This was lower than in 2018 (56% of total regulated serovars) and 2017 (61% of total regulated serovars).

During 2019, there were 38 reports of regulated serovars from raw pet food (Table 11.2) compared with 35 reports in 2018 and 19 reports in 2017. The serovars reported were eleven isolations of S. Typhimurium (DT2 (x1), DT104 (x5), NOPT (x3) and UNTY (x2)), eleven isolations of Salmonella 4,12:i:- (DT193 (x8), NOPT (x1) and UNTY (x2)), nine isolations of Salmonella 4,5,12:i:- (DT193 (x7), NOPT (x1) and UNTY (x1)), three isolations of S. Enteritidis (single isolations of PT1, PT4 and RDNC), three isolations of S. Hadar and one isolation of S. Infantis. See Table 11.8b for details.

The most commonly reported serovars from animal feedingstuffs and compound feeds during 2019 were S. Tennessee (60 isolations), S. Senftenberg (47 isolations) and S. Ohio (42 isolations) (Tables 11.3, 11.4, 11.5, 11.6 and 11.7). This is similar to 2018 when the most commonly reported serovars were S. Tennessee (50 isolations), S. Senftenberg (48 isolations) and S. Rissen (38 isolations).

The majority of S. Tennessee isolations were from rape seed (46/60 isolations) with further isolations from a variety of other products (Tables 11.3, 11.4, 11.5, 11.8a and 11.8b). The reports of S. Senftenberg were from ten different sample types with the greatest number coming from feedmill environmental samples (16 isolations) (Tables 11.3, 11.4, 11.5, 11.8a and 11.8b). Salmonella Ohio was reported mainly from feedmill environment samples (25 isolations) (Tables 11.3, 11.4, 11.8a and 11.8b).

In total, 648 batches of domestically-produced processed animal protein were tested for Salmonella during 2019 (Table 11.9). This was a decrease of 2.3% and 17.6%, respectively, compared with the number of batches tested in 2018 and 2017 (663 batches in 2018 and 786 batches in 2017). There were eleven Salmonella-positive batches in 2019 (1.7% of all tested batches), which is higher than in both 2018 (3 positive batches; 0.5%) and 2017 (10 positive batches; 1.3%). The serovars reported during 2019 are shown in Table 11.10. There were no regulated serovars reported from this category of material in 2019.

No batches of imported animal protein were tested for Salmonella during 2019. This was also true in both 2018 and 2017 (see Table 11.11). The last time a batch of imported animal protein tested positive for Salmonella was in 2009 (Figure 11.9).

157

Figure 11.1: Animal feedingstuffs and ingredients in GB (tests performed under the ABP (Enforcement) Regulations 2013 and Defra Codes of Practice) 2015 - 2019

158

Figure 11.2: Animal feedingstuffs and ingredients in GB contamination rate 2015 - 2019

159

Table 11.1: Regulated Salmonella serovars in animal feedingstuffs in Great Britain 2017 – 2019

Salmonella serovar

Finished feedVegetable material Misc. Finished feed

Vegetable material Misc. Finished feed

Vegetable material Misc.

Enteritidis PT1 - - - - - - - 1 1Enteritidis PT2 - - - - - - - 1 -Enteritidis PT3b - - - - 1 - - - -Enteritidis PT4 - - - - - - - - 1Enteritidis PT8 - - - - - 1 - - 1Enteritidis NOPT - - - - - 2 - - 1Enteritidis RDNC - - - - - - - - 1Enteritidis UNTY - - 1 - - - - - -

Hadar - - - - - - 1 - 3

Infantis - 1 10 5 3 10 1 - 10

Typhimurium DT1 - - 1 - - - - - -Typhimurium DT2 - - 1 - - - - - 1Typhimurium DT12 - - - - - 2 - - -Typhimurium DT35 - - - - - 2 - - -Typhimurium DT73 - - - - - - - - 2Typhimurium DT99 - 1 - - 1 - - - -Typhimurium DT104 - - 2 - - 1 - - 16Typhimurium DT193 - - 2 - 1 - 1 2 1Typhimurium DT204e - - - - - 1 - - -Typhimurium U288 - - - - - 2 - - -Typhimurium U302 - - - - 2 2 - - -Typhimurium NOPT - - - - - 5 1 - 4Typhimurium RDNC - - - - - 2 - - -Typhimurium UNTY - - - - - - - - 7

4,5,12:i:- DT12 - - - - - 1 - - -4,5,12:i:- DT40 - 1 - - - - - - -4,5,12:i:- DT193 - - 1 - - 10 - - 94,5,12:i:- NOPT - - - - - - - - 14,5,12:i:- UNTY - - - - - - - - 1

Type of material - 2018 Type of material - 2019Type of material - 2017

160

Table 11.1: Regulated Salmonella serovars in animal feedingstuffs in Great Britain 2017 – 2019 - continued

Salmonella serovar

Finished feedVegetable material Misc. Finished feed

Vegetable material Misc. Finished feed

Vegetable material Misc.

4,12:i:- DT193 - - 5 - - 4 2 1 114,12:i:- DT208 - - 1 - - - - - -4,12:i:- U311 1 - 1 - - 1 - - -4,12:i:- NOPT - - - - - 4 - 1 24,12:i:- UNTY - - 2 - - 3

TOTAL 1 3 27 5 8 50 6 6 76

Misc. - miscellaneous

Type of material - 2017 Type of material - 2018 Type of material - 2019

161

Table 11.2: Isolations of Salmonella serovars considered to be of special public health importance from products monitored in Great Britain under the Defra Codes of Practice, 2019

Salmonella serovar Feedingstuff NEnteritidis PT1 Pet food (raw) 1Enteritidis PT1 Rape seed 1Enteritidis PT2 Wheat 1Enteritidis PT4 Pet food (raw) 1Enteritidis PT8 Environmental 1Enteritidis NOPT Malt 1Enteritidis RDNC Pet food (raw) 1

Hadar Compound dog feed 1Hadar Pet food (raw) 3

Infantis Compound feed - unspecified species 1Infantis Environmental 8Infantis Pet food (raw) 1Infantis Rendering plant material 1

Typhimurium DT2 Pet food (raw) 1Typhimurium DT73 Environmental 1Typhimurium DT73 Meat and bone meal 1Typhimurium DT104 Environmental 1Typhimurium DT104 Pet food (raw) 5Typhimurium DT104 Rendering plant material 10Typhimurium DT193 Compound chicken feed 1Typhimurium DT193 Environmental 1Typhimurium DT193 Soya 2Typhimurium NOPT Compound fish feed 1Typhimurium NOPT Pet food (raw) 3Typhimurium NOPT Rendering plant material 1Typhimurium UNTY Environmental 4Typhimurium UNTY Pet food (raw) 2Typhimurium UNTY Rendering plant material 1

4,5,12:i:- DT193 Pet food (raw) 74,5,12:i:- DT193 Rendering plant material 24,5,12:i:- NOPT Pet food (raw) 14,5,12:i:- UNTY Pet food (raw) 1

4,12:i:- DT193 Compound dog feed 24,12:i:- DT193 Environmental 14,12:i:- DT193 Malt 14,12:i:- DT193 Pet food (raw) 84,12:i:- DT193 Rape seed 14,12:i:- DT193 Rendering plant material 14,12:i:- NOPT Environmental 14,12:i:- NOPT Herbs 14,12:i:- NOPT Pet food (raw) 14,12:i:- UNTY Environmental 14,12:i:- UNTY Pet food (raw) 2

TOTAL 88

162

Figure 11.3: Number of isolations of regulated Salmonella serovars in animal feedingstuffs and products associated with the ABPR 2015 - 2019 by type of feedingstuff

163

Figure 11.4: Number of isolations of regulated Salmonella serovars in animal feedingstuffs and products associated with the ABPR 2015 – 2019

164

Figure 11.5: Number of isolations of Salmonella in compound animal feedingstuffs 2015 – 2019

Table 11.3: Serovars of Salmonella isolated from compound ruminant feed in Great Britain in 2019, compared with the previous two years

Salmonella serovar Isolations Salmonella serovar Isolations Salmonella serovar Isolations2017 2018 2019

Tennessee 4 Tennessee 4 Senftenberg 3Idikan 2 Idikan 2 Idikan 1Liverpool 2 Kentucky 2 Mbandaka 1Aarhus 1 Montevideo 2 Ohio 1Ealing 1 Ealing 1 Rissen 1Hvittingfoss 1 Infantis 1 Stanleyville 1Kentucky 1 Kedougou 1 Tennessee 1Mbandaka 1 Mbandaka 1 3,19:i:- 1Offa 1 Ohio 1Ruiru 1 Rissen 1Senftenberg 1 Senftenberg 1Wagenia 147:z4,z23:- 1

TOTAL 18 TOTAL 17 TOTAL 10

165

Table 11.4: Serovars of Salmonella isolated from compound pig feed in Great Britain in 2019, compared with the previous two years

Salmonella serovar Isolations Salmonella serovar Isolations Salmonella serovar Isolations2017 2018 2019

Tennessee 2 Rissen 10 Derby 1Rissen 1 Cubana 2 Senftenberg 1

Agona 1 Tennessee 1Livingstone 1 13,23:i:- 1Ohio 1Senftenberg 1Tennessee 13,19:z27:- 113,23:i:- 1

TOTAL 3 TOTAL 19 TOTAL 4

166

Figure 11.6: Isolations of the most common serovars in compound ruminant feed, cattle and sheep in GB 2019

Senftenberg30.0%

Idikan10.0%

Mbandaka10.0%Ohio

10.0%

Rissen10.0%

Stanleyville10.0%

Tennessee10.0%

3,19:-:-10.0%

Compound ruminant feed (n=10)

Dublin55.9%

Mbandaka16.7%

Typhimurium11.6%

Montevideo3.9%

4,12:i:-1.5%

4,5,12:i:-1.5%

New port1.3%

Other serovars7.7%

Cattle (n=467)

enterica diarizonae

61:k,1,5,(7) and variants57.3%

Montevideo15.5%

Dublin5.8%

Agama3.9%

Typhimurium3.9%

Other serovars13.6%

Sheep (n=103)

167

Figure 11.7: Isolations of the most common serovars in compound pig feed and pigs in GB 2019

Derby25.0%

Senftenberg25.0%

Tennessee25.0%

13,23:i:-25.0%

Compound pig feed (n=4)

Typhimurium29.9%

4,12:i:-28.1%

4,5,12:i:-18.0%

Bovis-morbif icans7.2%

Kedougou4.8%

Derby3.6%

New port3.6%

Other serovars4.8%

Pigs (n=167)

168

Table 11.5: Serovars of Salmonella isolated from compound poultry feed in Great Britain in 2019, compared with the previous two years

Salmonella serovar Isolations Salmonella serovar Isolations Salmonella serovar Isolations2017 2018 2019

Ohio 6 13,23:i:- 13 Senftenberg 813,23:i:- 5 Kedougou 7 Ohio 6Senftenberg 3 Senftenberg 5 Kedougou 5Tennessee 3 Infantis 3 Tennessee 5Agama 2 Livingstone 3 Livingstone 3Kedougou 2 Ohio 3 Nottingham 3Agona 1 Kottbus 2 Liverpool 2Anatum 1 Bonn 1 Mbandaka 2Bareilly 1 Corvallis 1 Newport 2Cubana 1 Isangi 1 Agona 1Mbandaka 1 Liverpool 1 Havana 1Montevideo 1 Mbandaka 1 Montevideo 1Muenster 1 Tel-el-Kebir 1 Oslo 13,19:z27:- 1 Tennessee 1 Putten 14,12:-:- 1 4,12:d:- 1 Soerenga 1

6,7:-:- 1 Solt 16,8:e,h:- 1 Typhimurium DT193 1

3,19:-:- 13,19:rough:- 14,12:d:- 113,23:i:- 1

TOTAL 30 TOTAL 46 TOTAL 48

169

Table 11.6: Serovars of Salmonella isolated from compound feed for other species* feed in Great Britain in 2019, compared with the previous two years

Salmonella serovar Isolations Salmonella serovar Isolations Salmonella serovar Isolations2017 2018 2019

