listeria monocytogenes in the smoked salmon industry

International Journal of Food Microbiology 62 (2000) 183–190www.elsevier.nl / locate / ijfoodmicro

Listeria monocytogenes in the smoked salmon industry

,1Liv Marit Rørvik*

The Norwegian School of Veterinary Science, Department of Pharmacology, Microbiology and Food Hygiene, P.b. 8146 Dep., 0033Oslo, Norway

Accepted 25 April 2000

Abstract

Smoked salmon is sporadically contaminated with Listeria monocytogenes. Contamination levels are normally low andconsumers are probably seldom exposed to risk concentrations. No clones of L. monocytogenes seem to be specific tosmoked salmon, some clones found in smoked salmon having been isolated from several sources, including patients.Cold-smoking has been shown to eliminate L. monocytogenes in challenge tests at temperatures from 17.1 to 21.18C, whilefrom 22.2 to 308C the bacteria survived. Under natural cold-smoking conditions (19 to 228C) the frequency and level of L.monocytogenes seems to decrease. Hot-smoking seems to eliminate the bacteria when smoke is applied during the wholeheating process. The prevention of recontamination of both cold-smoked and hot-smoked salmon is therefore of greatimportance. L. monocytogenes multiply considerably in smoked salmon during storage. Growth is faster in challenge teststhan in naturally-contaminated smoked salmon. The declared shelf-life under refrigeration should be shorter than thatcustomarily stipulated by many producers. While the sources of L. monocytogenes in smoked salmon processing plants havestill to be determined, raw salmon does not seem to be an important source. The main issue for producers is to preventcolonization of the processing environment and spread of the bacteria to products. This should be achieved by the systemicimplementation of hygienic measures, including the HACCP approach. 2000 Elsevier Science B.V. All rights reserved.

Keywords: Smoked salmon; Listeria monocytogenes; Hygiene

1. Introduction tures of weeks. The salt content, pH and wateractivity values are normally within a range permit-

Cold-smoked and hot-smoked salmon are ready- ting the growth of Listeria monocytogenes (Seeligerto-eat foods which are normally purchased vacuum- and Jones, 1984). Contaminated cold-smoked rain-packed and with a shelf-life at refrigeration tempera- bow trout was recently considered to be the source of

five listeriosis cases in Finland, and gravad, cold-smoked or hot-smoked products of rainbow trout

*Tel.: 1 47-2250-7308; fax: 1 47-2259-7475.were earlier suspected to cause a few cases inE-mail address: [email protected] (L.M. Rørvik).

1 Sweden (Ericsson et al., 1997; Miettinen et al.,Present address: National Veterinary Institute, P.O. Box 8156Dep., Oslo. 1999). Smoked salmon and smoked rainbow trout

0168-1605/00/$ – see front matter 2000 Elsevier Science B.V. All rights reserved.PI I : S0168-1605( 00 )00334-2

184 L.M. Rørvik / International Journal of Food Microbiology 62 (2000) 183 –190

are therefore considered to be risk products for positive samples, with the figures referring roughlyhuman listeriosis, and L. monocytogenes contamina- to the start and the end of shelf-life. They observedtion is of great concern for the smoked fish industry. that the prevalence over time was stable for each

processing plant and ranged from 0.1 to 100%. Thedifferent studies are difficult to compare, with biases

2. Smoked salmon regarding the number of samples from each plant,the time of analysis during shelf-life, etc.

Smoking was traditionally applied as a preserva- For hot-smoked salmon, Ben Embarek reportedtion method, but the sensoric influence of smoking is about 9% contamination, while other studies havenow more important. Smoking of salmon may imply reported contamination rates ranging from 0 to 8.1%cold-smoking at below 308C or hot-smoking at high (Fuchs and Nicolaides, 1994; Heinitz and Johnson,temperatures ( . 608C). 1998).