Give 7 4,12:e,h:- 4 13,23:i:- 5Anatum 3 Havana 3 61:-:1,5 5Panama 3 Montevideo 3 Mbandaka 213,23:i:- 2 Kedougou 2 Ohio 2Butantan 1 Mbandaka 2 4,12:i:- DT193 2Derby 1 Ohio 2 Agona 1Indiana 1 Anatum 1 Budapest 1Livingstone 1 Bonn 1 Derby 1Mbandaka 1 Indiana 1 Hadar 1Mokola 1 Infantis 1 Infantis 1Montevideo 1 Isangi 1 Kedougou 1Ohio 1 Newport 1 Kottbus 1Orion 1 Soerenga 1 Livingstone 1Schwarzengrund 1 3,10:e,h:- 1 Montevideo 13,10:lv:- 1 61:k:1,5 1 Oslo 14,12:i:- U311 1 Typhimurium NOPT 147:z4,z23:- 1 3,19:-:- 1

61:k:1,5 1

TOTAL 28 TOTAL 25 TOTAL 29

* Other species in 2019 were: Dogs (14 reports), cats (2 reports), fish (2 reports), mixed species (1 report) and unspecified (10 reports)

For details of other species in 2018 and 2017, see the 2018 and 2017 editions, respectively, of Salmonella in Livestock Production in GB

170

Figure 11.8: Isolations of the most common serovars in compound poultry feed, and positive flocks of chickens and turkeys from NCP testing in GB 2019

* Only adult flocks

* 15 flocks positive for 2 serovars (these are counted only once in the total) * Only adult flocks. 1 flock positive for 3 serovars (these are counted only once in the total)

† 3 flocks positive for 2 serovars (these are counted only once in the total)

* Only adult flocks

Senf tenberg16.7%

Ohio12.5%

Kedougou10.4%

Tennessee10.4%

Liv ingstone 6.3%

Nottingham6.3%

Liv erpool4.2%

Mbandaka4.2%

Newport4.2%

Other serov ars

25.0%

Compound poultry feed (n=48)

13,23:i:-53.8%

Ohio15.4%

Kottbus7.7%

Notingham7.7%

6,7:-:enz157.7%

3,19:z27:-7.7%

Breeder chickens (NCP testing only) (n=13*)

13,23:i:-28.1%

Mbandaka22.4%

Kedougou22.2%

Montev ideo9.7%

Ohio4.6%

Senf tenberg2.1%

Derby1.9%

Agona1.9%

Other serov ars

6.9%

Broiler chickens(NCP testing only) (n=1,472*)

Enteritidis29.2%

Kedougou8.3%

Agama6.3%

Newport6.3%Anatum

4.2%

Montev ideo4.2%

Nottingham4.2%

Tennessee4.2%

Other serov ars

33.3%

Layer chickens(NCP testing only) (n=48*)

Derby54.4%

Senf tenberg18.7%

Kedougou14.5%

Agona2.6%

Anatum2.1%

Kottbus2.1%

Other serov ars

5.7%

Breeder and fattening turkeys (combined) (NCP testing only) (n=190†*)

171

Table 11.7: Salmonella serovars reported from animal feedingstuff ingredients and products associated with the ABPR in GB 2017 – 2019

Salmonella serovar Isolations Isolations Isolations2017 2018 2019

Aarhus - 4 -Africana 1 - -Agama 10 3 1Agona 4 2 9Ajiobo - 1 -Amsterdam - - 2Anatum 6 10 3Aqua - - 1

Banana - 3 -Bardo - - 1Berta - - 1Bovismorbificans 9 2 14Brandenburg 1 - 7Bredeney 1 - 14Budapest - 3 4

Cerro 2 3 3Coeln - - 1Corvallis - - 1Cubana 2 - 1

Derby 11 19 16Denver - - 1Dublin 1 7 13Duisberg - 1 -Durban - - 2Durham - - 1

Ealing 2 - 3Eastbourne - - 1Enteritidis 1 4 7

Fresno 2 1 -

Give 2 6 8Goldcoast - - 1

Hadar - - 3Havana 2 - 4

Ibadan - - 1Idikan 2 22 11

172

Table 11.7: Salmonella serovars reported from animal feedingstuff ingredients and products associated with the ABPR in GB 2017 – 2019 (continued)

Salmonella serovar Isolations Isolations Isolations2017 2018 2019

Indiana 37 21 31Infantis 11 13 10Isangi 1 10 -

Jodhpur - 1 1

Kedougou 16 18 33Kentucky 5 2 4Kingston 1 - 1Kottbus 10 12 7

Lagos - - 1Lexington - 3 1Lille 1 - -Litchfield - 1 -Liverpool 6 5 7Livingstone 12 10 15Llandoff 1 - -London 4 2 3

Mbandaka 19 26 33Meleagridis 2 - -Menston - 1 -Minnesota - 2 -Moloka - 1 -Montevideo 21 12 22

Newport 10 11 10Nottingham 9 - 6

Offa 9 - -Ohio 27 30 33Oranienburg 1 - -Orion 6 9 3O rough :d:enz15 - - 1O rough:f,g:- - 1 -O rough:i:1,2 - 1 -O rough:z:1,6 - - 1Oslo - 1 2Ouakam - 1 -

Panama 5 4 3Paratyphi B var. Java - 2 -

173

Table 11.7: Salmonella serovars reported from animal feedingstuff ingredients and products associated with the ABPR in GB 2017 – 2019 (continued)

Salmonella serovar Isolations Isolations Isolations2017 2018 2019

Passing 1 - -Pomona - - 1Poona - - 2Putten - - 1

Ramatgan 1 -Reading 9 6 4Riggil - 1Rissen 3 27 12

Saintpaul 1 3 -Schwarzengrund 1 - 2Senftenberg 19 41 35Soerenga 2 1 1Stanley 1 1 5Stanleyville - 2 -Stockholm 1 - -

Tel-el-Kebir - - 1Tennessee 30 46 53Thompson - 2 1Typhimurium 7 21 33

Uganda - - 2

Virginia - - 1

Wandsworth - 1 -

Yoruba 1 - -

3,10:-:- - 1 -3,10:e,h:- - 1 -3,10:lv:- 2 4 93,10:y:- 1 - -3,15:d:e,nz15 1 - -3,19:d:- - 1 -3,19:z27:- - 5 -3,19:-:- 1 - 13,19:Z45:- 2 1 -3,19:rough:- - - 14,5,12:b:- - - 14,5,12:e,h:- - - 14,5,12:i:- 2 11 11

174

Table 11.7: Salmonella serovars reported from animal feedingstuff ingredients and products associated with the ABPR in GB 2017 – 2019 (continued)

Salmonella serovar Isolations Isolations Isolations2017 2018 2019

4,12:d:- - 1 54,12:i:- 9 9 174,12:z:- 5 3 36,7:e,h:- - - 16,7:enz15 1 8 66,7:-:l,w - - 26,7:r:- - 1 -6,7,z10:- 3 - 56,7:-:- - - 16,8:e,h:- - 3 48,20:z4,z23 1 - -9,12:gt:- - - 113,23:i:- 11 21 2113,23:z:1,5 - - 113,23:-:1,5,7 - - 113,23:-:1,7 - - 130:-:- - - 142:l,v:1,5 - 1 -61:k:1,5 - 1 -61:k:1,5,7 1 - -61:-:1,5 - 2 461:-:1,5,7 1 3 7

TOTAL 391 520 622

For a breakdown of isolations by feedingstuff ingredient and serovar please see Tables 11.8a and 11.8b.

175

Table 11.8a: Serovars of Salmonella in feedingstuff ingredients in GB 2017 - 2019

Feedingstuff Salmonella serovar Isolations Isolations Isolations2017 2018 2019

Apple Agama - 1 -

Beans Senftenberg - 1 -

Barley Offa 6 - -Tennessee - - 16,7:-:l,w - - 1

Biscuit Infantis - 1 -

Brewers' yeast Anatum - 4 -Isangi - 7 -Senftenberg - 1 -13,23:i:- - 1 -

Cooked pulses Anatum 1 - -Orion - - 1

Egg pellets Ohio 1 - -

Feather meal Infantis 1 - -Montevideo 1 - -Tennessee 1 - -

Fishmeal Cerro 1 - -Liverpool - - 1Montevideo 1 - 3Nottingham 1 - -Senftenberg 1 - -Soerenga - 1 -

Guar protein Jodhpur - - 1Kentucky - - 1

Haylage Thompson - 1 -

Herbs Thompson - - 14,12:i:- NOPT - - 1

Maize Banana - 1 -Livingstone - - 4Newport - - 1Ramatgan 1 - -6,7:z10:- 1 - -

176

Table 11.8a: Serovars of Salmonella in feedingstuff ingredients in GB 2017 – 2019 (continued)

Feedingstuff Salmonella serovar Isolations Isolations Isolations2017 2018 2019

Malt Anatum 2 - -Bovismorbificans - 1 -Enteritidis NOPT - - 1Enteritidis UNTY 1 - -Indiana - 1 -Livingstone - - 1Mokola - 1 -Newport 1 - -Orion - 1 2Wandsworth - 1 -

Minerals Infantis - 1 -Isangi - 2 -

Mixed cereals Africana 1 - -Livingstone - 1 -Senftenberg 1 - -

Mixed ingredients Kedougou - - 1Mbandaka - - 1Tennessee - 1 -

Mixed oil seeds Ealing - - 1Minnesota - 1 -Rissen - 11 2Senftenberg 2 9 1Tennessee - 5 -13,23:i:- 1 - -

Mixed vegetable protein Mbandaka 1 - -3,19:d:- - 1 -

Palm kernel Fresno - 1 -Typhimuirum DT193 - 1 -

Rapeseed Bredeney - - 11Cubana 2 - 1Derby - - 1Ealing 1 - 2Enteritidis PT1 - - 1Idikan 1 16 8Kedougou - 1 -Kentucky - - 1

177

Table 11.8a: Serovars of Salmonella in feedingstuff ingredients in GB 2017 – 2019 (continued)

Feedingstuff Salmonella serovar Isolations Isolations Isolations2017 2018 2019

Rapeseed - continued Montevideo - - 3Ohio - 1 -Oranienburg 1 - -Rissen 2 15 6Senftenberg 2 10 4Tennessee 18 32 463,19:rough:- - - 14,12:d:- - - 113,23:i:- - 1 1

Soya Aarhus - 1 -Agona 2 - -Banana - 2 -Budapest - 3 4Denver - - 1Havana - - 1Idikan 1 1 -Infantis - 3 -Kentucky 1 - 1Liverpool 3 1 3Lexington - 1 -Livingstone 2 - 1Mbandaka 6 1 6Meleagridis 2 - -Montevideo - 1 2Ohio - 1 -Ouakam - 1 -Rissen 1 - -Senftenberg 3 6 6Soerenga 2 - -Tennessee 1 2 -Typhimurium DT99 - 1 -Typhimurium DT193 - - 2Typhimurium U302 - 2 -Yoruba 1 - -3,19:rough:- - - 13,19:z27:- - 3 -4,5,12:i:- DT40 1 - -4,12:d:- - - 16,7:r:- - 1 -6,7,z10:- 1 - -13,23:i:- - - 1

178

Table 11.8a: Serovars of Salmonella in feedingstuff ingredients in GB 2017 – 2019 (continued)

Feedingstuff Salmonella serovar Isolations Isolations Isolations2017 2018 2019

Sunflower seed Bredeney - - 1Enteritidis PT3b - 1 -Havana - - 1Lexington - 1 -Liverpool - 1 1Mbandaka - 1 1Montevideo - - 2Nottingham - - 1Senftenberg - - 1Typhimurium DT99 1 - -

Wheat Agama 1 - -Agona - - 3Enteritidis PT2 - - 1Havana - - 1Infantis 1 - -Kingston - - 1Offa 1 - -Ohio - - 13,10:lv:- 1 - -

86 169 158TOTAL

179

Table 11.8b: Serovars of Salmonella in other products associated with the ABPR in GB 2017 - 2019

Feedingstuff Salmonella serovar Isolations Isolations Isolations2017 2018 2019

Blood products Agama 1 - -Agona 1 - -Bovismorbificans - - 1Derby - - 1Kedougou - 1 -Mbandaka - 1 -Senftenberg 2 - 2Tennessee 4 4 -Typhimurium DT193 1 - -

Bone meal Isangi 1 - -Kedougou - - 1Livingstone - - 1Montevideo 1 - 113,23:i:- - - 1

Compost Agona - 1 -Amsterdam - - 1Aqua - - 1Cerro - 1 -Derby - 1 -Durban - - 2Kedougou - 1 1Kentucky - 1 -Kottbus - - 1Lille 1 - -Mbandaka - - 1Montevideo 2 1 1Nottingham 2 - 1Offa 1 - -Ohio - - 1Pomona - - 1Senftenberg - - 13,19:z27:- - 1 -4,5,12:i:- DT193 1 - -

Digestate Amsterdam - - 1Brandenburg - - 2Fresno 1 - -Give - - 1Indiana 1 - -Kentucky - - 1Mbandaka - 2 2

180

Table 11.8b: Serovars of Salmonella in other products associated with the ABPR in GB 2016 – 2018 (continued)

Feedingstuff Salmonella serovar Isolations Isolations Isolations2017 2018 2019

Digestate - continued Nottingham 2 - -13,23:i:- - - 1

Feedmill environment Agama 3 2 1Agona - - 1Ajiobo - 1 -Anatum - 1 2Derby - 1 -Enteritidis PT8 - 1 1Enteritidis NOPT - 2 -Ibadan - - 1Idikan - - 1Indiana 1 - -Infantis - 5 8Jodpuhr - 1 -Kedougou 11 11 21Kentucky - 1 -Litchfield - 1 -Liverpool - - 1Mbandaka 5 7 5Minnesota - 1 -Montevideo 1 1 -Newport 1 1 2Nottingham - - 2Ohio 19 23 25Orion - 1 -O rough:f,g:- - 1 -O rough:i:1,2 - 1 -Oslo - - 1Panama 1 1 -Passing 1 - -Rissen - 1 -Senftenberg 5 11 16Sorenga - - 1Stanley 1 - -Tel-el-Kebir - - 1Tennessee 2 1 3Thompson - 1 -Typhimurium DT35 - 2 -Typhimurium DT73 - - 1Typhimurium DT104 - - 1Typhimurium DT193 - - 1

181

Table 11.8b: Serovars of Salmonella in other products associated with the ABPR in GB 2016 – 2018 (continued)

Feedingstuff Salmonella serovar Isolations Isolations Isolations2017 2018 2019

Feedmill environment - Typhimurium U302 - 1 -continued Typhimurium UNTY - - 4

3,10:-:- - 1 -4,5,12:b:- - - 14,5,12:d:- - - 14,12:i:- DT193 1 - 14,12:i:- DT208 1 - -4,12:i:- NOPT - - 14,12:i:- UNTY - - 16,7:enz15 1 4 36,7:-:l,w - - 16,7:z10:- - - 113,23:i:- 4 17 1242:l,v:1,5 - 1 -61:-:1,5,7 - - 1

Filled dog bones Putten - - 1

Landfill Fresno 1 - -Indiana 2 - -Infantis 1 - -Kedougou 1 - -Llandoff 1 - -London - 1 -Nottingham 1 - -Orion - 1 -Stanley - 1 -Tennessee 1 - -

Meat meal Aarhus - 3 -Agona - 1 -Anatum 4 1 -Bovismorbificans - 1 -Cerro 1 1 -Duisberg - 1 -Havana 2 - -Idikan - 5 -Liverpool 2 1 -Livingstone 7 2 1Mbandaka 1 - -Menston - 1 -Montevideo 2 3 -

182

Table 11.8b: Serovars of Salmonella in other products associated with the ABPR in GB 2016 – 2018 (continued)

Feedingstuff Salmonella serovar Isolations Isolations Isolations2017 2018 2019

Meat meal - cotinued Ohio 4 2 1Senftenberg 1 - -Stanleyville - 1 -Tennessee 2 - -3,15:d:e,nz15 1 - -3,19:z27:- - 1 -3,19:z45:- 1 - -4,12:d:- - 1 -4,12:z:- - 1 -4,5,12:i:- DT193 - 1 -8,20:z4,z23:- 1 - -13,23:i:- - 1 -

Meat & bone meal Ealing 1 - -Kentucky 1 - -Livingstone - 1 -London 2 - -Montevideo 4 - -Newport 1 - -Offa 1 - -Orion 1 - -Schwarzengrund 1 - -Typhimurium DT73 - - 14,12:i:- DT193 - 1 -

Pet food (raw) Agama 2 - -Agona - - 5Anatum - 4 1Bardo - - 1Berta - - 1Bovismorbificans 9 - 12Brandenburg 1 - 5Bredeney 1 - 2Cerro - 1 3Coeln - - 1Derby 11 17 14Dublin 1 7 6Eastbourne - - 1Enteritidis PT1 - - 1Enteritidis PT4 - - 1Enteritidis RDNC - - 1Give 2 6 7Goldcoast - - 1Hadar - - 3Idikan - - 2

183

Table 11.8b: Serovars of Salmonella in other products associated with the ABPR in GB 2016 – 2018 (continued)

Feedingstuff Salmonella serovar Isolations Isolations Isolations2017 2018 2019

Pet food (raw) - continued Indiana 33 20 31Infantis 8 3 1Isangi - 1 -Kedougou 1 3 4Kentucky 3 - -Kingston 1 - -Kottbus 10 12 6Lagos - - 1Lexington - 1 1Liverpool 1 2 -Livingstone 1 2 4London 2 1 3Mbandaka 6 12 14Montevideo 7 6 9Newport 7 10 6Nottingham 3 - -Ohio 2 3 1Orion 5 5 -O rough:d:enz15 - - 1Oslo - - 1Panama 4 3 3Paratyphi var. Java - 2 -Reading 9 6 4Riggil - 1 -Rissen - - 4Saintpaul 1 3 -Schwarzengrund - - 2Senftenberg 2 3 1Stanley - - 5Stanleyville - 1 -Stockholm 1 - -Tennessee - - 1Typhimurium DT1 1 - -Typhimurium DT2 - - 1Typhimurium DT12 - 2 -Typhimurium DT104 2 1 5Typhimurium DT193 1 - -Typhimurium DT204e - 1 -Typhimurium U288 - 2 -Typhimurium U302 - 1 -Typhimurium NOPT - 5 3Typhimurium RDNC - 2 -Typhimurium UNTY - - 2

184

Table 11.8b: Serovars of Salmonella in other products associated with the ABPR in GB 2016 – 2018 (continued)

Feedingstuff Salmonella serovar Isolations Isolations Isolations2017 2018 2019

Pet food (raw) - continued Uganda - - 1Virginia - - 13,10:e,h:- - 1 -3,10:lv:- 1 4 93,10:y:- 1 - -3,19:-:- 1 - -3,19:z45:- 1 1 -4,5,12:e,h:- - - 14,5,12:i:- DT12 - 1 -4,5,12:i:- DT193 - 9 74,5,12:i:- NOPT - - 14,5,12:i:- UNTY - - 14,12:i:- DT193 4 3 84,12:i:- U311 1 1 -4,12:i:- NOPT - 4 14,12:i:- UNTY 2 - 24,12:z:- 5 2 36,7:e,h:- - - 16,7:-:- - - 16,7:-:enz15 - 4 36,7:z10:- 1 - 16,8:e,h:- - 3 49,12:gt:- - - 113,23:z:1.5 - - 113,23:-:1,5,7 - - 113,23:-:1,7 - - 113,23:i:- 3 - 430:-:- - - 161:k:1,5 - 1 -61:-:1,5 - 2 461:k:1,5,7 1 - -61:-:1,5,7 1 3 5

Poultry offal meal Agona 1 - -Havana - - 1Kedougou - 1 -Livingstone - - 3Mbandaka - 1 2Montevideo 1 - -Ohio 1 - -Orion - 1 -Senftenberg - - 1Tennessee 1 - 2

185

Table 11.8b: Serovars of Salmonella in other products associated with the ABPR in GB 2016 – 2018 (continued)

Feedingstuff Salmonella serovar Isolations Isolations Isolations2017 2018 2019

Poultry offal meal - Typhimurium DT2 1 - -continued Uganda - - 1

13,23:i:- - 1 -

Rendering plant material Dublin - - 7Infantis - - 1Mbandaka - - 1Montevideo - - 1Newport - - 1Nottingham - - 2O rough:z:1,6 - - 1Poona - - 2Typhimurium DT104 - - 10Typhimurium NOPT - - 1Typhimurium UNTY - - 14,5,12:i:- DT193 - - 24,12:i:- DT193 - - 16,7:z10:- - - 361:-:1,5,7 - - 1

Tallow Livingstone 1 - -Tennessee - 1 -

Unspecified Agama 2 - -Bovismorbificans - - 1Corvallis - - 1Durham - - 1Kedougu 3 - 5Liverpool - - 1Livingstone 1 4 -Mbandaka - 1 -Montevideo 1 - -Ohio - - 4Oslo - 1 -Senftenberg - - 24,12:d:- - - 313,23:i:- 2 - 1

304 351 464TOTAL

186

Table 11.9: Animal By-Products (Enforcement) Regulations, 2013 - domestic protein official testing – contamination rates in GB 2017 – 2019

Table 11.10: Animal By-Products (Enforcement) Regulations, 2013 - serovars isolated during 2017 – 2019 from official and private testing of domestic protein and other products associated with the regulations in GB

Sample TypeN +ve % +ve N +ve % +ve N +ve % +ve

Blood meal 5 - - 3 - - 5 1 20.0Bone meal - - - - - - - - -Feather meal 13 - - 6 - - 9 - -Greaves 5 - - 2 - - 5 - -Hoof meal - - - - - - - - -Meat & bone meal 9 - - 3 - - 5 - -Meat meal 1 - - - - - - - -Poultry offal meal 26 - - 4 - - 12 2 16.7

Herring meal - - - - - -White fish meal 13 - - 11 - - 9 - -Other fish meal 4 - - 1 - - 2 - -

Others 710 10 1.4 633 3 0.5 601 8 1.3

TOTAL 786 10 1.3 663 3 0.5 648 11 1.7

NB: This table excludes the results of private testing

Batches Tested in 2018 Batches Tested in 2019Batches Tested in 2017

Salmonella serovar Isolations Salmonella serovar Isolations Salmonella serovar Isolations2017 2018 2019

Montevideo 4 Montevideo 2 Montevideo 3Livingstone 2 Oslo 1 Livingstone 3Agona 1 Amsterdam 1Kentucky 1 Bovismorbificans 1Kottbus 1 Derby 16,8:-:e,n,z15 1 Newport 1

Senftenberg 1

TOTAL ISOLATIONS 10 TOTAL ISOLATIONS 3 TOTAL ISOLATIONS 11POSITIVE BATCHES 10 POSITIVE BATCHES 3 POSITIVE BATCHES 11

187

Table 11.11: The Importation of Processed Animal Protein Order, 1981 - imported animal protein contamination rates in Great Britain in 2019, compared with previous years

N +ve % +ve N +ve % +ve N +ve % +veBlood meal - - - - - - - - -Bone meal - - - - - - - - -Feather meal - - - - - - - - -Meat & bone meal - - - - - - - - -Meat meal - - - - - - - - -Poultry offal meal - - - - - - - - -Greaves - - - - - - - - -

Herring meal - - - - - - - - -White fish meal - - - - - - - - -Other fish meal - - - - - - - - -

Others - - - - - - - - -

TOTAL 0 0 0 0 0 0 0 0 0

Batches Tested in 2018 Batches Tested in 2019Sample Type Batches Tested in 2017

188

Figure 11.9: Contamination rate for domestic and imported processed animal protein (batches tested) in GB 2010 - 2019

* Imported - no batches tested in 2011, 2014, 2015, 2017, 2018 and 2019

For data data prior to 2010, see Salmonella in Livestock Production in GB 2013

0

0.5

1

1.5

2

2.5

3

3.5

2010 2011 2012 2013 2014 2015 2016 2017 2018 2019

% b

atch

es te

sted

pos

itive

Year

Domestic

Imported*

189

Chapter 12: Antimicrobial susceptibility in Salmonella Salmonella isolates received for serological identification at APHA Weybridge and Lasswade are tested for their in vitro sensitivity to 16 antimicrobials. The majority of these isolates originate from animals and their environment in England and Wales; some isolates (mainly from poultry) also originate from Scotland. Isolates are included which have been recovered under the Salmonella National Control Programmes (apply to chickens and turkeys) and these isolates are derived from premises located throughout GB.

The choice of antimicrobials, which is reviewed periodically, is designed to comprise a core set which has been used in veterinary practice for many years. It also includes some of the more recently licensed antimicrobials and some which are not authorised for use in animals in the UK, but which are used in human medicine. The antimicrobials selected provide useful information on resistance mechanisms and are also useful for epidemiological purposes. All tests are performed using the British Society for Antimicrobial Chemotherapy (BSAC) disc diffusion technique (www.bsac.org.uk) on Oxoid “Isosensitest” agar and antimicrobial discs as listed in the table. BSAC recommendations and clinical breakpoints have been adopted for antimicrobials, where BSAC breakpoints are available.

Revisions to the methodology have been catalogued in previous reports and include changes made to enhance the detection of resistance to third generation cephalosporins and fluoroquinolones. In 2007, the interpretative criterion was changed for ciprofloxacin from the historical APHA veterinary breakpoint of resistant < 13mm used in previous years, to the BSAC breakpoint of resistant or intermediate < 19mm (this breakpoint was that recommended by BSAC on 1/1/2007); trends in ciprofloxacin resistance should therefore be interpreted taking into account this change to the breakpoint. Where no BSAC breakpoints are available, then the historical APHA veterinary breakpoint has been used or a breakpoint has been derived (APHA data on file; UK-VARSS Report 2018 provides further details in an annex and is available at https://assets.publishing.service.gov.uk/government/uploads/system/uploads/attachment_data/file/842680/PCDOCS-_1705030-v1-UK-VARSS_Supplementary_Material_2018__2019__FINAL.pdf).

The sole change made to the zone size breakpoints and disc concentrations used over the period 2008 - 2019 related to the ceftazidime disc where the zone size was reduced from 29mm to 26mm in 2012, in line with BSAC recommendations. The BSAC disc diffusion method is no longer being developed, but the BSAC clinical breakpoints were fully harmonised with those of the European Committee on Antimicrobial Susceptibility Testing (EUCAST) and will remain valid, unless EUCAST clinical breakpoints for the antimicrobials included in this report are revised.

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Antimicrobial Concentration (µg per ml) Code Zone Size

(R<x mm)

1 Nalidixic acid 30 NA 13

2 Tetracycline 10 T 13

3 Neomycin 10 N 13

4 Ampicillin 10 AM 13

5 Furazolidone 15 FR 13

6 Ceftazidime 30 CAZ 26

7 Sulphamethoxazole/ trimethoprim

25 TM 15

8 Chloramphenicol 30 C 20

9 Amikacin 30 AK 18

10 Amoxicillin/clavulanic acid 30 AMC 14

11 Gentamicin 10 CN 19

12 Streptomycin 10 S 13

13 Sulphonamide compounds 300 SU 13

14 Cefotaxime 30 CTX 29

15 Apramycin 15 APR 13

16 Ciprofloxacin 1 CIP 19

Prior to 1996, all Salmonella isolates received were tested for antimicrobial susceptibility, but since then only the first isolate of a given serotype or phage type from each incident has usually been tested. The number of isolates received from a farm varies enormously, especially in the case of those received from poultry premises. Some poultry companies have a continuous monitoring programme and large numbers of Salmonella isolates may

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be received from a particular company relating to one premises. Thus, in that situation, the numbers of isolates of a particular serotype and their antimicrobial susceptibility may not reflect the prevalence in the animal population as a whole but rather the intensity of the monitoring programme on a farm or group of farms. Therefore, to better indicate the prevalence of resistance, only the first isolate from each incident has usually been tested since the start of 1996.

Salmonella Dublin Of the 269 Salmonella Dublin isolates tested during 2019, 99.6% were susceptible to all 16 antimicrobials (Table 12.1). The percentage of S. Dublin isolates sensitive to all 16 antimicrobials has shown only slight fluctuations over the period 2006 - 2019 and the majority of isolates remain susceptible; this has been the situation since surveillance began in 1971. Most S. Dublin isolates (87.7%) originated from cattle in 2019 and this was similar to the situation recorded in previous years. S. Dublin isolates from species other than cattle in 2019 comprised five isolates from sheep, nine from dogs, one from chickens, one from a cat, one from a horse, one from an unspecified mammal, one from an environmental sample and 14 from animal feed.

Salmonella Typhimurium The number of isolates of Salmonella Typhimurium tested in 2019 was 254 (Table 12.2). The eight most frequent definitive or undefined phage types subjected to susceptibility testing at APHA are shown in Figure 12.1. 26.4% of S. Typhimurium isolates were phage types DT104 (n=45), DT104b (n=4) or U302 (n=18) i.e. within the ‘DT104 complex’ (Table 12.2). The percentage of the eight most common definitive and undefined phage types of S. Typhimurium sensitive to all 16 antimicrobial agents in 2019 is shown in Figure 12.2. The overall percentage of S. Typhimurium isolates that were sensitive to all of the antimicrobials tested was 49.2% (Table 12.2), which is a slight decrease compared to the 2018 figure (54.4%), but higher than reported in 2017 (34.2%) and 2016 (30.1%).

The generally high level of resistance of S. Typhimurium isolates observed in recent years has partly been a reflection of the contribution of DT104 and its variants DT104b and U302. The occurrence of S. Typhimurium DT104 and its variants, which had shown a general decline in 2007-2014, showed a resurgence in 2017/18, but has now returned to baseline levels. These phage types which are preferentially selected for susceptibility tests because of the importance of the pentavalent resistance pattern, have made up more than a quarter of isolates tested in some years of the last decade (Table 12.2). In 2019, only two of the 45 DT104 isolates tested were sensitive to all antimicrobials tested. The remaining DT104 isolates, plus all four DT104b isolates and 11/18 U302 isolates, were resistant to at least one of the 16 antimicrobials tested.

The typical pentavalent resistance pattern AmCSSuT was the most common resistance pattern seen in S. Typhimurium DT104 and DT104b isolates, representing 91.8% (45/49)

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of isolates. None of the 49 DT104 and DT104b isolates were resistant to nalidixic acid or sulphamethoxazole/ trimethoprim. No isolates of DT104 which was previously fairly commonly reported, have been recovered from turkeys since 2011. DT104 isolates from turkeys had commonly shown nalidixic acid resistance in previous years. Nalidixic acid resistance in S. Typhimurium DT104 by species of origin is listed in Table 12.3 for the main food-producing species over the last eleven years.

Salmonella Typhimurium U288 and DT193 from pigs accounted for 10.6% (27) and 6.7% (17) of the total numbers of S. Typhimurium isolates tested, respectively; none of the U288 and DT193 isolates from pigs were fully susceptible in 2019.

Considering all definitive types of S. Typhimurium, resistance to sulphamethoxazole/ trimethoprim has fluctuated markedly in recent years, with prevalence ranging between 15.7% and 44.8% (Table 12.2). The prevalence of resistance to sulphamethoxazole/ trimethoprim was 24.0% in 2019. Isolates from pigs have been predominantly responsible for these fluctuations in resistance (Table 12.4); a high proportion of many definitive types of S. Typhimurium isolated from pigs are resistant to sulphamethoxazole/ trimethoprim. Most isolations of S. Typhimurium from pigs that were resistant to sulphamethoxazole/ trimethoprim in 2019 involved two phage types: DT193 (17 isolates; all resistant to sulphamethoxazole/ trimethoprim) and U288 (27 isolates, all resistant to sulphamethoxazole/ trimethoprim (Table 12.5). The resistance pattern AmCSSuTTm was the most common phenotype observed amongst isolates of DT193 (9/17 isolates) and U288 (21/27 isolates) from pigs.

Apramycin resistance in S. Typhimurium increased in 2011 and 2012 to 20.4% of isolates. This was a notable change compared with preceding years when apramycin resistance had been consistently less than 5%. In 2013, apramycin resistance in S. Typhimurium decreased to 1.8%, and has remained low ever since (0.9% in 2014, 0% in 2015, 2.4% in 2016, 0% in 2017,1.8% in 2018, and 0.8% in 2019).

No S. Typhimurium isolates tested in 2019 were resistant to ciprofloxacin, amikacin, ceftazidime, cefotaxime or nalidixic acid.

Multiple antibiotic resistance (i.e. resistance to four or more antimicrobial agents in the panel of 16) was detected in isolates from the following definitive and undefined phage types of S. Typhimurium: DT104 (from cat, cattle, dog, environment, horse, feed and pig), DT104b (cattle), DT12 (feed), DT193 (pig, dog, cattle), DT2 (pheasant), DT32 (pig), U288 (pig), U302 (cat, cattle, horse, pig). Multiple antibiotic resistance was also detected in isolates which did not react to phages in the current typing scheme or did not conform to a definitive or undefined phage type (dog, pig, finch, feed, cattle). Of the 28 different definitive and undefined phage types detected, 15 (namely DT13, DT135, DT168, DT189, DT204b, DT35, DT36, DT40, DT41, DT73, DT8, DT99, U188, U320, U323), several of which are mainly associated with wildlife, were fully susceptible to all of the antimicrobials in the test panel.

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Monophasic Salmonella Typhimurium Serovars One-hundred and twenty-four isolates of Salmonella 4,12:i:- were tested, belonging to definitive phage types DT193 (n=102), DT120 (n=3) and DT2 (n=2), and undefined phage types U302 (n=1) and U323 (n=1); eleven isolates were not typable (UNTY) and for four isolates a phage type could not be determined based on the current typing scheme (RDNC). Most isolates were from pigs (47.5%), with feed and related samples being the next most common origin (22.1%). The most common pattern of resistance observed was AmSSuT, which occurred in 37/102 of DT193 isolates, in 1/3 DT120 isolates, in 1/1 U302 isolates, in 2/11 of the UNTY isolates and 2/4 of the RDNC. Considering the DT193 isolates, 69/102 (67.6%) had the AmSSuT resistance pattern alone or with one or more additional resistances. Most isolates from sources other than chickens and turkeys were not tested by PCR to confirm their status as variants of S. Typhimurium.

A total of 86 isolates of Salmonella 4,5,12:i:- were tested, including phage types DT193 (n=81), UNTY (n=4) and RDNC (n=1). The most common resistance pattern in DT193 isolates was AmSSuT, occurring in 33.3% of isolates (27/81). A high proportion of DT193 isolates were from pigs (44.2%).

Considering the aminoglycosides other than streptomycin, apramycin resistance was detected in 39.7% and neomycin resistance in 27.6% of Salmonella 4,12:i:- isolates from pigs (n=58). Resistance to neomycin and apramycin was observed in 3.7% of Salmonella 4,12:i:- isolates from feed or feed constituents (n=27). Apramycin resistance was detected in 37.5% and neomycin resistance in 52.5% of Salmonella 4,5,12:i:- from pigs (n=40). Resistance to apramycin was also observed in 5.3% of Salmonella 4,5,12:i:- isolates from feed or feed constituents (n=19). Resistance to the aminoglycosides apramycin and neomycin was therefore detected in monophasic S. Typhimurium isolates from both pigs and feed in 2019. In recent years there has been a rise in monophasic Typhimurium infections in pigs involving isolates that are resistant to nine antimicrobials; amoxicillin, streptomycin, sulphonamides, tetracycline, chloramphenicol, neomycin, apramycin, gentamicin and trimethoprim/sulphonamide.

Serotypes Other Than Salmonella Dublin and Salmonella Typhimurium Of the 4,010 isolates of serotypes other than S. Dublin and S. Typhimurium tested, 71.9% were sensitive to all the antimicrobials in the panel (Table 12.6). This is a slight decrease on the figure recorded in 2018, when 77.7% were fully sensitive. One-hundred and thirty-two isolates of S. Enteritidis were tested (3.9% of the total) and 118/132 (89.4%) were fully susceptible. Ten isolates of S. Enteritidis were resistant to nalidixic acid, including four isolates of phage type PT13a (1x chicken layer and 3x horse), three isolates of PT3a (feed), one isolate of PT1 (feed), one isolate of PT12 (quail), and one isolate of PT21 (horse).

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Neomycin resistant Salmonella isolates other than S. Dublin and S. Typhimurium originated mainly from pigs (148 isolates; 25.7% resistant), ducks (297 isolates; 6.4% resistant), feed or feed constituents (971 isolates; 1.3% resistant) and chicken (1,695 isolates, 0.2% resistant. In ducks, S. Indiana was the main serotype showing resistance to neomycin (17/96 isolates; 17.7% resistant); the S. Indiana isolates from ducks were also frequently resistant to furazolidone (36/96 isolates; 37.5% resistant) and this was similar to the situation observed in 2018.

Considering Salmonella isolates other than S. Dublin and S. Typhimurium from turkeys that were tested in 2019 (n=270), 47.4% were resistant to streptomycin, 57.0% to sulphonamides and 54.4% to tetracyclines; similar to the equivalent figures for pigs in 2019 (62.8%, 66.9% and 66.2%, respectively), but higher than those for chickens (8.6%, 18.2% and 15.6%, respectively) or cattle (5.6%, 4.5% and 9.0%, respectively). In 2019, the proportion of Salmonella isolates tested that originated from feed (24.2%) was similar to 2018 (23.0%); however, the proportion of fully susceptible isolates from feed decreased slightly from 78.2% to 74.7%.

Individual Antimicrobials Of the 4,533 Salmonella isolates tested in 2019, 3,273 (72.2%) were sensitive to all of the antimicrobials tested (Table 12.7). This is similar to the situation in 2018, when 4,413 isolates were tested and 3,376 (76.5%) were sensitive to all of the antimicrobials tested. Considering all Salmonella isolates from pigs, the percentage of fully susceptible isolates was 21.4% (44/206) in 2019, which is an increase compared to recent years (12.5% in 2012, 12.9% in 2013, 18.6% in 2014, 3.5 % in 2015, 9.4% in 2016, 10.1% in 2017, and 14.4% in 2018).

Tetracycline resistance was most commonly found in Salmonella isolates originating from pigs and turkeys in 2019. This was also the situation for resistance to sulphonamides and streptomycin. Findings were similar in 2018.

Resistance to apramycin in all Salmonella serovars was 1.2% in 2019, similar to the level observed in 2018 of 0.9%. Salmonella isolates from pigs, where resistance was 19.9% in 2019, contributed most to the overall apramycin resistance figure; in pigs, apramycin resistance was observed in both monophasic S. Typhimurium variants 4,12:i:- and 4,5,12:i:-. In 2019, 39.7% of Salmonella 4,12:i:- isolates from pigs (n=58) and 37.5% of Salmonella 4,5,12:i:- isolates from pigs (n=40) were resistant to apramycin. Resistance to gentamicin in all Salmonella serovars was 1.2%, mostly in isolates from pigs. No resistance was detected to the aminoglycoside amikacin.

The highest prevalence of resistance to nalidixic acid in 2019 was observed in Salmonella isolates from turkeys, the environment, dogs and feed (Table 12.7). The high proportion of nalidixic acid resistant isolates in the environment and feed categories represents a difference from 2013-2016 when resistance to nalidixic acid was mostly observed in Salmonella from turkeys and “other avian species”. In turkeys, 52/53 S. Senftenberg

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isolates and 1/1 Salmonella 3,19:-:- isolates were resistant to nalidixic acid in 2019. The situation in turkeys was similar in 2013 - 2018, with nalidixic acid resistance frequently detected in this serotype. In broilers, resistance to nalidixic acid was found in Salmonella 13,23:i:-, S. Indiana, S. Senftenberg and S. Montevideo. Ciprofloxacin resistance occurred in 17.0% of S. Senftenberg isolates from turkeys and the ciprofloxacin-resistant isolates were also resistant to nalidixic acid. The other ciprofloxacin-resistant isolates detected in 2019 originated from a dog (S. O Rough:r:1,5 (1/1 resistant)), feed and related samples (S. Orion (4/5 resistant), quail (1/1 resistant)) and the environment (S. Newport (1/2 resistant).

Resistance to cefotaxime was detected in 2019 in two S. Infantis isolates from environmental samples relating to animal by-products.

Public Health Considerations Antimicrobial susceptibility patterns have historically been useful in conjunction with Salmonella serotype and (where appropriate) phage type data to investigate the epidemiology of Salmonella infections in humans and animals. When new serotypes or phage types or patterns of resistance emerge in humans, comparative analysis can be done to provide an indication of the possible role or involvement of UK livestock. Genome sequencing has replaced older methods of Salmonella typing to characterise and compare human-derived isolates. Ongoing liaison takes place between the Agencies concerned in relation to the strains detected and their resistance.

Regarding the antimicrobials referred to in this report, resistance to third generation cephalosporins and fluoroquinolones is considered of greatest importance, since these antimicrobials are particularly relevant for the treatment of human salmonellosis, where this is required. [Most cases of non-typhoidal Salmonella infection in humans are non-invasive, limited to the gastro-intestinal tract and do not require treatment with antimicrobials]. The percentage of Salmonella isolates that were resistant to ciprofloxacin in 2019 was 0.4%. Cefotaxime or ceftazidime resistance was not detected in S. Enteritidis from animals in 2019. One single S. Enteritidis isolate (a PT12 from quail) was resistant to ciprofloxacin in 2019. No cefotaxime or ceftazidime resistance was detected in S. Typhimurium from animals in 2019. These findings are important since these serovars are of particular public health importance.

Two S. Infantis isolates, obtained from environmental samples related to animal by-products, were resistant to cefotaxime. These isolates were also resistant to another 9 and 10 (respectively) antimicrobials included in the panel. Multidrug resistant clones of S. Infantis have been reported in central Europe since 2012. These clones have subsequently acquired further antimicrobial resistance to third generation cephalosporins and isolates with cephalosporin resistance have been reported from other countries, in particular from Italy and the USA. Cephalosporin resistance in S. Infantis isolates from livestock has not previously been reported in UK, and it is suspected that the positive samples related to contamination originally from imported chicken.

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The resurgence of pentavalent (AmCSSuT) S. Typhimurium DT104 began in 2017. This was mainly due to a localised increase in number of incidents of this Salmonella in sheep and cattle in 2016/17. In 2019, incidents of this phenotype were still identified, but at lower levels than in 2017.

The number of S. Enteritidis isolations was higher in 2019 (n=132) when compared to 2018 (n=48). In 2019, the increase was mainly due to the identification of S. Enteritidis PT8 in laying hens on five separate holdings which were potentially linked by the use of common packing centres. This strain was sensitive to all 16 antimicrobials tested.

APHA offers an advisory visit when cases of Salmonella infection in food-producing animals with resistance to third generation cephalosporins or ciprofloxacin are detected, both to explain the significance of the findings and to provide appropriate advice on control.

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Table 12.1: Salmonella Dublin: antimicrobial susceptibility monitoring 2009 – 2019

Year No of isolates

Percentage susceptible to all 16

antimicrobials*AM C NA S APR CN N FR SU TM T

2009 560 92.3 0.5 0.4 0.4 7.0 - - - 0.2 0.5 - 0.9

2010 630 95.7 0.2 0.2 1.3 2.7 - 0.2 - - 0.5 - -

2011 453 96.0 0.2 0.4 0.4 3.3 0.2 - - - 0.4 - 0.4

2012 327 97.2 0.6 0.3 0.6 1.8 - - - - - - 0.3

2013 393 96.9 0.3 - 1.0 1.3 - 0.3 0.3 - - - -

2014 286 96.5 0.7 - - 2.4 - - 0.3 0.3 0.7 0.7 1.1

2015 226 94.2 1.7 0.4 2.2 0.4 - - 2.2 - - - 0.4

2016 245 96.3 0.4 0.4 1.2 1.6 - - - - - - 0.4

2017 272 100.0 - - - - - - - - - - -

2018 320 96.2 - 0.3 2.2 0.3 - - 0.3 - 0.3 - 0.3

2019 269 99.6 - 0.4 - 0.4 - - - - 0.4 0.7 0.4

* For a key to the antimicrobials used please see the table towards the beginning of this chapter

Percentage of isolates resistant to:

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Table 12.2: Salmonella Typhimurium: antimicrobial susceptibility monitoring 2009 – 2019

Year No of isolates

Percentage susceptible to all 16

antimicrobials*AM C NA S APR N FR SU TM T

2009 440 a 25.7 61.1 46.1 4.1 60.7 1.1 3.0 0.2 67.5 40.7 65.72010 328 b 33.5 51.2 36.3 5.2 54.6 4.0 3.0 0.3 56.7 27.1 58.22011 427 c 34.4 49.2 24.6 4.9 51.3 20.4 3.5 - 56.2 37.5 57.42012 191 d 27.2 56.5 30.4 2.6 59.1 20.4 2.1 0.5 63.9 41.9 64.92013 165 e 30.3 57.6 35.2 4.8 54.5 1.8 0.6 - 60.6 44.8 61.22014 224 f 44.2 43.3 36.6 0.9 39.7 0.9 - - 43.8 35.7 49.12015 165 g 41.8 46.7 46.0 1.2 51.5 - 2.4 - 48.5 32.1 46.72016 166 h 30.1 60.2 57.8 - 63.9 2.4 0.6 0.6 66.3 28.9 61.42017 187 i 34.2 58.3 53.5 1.6 57.1 - - - 62.6 19.8 54.52018 504 j 54.4 30.1 29.9 0.4 40.7 1.8 1.8 - 44.0 15.7 36.32019 254 k 49.2 46.1 44.1 - 40.2 0.8 0.8 - 46.1 24 42.1

* For a key to the antimicrobials used please see the table towards the beginning of this chapter

a 64 (14.5%) of these strains were DT104 and its variantsb 45 (13.7%) of these strains were DT104 and its variantsc 52 (12.2%) of these strains were DT104 and its variantsd 35 (18.3%) of these strains were DT104 and its variantse 47 (28.5%) of these strains were DT104 and its variantsf 33 (14.7%) of these strains were DT104 and its variantsg 39 (23.6%) of these strains were DT104 and its variantsh 52 (31.3%) of these strains were DT104 and its variantsi 67 (35.8%) of these strains were DT104 and its variantsj 47 (17.0%) of these strains were DT104 and its variantsk 67 (26.4%) of these strains were DT104 and its variants

Percentage of isolates resistant to:

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Table 12.3: Nalidixic acid resistance in Salmonella Typhimurium DT104 from domestic livestock in 2009 - 2019. Number of isolates tested (percentage resistant to nalidixic acid)

Cattle Sheep Pigs Chickens Turkeys Ducks2009 25 (8.0) 1 (0.0) 13 (15.4) 2 (0.0) 0 (0.0) 0 (0.0)

2010 19 (0.0) 2 (0.0) 3 (0.0) 5 (0.0) 2 (100.0) 0 (0.0)

2011 16 (18.8) 1 (0.0) 0 (0.0) 1 (0.0) 2 (100.0) 0 (0.0)

2012 6 (0.0) 2 (0.0) 5 (0.0) 0 (0.0) 0 (0.0) 0 (0.0)

2013 9 (33.3) 0 (0.0) 1 (0.0) 8 (0.0) 0 (0.0) 0 (0.0)

2014 10 (0.0) 0 (0.0) 1 (0.0) 0 (0.0) 0 (0.0) 0 (0.0)

2015 5 (0.0) 0 (0.0) 1 (0.0) 0 (0.0) 0 (0.0) 0 (0.0)

2016 11 (0.0) 7 (0.0) 2 (0.0) 5 (0.0) 0 (0.0) 0 (0.0)

2017 34 (5.9) 16 (0.0) 1 (0.0) 1 (0.0) 0 (0.0) 0 (0.0)

2018 20 (0.0) 12 (0.0) 1 (0.0) 0 (0.0) 0 (0.0) 0 (0.0)

2019 21 (0.0) 1 (0.0) 1 (0.0) 0 (0.0) 0 (0.0) 0 (0.0)

Livestock speciesYear

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Table 12.4: Trimethoprim/sulphonamide resistance in Salmonella Typhimurium (all phage types) from domestic livestock in 2009 – 2019. Number of isolates tested (percentage resistant to trimethoprim/sulphonamide)

Cattle Sheep Pigs Chickens Turkeys Ducks2009 70 (0.0) 4 (0.0) 237 (70.5) 41 (7.3) 1 (0.0) 11 (0.0)

2010 63 (4.8) 5 (20.0) 108 (66.7) 25 (4.0) 5 (40.0) 44 (9.1)

2011 39 (15.4) 1 (0.0) 244 (60.7) 20 (10.0) 6 (0.0) 40 (2.5)

2012 15 (6.7) 5 (0.0) 99 (72.7) 9 (22.2) 0 (0.0) 4 (0.0)

2013 24 (12.5) 0 (0.0) 71 (93.0) 12 (8.3) 0 (0.0) 3 (0.0)

2014 26 (11.5) 0 (0.0) 102 (66.7) 1 (0.0) 1 (0.0) 6 (0.0)

2015 9 (0.0) 0 (0.0) 52 (92.3) 6 (0.0) 0 (0.0) 2 (0.0)

2016 23 (8.7) 12 (0.0) 47 (87.2) 8 (0.0) 0 (0.0) 1 (0.0)

2017 52 (0.0) 25 (0.0) 39 (82.1) 5 (0.0) 0 (0.0) 5 (0.0)

2018 92 (2.2) 175 (0.0) 79 (87.3) 10 (0.0) 6 (0.0) 10 (0.0)

2019 51 (1.9) 4 (0.0) 58 (98.3) 12 (0.0) 0 (0.0) 2 (0.0)

YearLivestock species

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Table 12.5: Trends in trimethoprim/sulphonamide resistance in certain types of Salmonella Typhimurium from pigs over the period 2009 – 2019. Number of isolates tested (percentage resistant to trimethoprim/sulphonamide)

DT193 DT208 U2882009 71 (69.0) 2 (50.0) 100 (98.0)

2010 35 (57.1) 1 (0.0) 38 (89.5)

2011 39 (46.2) 1 (0.0) 55 (96.4)

2012 24 (62.5) 0 (0.0) 34 (94.1)

2013 22 (91.0) 0 (0.0) 21 (100.0)

2014 13 (100.0) 0 (0.0) 28 (96.4)

2015 9 (100.0) 0 (0.0) 23 (95.7)

2016 7 (100.0) 0 (0.0) 29 (96.6)

2017 19 (47.4) 0 (0.0) 26 (88.5)

2018 34 (67.6) 0 (0.0) 40 (97.5)

2019 17 (100.0) 0 (0.0) 27 (100.0)

YearDefinitive or undefined phage type

202

Figure 12.1: Number of isolates of S. Typhimurium of the eight most frequent phage types subjected to susceptibility testing at APHA 2010 – 2019

203

Figure 12.2: Percentage of the eight most common definitive and undefined phage types of Salmonella Typhimurium susceptible to all 16 antimicrobial agents in 2019

204

Table 12.6: Salmonella other than Salmonella Dublin and Salmonella Typhimurium: antimicrobial susceptibility monitoring 2009 - 2019

AM C NA S APR N FR SU TM T2009 1990 64.0 8.1 2.5 2.1 16.4 1.7 4.1 2.9 23.2 12.6 24.4

2010 2126 56.7 12.9 1.3 1.8 29.1 0.7 3.4 0.8 35.7 11.2 32.5

2011 1982 56.4 16.3 3.6 2.6 27.2 3.2 2.7 0.2 35.1 13.6 31.1

2012 2018 56.7 13.9 1.7 4.0 25.0 2.0 3.6 1.5 33.1 12.2 33.4

2013 2328 61.2 12.3 1.7 5.7 19.2 1.4 3.4 3.1 26.5 12.2 28.0

2014 1837 68.2 12.7 1.8 4.0 18.8 1.6 2.0 2.1 20.9 7.5 20.0

2015 2198 60.2 13.3 2.4 5.5 22.6 2.9 3.2 1.9 26.4 10.4 25.5

2016 1986 68.9 11.1 2.6 2.6 16.0 2.0 2.2 1.4 23.7 10.4 22.9

2017 5652 71.2 10.3 2.0 5.8 13.1 1.6 2.0 1.6 19.0 6.2 19.6

2018 3589 77.7 7.7 1.5 1.4 11.7 0.8 1.8 1.2 15.7 5.3 14.9

2019 4010 71.9 7.4 2.1 2.7 15.0 1.3 2.6 1.6 20.2 10.2 20.2

* For a key to the antimicrobials used please see the table towards the beginning of this chapter

Percentage susceptible to all 16

antimicrobials*Year No of

isolates Percentage of isolates resistant to:

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Table 12.7: All salmonellas: antimicrobial susceptibility 2019

Species No of isolates

Percentage susceptible to all 16

antimicrobials*AM AMC CAZ CTX C NA CIP S APR CN N FR SU TM T

Cattle 464 89.0 8.0 0.0 0.0 0.0 6.5 0.0 0.0 8.8 0.0 0.0 0.0 0.0 8.4 0.6 9.9

Sheep 82 98.8 0.0 0.0 0.0 0.0 0.0 0.0 0.0 1.2 0.0 0.0 0.0 0.0 1.2 0 0.0

Pigs 206 21.4 69.4 0.0 0.0 0.0 53.4 0.0 0.0 66.0 19.1 19.9 19.4 0.0 75.7 57.3 53.4

Chickens 1708 76.8 1.9 0.0 0.0 0.0 0.3 0.6 0.0 8.5 0.1 0.1 1.8 0.4 18.0 13.1 0.3

Turkeys 270 18.5 12.2 0.0 0.0 0.0 0 19.6 3.3 47.4 0.0 0.0 0.4 0.0 57.0 19.6 0.0

Ducks 299 79.9 4.0 0.0 0.0 0.0 0.0 0.0 0.0 9.4 0.0 0.0 6.4 15.1 1.7 0.0 0.0

Horses 146 71.9 11.0 0.0 0.0 0.0 4.8 2.7 0.0 9.6 0.0 0.0 0.0 0.0 10.3 4.1 4.8

Dogs 76 68.4 23.7 0.0 0.0 0.0 5.3 5.3 1.3 23.7 0.0 0.0 3.9 3.9 26.3 7.9 5.3Other non-avian species‡ 175 91.4 1.7 0.0 0.0 0.0 1.2 1.2 0.0 4.0 0.0 0.0 0.0 0.0 2.9 0.0 4.0

Other avian species† 33 72.7 15.2 0.0 0.0 0.0 3.0 3.0 1.3 24.2 0.0 0.0 0.0 0.0 21.2 3.0 3.0

Feed 1035 74.5 10.8 0.0 0.0 0.2 3.8 3.1 0.4 17.0 1.1 1.2 1.3 0.7 19.6 4.5 3.8

Environment 39 51.3 5.1 0.0 0.0 0.0 2.6 7.7 2.6 5.1 0.0 0.0 2.6 7.7 41.0 33.3 2.6

TOTAL 4533 72.2 9.1 0.0 0.0 0.04 4.4 2.4 0.4 15.6 1.2 1.2 2.4 1.4 20.5 10.4 4.4

* For a key to the antimicrobials used please see the table towards the beginning of this chapter

‡ Alpacas, camels, cats, donkeys, goats, hedgehogs, leopards, lions, lizards, racoon dogs, reptiles/amphibians, snakes, tigers, turtles, wallabies and unspecified mammals

† Canaries, cranes, finches, partridges, pheasants, pigeons and quail

Percentage of isolates resistant to:

No isolates were resistant to amikacin

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Further Publications of Interest Andres VM, Davies RH (2015) Biosecurity measures to control salmonella and other infectious agents in pig farms: a review.

Comprehensive Reviews in Food Science and Food Safety 14 (4), pp. 317-335. http://dx.doi.org/10.1111/1541-4337.12137.

Anjum MF, Duggett NA, Aboun M, Randall L, Nunez-Garcia J, Ellis RJ, Rogers J, Horton R, Brena C, Williamson S, Martelli F, Davies R, Teale C (2016) Colistin resistance in salmonella and Escherichia coli isolates from a pig farm in Great Britain. Journal of Antimicrobial Chemotherapy 71 (8), pp. 2306-2313.

APHA (2018) Salmonella in Livestock Production in GB 2017 (ISBN 1 8995 1350 7). https://www.gov.uk/government/publications/salmonella-in-livestock-production-in-great-britain-2017

APHA (2017) Salmonella in Livestock Production in GB 2016 (ISBN 1 8995 1348 5). https://www.gov.uk/government/publications/salmonella-in-livestock-production-in-great-britain-2016

APHA (2018) Veterinary Investigation Surveillance Annual Report (VIDA) 2017. http://apha.defra.gov.uk/documents/surveillance/pub-surv-vida2017.pdf

APHA (2018) Veterinary Investigation Surveillance Report (VIDA) 2016 (ISBN 1 8995 1349 43). https://www.gov.uk/government/publications/veterinary-investigation-diagnosis-analysis-vida-report-2016

Arsevska E, Singleton D, Sanchez-Vizcaino F, Williams N, Jones PH, Smythe S, Heayns B, Wardeh M, Radford AD, Dawson S, Noble PJM and Davies RH (2017) Small animal disease surveillance: GI disease and salmonellosis. Veterinary Record 181 (9), pp. 228-232.

Azevedo C, Bohning D and Arnold M (2017) A ratio regression approach to estimate the size of the salmonella-infected flock population using validation information. In Bohning D; van der Heijden PGM; Bunge J (eds), Capture-Recapture Methods for the Social and Medical Sciences, Boca Raton, Taylor and Francis, pp. 61-78.

Birch C; Davies RH (2016) An in-vitro investigation into the efficacy of disinfectants used in the duck industry against salmonella. Avian Pathology 45 (5), pp. 576-581.

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Branchu P, Charity OJ, Bawn M, Thilliez G, Dallman TJ, Petrovska L, Kingsley RA (2019) SGI-4 in monophasic Salmonella typhimurium ST34 is a novel ICE that enhances resistance to copper. Frontiers in Microbiology 10 Article 1118.

Card R, Vaughan K, Bagnall M, Spiropoulos J, Cooley W, Strickland T, Davies R, Anjum MF (2016) Virulence characterisation of Salmonella enterica isolates of differing antimicrobial resistance recovered from UK livestock and imported meat samples. Frontiers in Microbiology 7, Article 640.

Carter A, Adams M, La Ragione RM and Woodward MJ (2017) Colonisation of poultry by Salmonella enteritidis S1400 is reduced by combined administration of Lactobacillus salivarius 59 and Enterococcus faecium PXN-33. Veterinary Microbiology 199, pp. 100-107.

Chousalkar K, Gast R, Martelli F and Pande V (2018) Review of egg-related salmonellosis and reduction strategies in United States, Australia, United Kingdom and New Zealand. Critical Reviews in Microbiology 44 (3), pp. 290-303.

Davies R (2019) Salmonellosis. Manual of diagnostic tests and vaccines for terrestrial animals 2019 pp.1735-1752.

Davies RH, Lawes JR, Wales AD (2019) Raw diets for dogs and cats: a review, with particular reference to microbiological hazards. Journal of Small Animal Practice 60 (6) pp. 329-339.

Davies R, Wales A (2019) Antimicrobial resistance on farms: a review including biosecurity and the potential role of disinfectants in resistance selection. Comprehensive Reviews in Food Science and Food Safety 18 (3) pp. 753-774.

Davies R, Gosling RJ, Wales AD, Smith RP (2016) Use of an attenuated live Salmonella typhimurium vaccine on three breeding pig units: a longitudinal observational field study. Comparative Immunology, Microbiology and Infectious Diseases 46, pp. 7-15.

Davies R, Kingsley RA (2016) Microevolution of monophasic Salmonella typhimurium during epidemic, United Kingdom, 2005–2010. Emerging Infectious Diseases 22 (4), pp. 617-624.

De Lucia A, Rabie A, Smith RP, Davies R, Ostanello F, Ajayi D, Petrovska L and Martelli F (2018) Role of wild birds and environmental contamination in the epidemiology of salmonella infection in an outdoor pig farm. Veterinary Microbiology 227, pp. 148-154.

EEC (2011) Commission Regulation (EU) No. 142/2011. Official Journal L54, pp. 1-254. Commission Regulation (EU) No. 142/2011 implementing Regulation (EC) No. 1069/2009 of the European Parliament and of the Council laying down health rules as regards animal by-products and derived products not intended for human consumption and implementing Council Directive 97/78/EC as regards certain samples and items exempt from veterinary checks at the border under that Directive.

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Defra (2016) Salmonella: get your broiler flock chickens tested. https://www.gov.uk/guidance/salmonella-get-your-broiler-flock-chickens-tested

Defra (2016) Laying hens and flocks: poultry testing for salmonella. https://www.gov.uk/guidance/salmonella-get-your-egg-laying-hens-tested

Defra (2018) Chicken breeders: poultry testing for salmonella. https://www.gov.uk/guidance/salmonella-get-your-breeding-chickens-tested

Defra (2016) Salmonella: get your fattening turkeys tested. https://www.gov.uk/guidance/salmonella-get-your-fattening-turkeys-tested

Defra (2019) Turkey breeders: poultry testing for salmonella. https://www.gov.uk/guidance/salmonella-get-your-breeding-turkeys-tested

EFSA Panel on Biological Hazards (BIOHAZ); Koutsoumanis K, Allende A, Alvarez-Ordonez A, Bolton D, Bover-Cid S, Chemaly M, De Cesare A, Herman L, Hilbert F, Lindqvist R, Nauta M, Peixe L, Ru G, Simmons M, Skandamis P, Suffredini E, Dewulf J, Hald T, Michel V, Niskanen T, Ricci A, Snary E, Boelaert F, Messens W, Davies R 2019 Salmonella control in poultry flocks and its public health impact. EFSA Journal 17 (2) e05596.

Figueiredo R, Card RM, Nunez-Garcia J, Mendonca N, Jorge de Silva G, Anjum MF (2019) Multidrug-resistant Salmonella enterica isolated from food animal and foodstuff may also be less susceptible to heavy metals. Foodborne Pathogens and Disease 16 (3) pp. 166-172.

Gavin C, Simons RRL, Berriman ADC, Moorhouse D; Snary EL, Smith RP and Hill AA (2018) A cost-benefit assessment of Salmonella-control strategies in pigs reared in the United Kingdom. Preventive Veterinary Medicine 160, pp. 54-62.

Gosling RJ, Mueller-Doblies D, Martelli F, Nunez-Garcia J, Kell N, Rabie A, Wales AD and Davies RH (2018) Observations on the distribution and persistence of monophasic Salmonella typhimurium on infected pig and cattle farms. Veterinary Microbiology 227, pp. 90-96.

Gosling RJ, Mawhinney I, Vaughan K, Davies RH and Smith RP (2017) Efficacy of disinfectants and detergents intended for a pig farm environment where salmonella is present. Veterinary Microbiology 204, pp. 46-53.

Hateley G and Carson A (2017) Salmonella investigations in ruminants. Veterinary Record 181 (14), pp. 366-367.

Hayward MR, Petrovska L, Jansen VAA, Woodward MJ (2016) Population structure and associated phenotypes of Salmonella enterica serovars Derby and Mbandaka overlap with host range. BMC Microbiology 16:15.

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Hill AA, Simons RRL, Kelly L, Snary EL (2016) A farm transmission model for salmonella in pigs, applicable to E.U. member states. Risk Analysis 36 (3), pp. 461-481.

Horton RA, Card R, Randall LP, Teale CJ (2016) Differentiation of UK endemic strains of Salmonella enterica serovar Newport from epidemic North American strains by PCR detection of a truncated bapA chromosomal gene. Research in Veterinary Science 104, pp. 113-116.

Kanagarajah S, Waldram A, Dolan G, Jenkins C, Ashton PM, Martin AIC, Davies R, Frost A, Dallman TJ, De Pinna EM, Hawker JI, Grant KA and Elson R (2018) Whole genome sequencing reveals an outbreak of Salmonella enteritidis associated with reptile feeder mice in the United Kingdom, 2012-2015. Food Microbiology 71, pp. 32-38.

Lawson B, Franklinos LHV, Rodriguez-Ramos Fernandez J, Wend-Hansen C, Nair S, Macgregor SK, John SK, Pizzi R, Nunez A, Ashton PM, Cunningham AA and de Pinna EM (2018) Salmonella enteritidis ST183: emerging and endemic biotypes affecting western European hedgehogs (Erinaceus europaeus) and people in Great Britain. Scientific Reports 8 (1) Art. no. 2449.

Marier E, Smith RP, Ellis-Iversen J, Watson E, Armstrong D, Hogeveen H, Cook AJC (2016) Changes in perceptions and motivators that influence the implementation of on-farm salmonella control measures by pig farmers in England. Preventive Veterinary Medicine 133, pp. 22-30.

Marin C, Martelli F, Rabie A and Davies R (2018) Commercial frozen mice used by owners to feed reptiles are highly externally contaminated with Salmonella enteritidis PT8. Vector-Borne and Zoonotic Diseases 18 (9), pp. 453-457.

Martelli F, Andres VM, Davies R and Smith RP (2018) Observations on the introduction and dissemination of salmonella in three previously low prevalence status pig farms in the United Kingdom. Food Microbiology 71, pp. 129-134.

Martelli F, Kidd S, Lawes J (2019) Surveillance for salmonella in horses in Great Britain. Veterinary Record 184 (2) pp. 56-58.

Martelli F, Kidd S and Lawes J (2018) Salmonella and salmonellosis in horses: an overview. Veterinary Record 182 (23), pp. 659-660.

Martelli F, Gosling RJ, Callaby R and Davies R (2017) Observations on salmonella contamination of commercial duck farms before and after cleaning and disinfection. Avian Pathology 46 (2), pp. 131-137.

Martelli F, Lambert M, Butt P, Cheney T, Tatone FA, Callaby R, Rabie A, Gosling RJ, Fordon S, Crocker G, Davies RH and Smith RP (2017) Evaluation of an enhanced cleaning and disinfection protocol in salmonella contaminated pig holdings in the United Kingdom. PLoS ONE 12(6): e0178897.

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Martelli F, Wales A and Davies R (2017) Of mice and hens - tackling salmonella in table egg production in the United Kingdom and Europe. In: Ricke SC (ed); Gast RK (ed), Producing safe eggs: microbial ecology of salmonella, Elsevier, London, 2017, pp. 3-23.

Martelli F, Birch C, Davies RH (2016) Observations on the distribution and control of salmonella in commercial duck hatcheries in the UK. Avian Pathology 45 (2), pp. 261-266.

Mellor KC, Petrovska L, Thomson NR, Harris K, Reid SWJ, Mather AE (2019) Antimicrobial resistance diversity suggestive of distinct Salmonella typhimurium sources or selective pressures in food-production animals. Frontiers in Microbiology 10 Article No. 708.

Mensah N, Tang Y, Cawthraw S, Abuoun M, Fenner J, Thomson NR, Mather AE, Petrovska-Holmes L (2019) Determining antimicrobial susceptibility in Salmonella enterica serovar Typhimurium through whole genome sequencing: a comparison against multiple phenotypic susceptibility testing methods. BMC Microbiology 19 p. 148.

Morris VK, Carrique-Mas JJ, Mueller-Doblies D, Davies RH, Wales AD, Allen VM (2015) A longitudinal observational study of salmonella shedding patterns by commercial turkeys during rearing and fattening, showing limitations of some control measures. British Poultry Science 56 (1), pp. 48-57. http://dx.doi.org/10.1080/00071668.2014.991273

Mueller-Doblies D, Speed KCR, Kidd S and Davies RH (2018) Salmonella typhimurium in livestock in Great Britain – trends observed over a 32-year period. Epidemiology and Infection 146 (4), pp. 409-422.

Muller-Doblies D, Mawhinney I, Martelli F, Gosling R, Rabie A and Davies RH (2018) Practical aspects of the suitability of different sampling methods for detecting salmonella infection in duck flocks. Journal of Applied Poultry Research 27 (4), pp. 616-626.

Naqid IA, Owen JP, Maddison BC, Spiliotopoulos A, Emes RD, Warry A, Flynn RJ, Martelli F, Gosling RJ, Davies RH, La Ragione RM, Gough KC (2016) Mapping B-cell responses to Salmonella enterica serovars typhimurium and enteritidis in chickens for the discrimination of infected from vaccinated animals. Scientific Reports 6, Article number: 31186.

PHE (2017) Zoonoses Summary Report UK 2015. https://www.gov.uk/government/uploads/system/uploads/attachment_data/file/621094/UK_Zoonoses_report_2015.pdf

Powell LF, Cheney TEA, Williamson S, Guy E, Smith RP, Davies RH (2016) A prevalence study of Salmonella spp., Yersinia spp., Toxoplasma gondii and porcine reproductive and respiratory syndrome virus in UK pigs at slaughter. Epidemiology and Infection 144 (7), pp. 1538-1549.

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Sevellec Y, Felten A, Radomski N, Granier SA, Le Hello S, Petrovska L, Mistou M-Y, Cadel-Six S (2019) Genetic diversity of Salmonella derby from the poultry sector in Europe. Pathogens 8 (2) p. 46.

Simons RRL, Hill AA, Swart A, Kelly L, Snary EL (2016) A transport and lairage model for salmonella transmission between pigs applicable to EU member states. Risk Analysis 36 (3), pp. 482-497.

Smith RP, Andres V, Cheney TE, Martelli F, Gosling R, Marier E, Rabie A, Gilson D and Davies RH (2018) How do pig farms maintain low salmonella prevalence: a case-control study. Epidemiology and Infection 146 (15), pp. 1909-1915

Smith RP, Andres V, Martelli F, Gosling B, Marco-Jimenez F, Vaughan K, Tchorzewska M and Davies R (2018) Maternal vaccination as a Salmonella typhimurium reduction strategy on pig farms. Journal of Applied Microbiology 124 (1), pp. 274-285.

Smith RP, Andres V, Dormer L, Gosling R, Oastler C and Davies RH (2017) Study of the impact on salmonella of moving outdoor pigs to fresh land. Epidemiology and Infection 145 (10) pp. 1983-1992.

Snary EL, Swart AN, Hald T (2016) Quantitative microbiological risk assessment and source attribution for salmonella: taking it further. Risk Analysis 36 (3), pp. 433-436.

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Wales A, Davies R (2019) Antimicrobial drug resistance in poultry. What do we know about risk factors? Zootecnica International 4th September 2019, 1-6.

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Wales AD and Davies RH (2017) Salmonella vaccination in pigs: a review. Zoonoses and Public Health 64 (1), pp. 1-13.

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Quality Statement

Section A

1. Coherence

Reports are obtained by various routes: direct submissions to APHA Veterinary Investigation Centres, reports of Salmonella isolations by private laboratories and Scottish submissions to Scotland’s Rural College (SRUC).

APHA is responsible for collation of data. Submissions result from cases of clinical disease in livestock, monitoring of healthy livestock and investigations of possible links with a human Salmonella outbreak.

All private laboratories submitting reports of Salmonella isolates to APHA do so using the standard APHA submission & supplementary forms or customised forms developed for them by APHA. Scottish submissions use the SRUC submission form & supplementary forms which are compatible with the APHA system and interpreted in the same way. All use the same definitions and essential categorisation.

An incident comprises the first isolation and all subsequent isolations of the same serovar or serovar and phage/definitive type combination of Salmonella from an animal, group of animals or their environment on a single premises, within a defined time period (usually 30 days).

An antimicrobial susceptibility test is performed for surveillance purposes against an extended panel of 16 antimicrobials on Salmonella isolates sent for serotyping to APHA Weybridge and APHA Lasswade.

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Antimicrobial Concentration ( µg per ml)

Code

1 Nalidixic acid 30 NA

2 Tetracycline 10 T

3 Neomycin 10 N

4 Ampicillin 10 AM

5 Furazolidone 15 FR

6 Ceftazidime 30 CAZ

7 Sulphamethoxazole/ trimethoprim 25 TM

8 Chloramphenicol 30 C

9 Amikacin 30 AK

10 Amoxicillin/ clavulanic acid 30 AMC

11 Gentamicin 10 CN

12 Streptomycin 10 S

13 Sulphonamide compounds 300 SU

14 Cefotaxime 30 CTX

15 Apramicin 15 APR

16 Ciprofloxacin 1 CIP

This panel is updated when there is a clear need to detect new or emergent types of resistance or to replace outdated antimicrobials. On specific occasions (e.g. detection of Salmonella vaccine strains, characterisation of 3rd generation cephalosporins resistance) more than 16 antimicrobials are used for susceptibility testing.

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From 1st January 2007, some of the breakpoints used in assessing antimicrobial resistance, which were previously set at less than or equal to 13mm, were changed. These new breakpoints were set at: Ceftazidime (CAZ) less than or equal to 27mm, Amikacin (AK) less than or equal to 18mm, Ciprofloxacin (CIP) less than or equal to 19mm and Cefotaxime (CTX) less than or equal to 29mm. This may result in an increased number of isolates resistant to these antimicrobials in 2007 and the subsequent years in comparison with previous years. The breakpoint for all other antimicrobials used remains at less than or equal to 13mm.

In 2008, the disc concentrations for streptomycin and chloramphenicol were changed to adopt the disc concentrations recommended by the British Society for Antimicrobial Chemotherapy (BSAC). In the case of streptomycin, the disc concentration was reduced from 25µg to 10µg. The zone size remained unchanged, so this change would be expected to increase the detection of isolates with lower level streptomycin resistance. Work done at APHA has shown that the 10µg disc provides much better discrimination between resistant and sensitive isolates (defined using the gold standard measure of MIC determination) than the 25µg disc.

The only other change made to the breakpoints and disc concentrations used over the period 2008-2015 related to the ceftazidime disc where the zone size was reduced from 29 to 26mm in 2012, in line with BSAC recommendations.

Some of the Salmonella serovars are recorded and reported in APHA under the old nomenclature. The nomenclature for these serovars under the original Kauffmann-White scheme is clarified in the table below:

APHA Serovar White-Kauffmann-Le Minor Serovar

Pullorum Gallinarum (biovar Pullorum)

Java Paratyphi B var. Java

Newington Anatum var. 15+

The Salmonella serovars S. Binza and S. Thomasville, which were previously recorded by the APHA under their old nomenclature, are now recorded using the White-Kauffmann-Le Minor notation as Salmonella Orion var. 15+ and Salmonella Orion var. 15+ 34+ respectively. This change was implemented during 2008.

2. Accuracy and precision

Sampling error: Isolations of Salmonella from statutory species are required to be reported, however the level of detection and testing (for species without a NCP) depends on submission of samples for laboratory investigation by private vets as well as on economic and other factors e.g. distance to laboratories etc.

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A susceptibility test is often performed on representative Salmonella isolates before the allocation of an automatic incident reference by the computer system. It is important for the Veterinary Investigation Centres to provide information to the testing laboratory on whether the submitted isolates are considered to comprise new incidents. As some companies perform extensive testing for Salmonella, this could skew the overall antimicrobial resistance data leading to the patterns obtained, at least in part, reflecting the intensity of sampling procedure. Also, limited resources may prevent susceptibility testing of all isolates. More than one isolate per incident is usually tested in cases where the resistance pattern of the serovar/phage type is likely to be of particular public health relevance in terms of antimicrobial resistance. These include S. Infantis, S. Kentucky, S, Newport, S. Heidelberg and S. Typhimurium DT104.

Coverage error: The reasons for sample submissions (particularly for non-NCP samples) need to be considered, as sources of error can be dependent on this factor. Also the ability to isolate Salmonella needs to be considered (dependent on sample type taken, age of sample, storage and transport, culture method used, laboratory staff technical expertise etc).

Non-response error: Although all Salmonella isolations from statutory species are required to be reported, not all data items requested are mandatory under the Zoonoses Order. Different categories of submissions may have different non-response rates for different data items.

Measurement error: Different Salmonella culture methods vary in their sensitivity, which varies according to sample type, type of Salmonella present and profile of competitive flora in the sample. Data on the APHA and SRUC forms are subject to individual interpretation by the person submitting the information, despite the guidance to authorised personnel.

The requirement of this report is to include as much data as is available. However only approved submissions are included, although efforts are made to ensure that all submissions are approved before the data is extracted. Data are scrutinised to correct errors in results for strategically important isolates (e.g. resistant to 3rd generation cephalosporins, resistant to ACSSuT pattern). It is not expected to routinely see resistance to amikacin, ciprofloxacin, ceftazidime or cefotaxime in any isolate. If any appears, it is followed up at the time of detection and the isolate would normally be re-tested.

Both laboratories at APHA Lasswade and APHA Weybridge that perform the expanded susceptibility testing have third party accreditation to ISO17025 provided by UKAS.

Data processing error: It is often difficult to obtain the required information from the sample submitted for non-mandatory data. It is the responsibility of the Nominated Officer to ensure that the data are accurate and complete. A validation exercise is carried out on a weekly basis at the APHA Veterinary Investigation Centres and by DES, and on a quarterly basis for NCP submissions.

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As a result of refinements to the method of defining incidents, it may not always be possible to reproduce isolation figures in previously published reports.

3. Timeliness and punctuality

The report includes provisional data (with the exception of the flock-level data for the chicken and turkey NCPs) which are subject to change. The APHA Salmonella warehouse is updated every night.

4. Accessibility and clarity

Salmonella data (APHA) have a related metadata profile (see section B).

5. Comparability

Salmonella cases in animals are reported both as isolations and incidents. An incident is defined as the first and all subsequent isolations of the same serovar or serovar and phage type combination of a particular Salmonella from an animal, group of animals or their environment on a holding within a defined time period, which is usually 30 days. An incident report is a herd/ flock (which is the epidemiological group of interest) level outcome.

Changes in the number of Salmonella isolations from poultry and pigs over time may reflect changes in the monitoring activity conducted by the livestock industry and not necessarily changes in incidence in Salmonella infection. The number of tests carried out by authorised laboratories is collated by Defra.

Sampling error, coverage error and measurement error is minimised for submissions from NCP samples as they follow a robust, harmonised protocol and test method.

Chicken and turkey data are not directly comparable before and after implementation of the NCPs. For example, before 2010 the turkey NCP was not in operation so all turkey submissions were voluntary whereas from the beginning of 2010, most turkey submissions were from statutory monitoring. Comparisons are more valid for years in which the NCPs have run for a full year previously.

The data on positive findings of Salmonella in laying, breeding and broiler chicken flocks, and in turkey flocks is reported as the number of positive flocks, as required by the legislation, as well as the number of positive isolations detected during the year. The number of reported isolations of Salmonella detected in chickens and turkeys does not equate directly to the overall number of positive flocks that are detected during the year. A flock is counted as positive only once, irrespective of the number of isolations occurring and the number of serovars identified.

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Hatchery isolations not associated with a specific flock.

Starting with samples collected from 1st January 2006, any hatchery isolates where there are no supply flock details available are treated as isolations only and not incidents as they cannot be traced back to a specific flock.

SRUC and other isolations/reports without cultures submitted.

Submissions received from the Scotland’s Rural College (SRUC), and any submissions received without a sample are now allocated an incident reference whereas previously these were not allocated such references. These reports appear in the quarterly reports. This improvement was put in place for all reports on the database in 2008.

Not all isolates of S. Typhimurium from bovine animals received from SRUC are phage typed. As the system does not allocate an incident reference number to a report of S. Typhimurium until the phage type result is received, this means that some isolates of S. Typhimurium from SRUC will not be allocated an incident reference and therefore the actual number of incidents of S. Typhimurium may be higher than the number recorded on the database.

APHA Quality Assurance Statement

The policy of the Animal and Plant Health Agency (APHA) is to ensure that its products and services fully meet the agreed needs of its customers, including those defined by statutory and regulatory requirements. APHA is committed to good professional practice and aims to support this commitment through the use of management systems that will be reviewed to assess effectiveness and to foster continual improvement.

The laboratory facilities are accredited by BS EN ISO 17025:2017 (Accreditation Lab No 1769 ) for an extensive range of tests supported by proficiency testing accredited to BS ISO 17043:2010 (Accreditation No. 0004). APHA is certificated to BS EN ISO 9001:2015 for ‘the provision of a range of specialist scientific services and products to the Government and other interested parties worldwide the provision of administrative services and control of technical services supporting regulation and enforcement of EU plant and seed directives’ (certificate number LRQ 4001392). This excludes work relating to field based veterinary surveillance and regional laboratory testing, which is covered by ISO 17025 and ISO 17043.

APHA research complies with the requirements of the Joint Code of Practice for Research.

APHA also holds approvals to Good Laboratory Practice and Good Manufacturing Practice and complies with Good Clinical Veterinary Practice (Veterinary).

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Section B

Metadata Elements

Metadata elements Definition

Creator Salmonella Surveillance Team, DES, APHA Weybridge, New Haw, Addlestone, Surrey KT15 3NB

Date created 23/03/2020 data retrieval from FarmFile/Salmonella database

Identifier Salmonella Annual Surveillance Report 2019, Version 1

Quality See Section A

Publisher Salmonella Surveillance team, DES, APHA Weybridge, New Haw, Addlestone, Surrey, KT15 3NB

Source FarmFile/ Salmonella database.

Title Salmonella in Livestock Production in GB 2019

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Additional Report Metadata Elements

Metadata elements Definition

Coverage spatial Salmonella reports made in Great Britain

Date. Issued 11/09/2020

Date. Updating frequency Annually

Format medium Word document

Language English

Mandate authorising statutes Data collected under:

Zoonoses Order 1989

CSPO 2007

CSBO 2009

CSTO 2009

ABPR 2013

IPAPO 1981

Rights. copyright Crown copyright

Subject. Category Zoonoses, Animal Health

Subject. Keywords Salmonella, Livestock

Subject. programme Bacterial Diseases and Food Safety

Subject. project Surveillance of Salmonella in animals (FZ2000)

Monitoring of Antimicrobial Resistance in Bacteria from Animals and their Environment (OM0190)

Microbiological monitoring of Animal By Products, laboratory inspection scheme

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Metadata elements Definition

and Quality Assurance sample supply (ABPR & IPAPO) (FZ2000)

Status Approved by: Rob Davies (rob.davies@apha.gov.uk)

Version 1

Type Report

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Acknowledgements Isolations were reported by Nominated Officers of the Animal and Plant Health Agency for England and Wales and Divisional Veterinary Managers for Scotland and, through them, by private laboratories.

Regional Veterinary Leads of the Animal and Plant Health Agency are responsible for the collection of samples of processed animal protein.

Staff of the Animal and Plant Health Agency processed the data.

The following reference laboratories made or confirmed the majority of isolations:

Animal and Plant Health Agency, Weybridge and Lasswade.

Gastrointestinal Bacteria Reference Unit, PHE Colindale

Scottish Salmonella Reference Laboratory, Glasgow.

This report was compiled by:

Joanna Lawes, Susan Withenshaw and Sue Kidd

Department of Epidemiological Sciences,

Animal and Plant Health Agency,

New Haw,

Addlestone,

Surrey,

KT15 3NB

Telephone: + 44 (0)208 026 0682

E-mail sue.kidd@apha.gov.uk

APHA is an Executive Agency of the Department for Environment, Food and Rural Affairs and was formed on 1st October 2014. Prior to this it was known as AHVLA.