The production of smoked salmon includes fillet- Although studies of L. monocytogenes contamina-ing, salting, drying, smoking, trimming and packag- tion in smoked salmon have often only been quali-ing. The process involves a lot of handling by tative, some information is available on contamina-workers, as well as the use of technically often tion levels. Most often , 100 cfu /g are detectedcomplex equipment. The fillets may be dry salted or (Eklund et al., 1995; Schmidt et al., 1997; Jørgensenbrined in a bath or by injection, the salt content and Huss, 1998), but Jørgensen and Huss found fourvarying with the consumer preferences. Smoking of 76 positive samples to contain . 1000 cfu /g,may be performed in a smoke oven or by using while 12/76 contained 100–1000 cfu /g, all afterliquid smoke, the intensity of smoking also varying $ 14 days of storage. Loncarevic et al. (1996) foundwith the customers’ taste. Retail products therefore levels as high as 25,400 cfu /g in cold-smokedshow great diversity in salt concentration, colour and rainbow trout, and 132,000 cfu /g in hot-smokedtaste. salmon. The latter item was smoked in a plant where

The preservation effect of smoking is partly due to a fish product earlier had been associated withlower water activity together with the formation of a gastrointestinal disease (Tham, personal communica-more membranous surface caused by salting and tion). The cold-smoked rainbow trout associated withdrying, which constitutes a physical barrier and the Finnish outbreak contained 190,000 cfu /g (Miet-inhibits growth of microorganisms. The smoke fur- tinen et al., 1999).ther contains a wide variety of compounds, including Consumers seem to be sporadically exposed to L.formaldehydes and phenols, and is known to have monocytogenes from smoked salmon. Contaminationbacteriostatic or bactericidal effects. levels are normally low, and though high levels are

Because smoking conditions are not standardized, found from time to time, consumers are probably notthe effect of smoking on bacteria, and the inhibitory often exposed to smoked salmon with potentiallyeffect during storage, may vary for cold-smoked and hazardous levels of L. monocytogenes.hot-smoked salmon from different producers.

4. Types of L. monocytogenes in smoked salmon3. Occurrence and levels of L. monocytogenes insmoked salmon To assess the significance of L. monocytogenes in

smoked salmon, it is important to know if theL. monocytogenes has been found in smoked processing environment and the products are niches

salmon in several studies. In a review of cold- for particular types of the bacteria, and if the samesmoked salmon samples, Ben Embarek (1994) re- types are seen in patients. The majority of L.ported a contamination rate of between 0% and 75%, monocytogenes isolated from smoked salmon belongwith an overall prevalence of 10%. In Norway, the to serotype 1/2 (or 1 when Difco antisera arefrequency decreased from 9 to 3% from 1991 to employed), although other serotypes are also occa-1996/97 (Ben Embarek, 1994; Lunestad, 1998). sionally found. Studies on isolates from smokedJørgensen and Huss (1998) reported 34 to 43% salmon or other fish isolates with other typing

L.M. Rørvik / International Journal of Food Microbiology 62 (2000) 183 –190 185

methods are scarce, but some information is avail- 26–30 h. No change was seen in the number ofable. Boerlin et al. (1997) examined 64 foreign bacteria after smoking. Eklund et al. (1995) foundisolates from 10 fish products and found no associa- that L. monocytogenes inoculated on the surface oftion between specific products and particular electro- salmon fillets decreased 10–25-fold when smokingphoretic types (ETs). Some ETs were common to temperatures of 17.2–21.18C were used, while theseveral producers, but could be differentiated by decrease was only threefold when the temperaturesREA or PFGE. There was a significant genetic were 22.2–308C. L. monocytogenes injected into thedifference between human and fish isolates. Nørrung flesh increased 2–20-fold and 100-fold, respectively.and Skovgaard (1993) found eight ETs among 20 Contamination of the salmon flesh by injected brinefish isolates, with five of these also found in humans. containing L. monocytogenes may therefore be fol-Thirty percent of the fish isolates were ET4/serotype lowed by an increase in the levels during cold-1, which was also predominant in meat, while only smoking. Recirculation of brine increases the risk of5% of human isolates were this type. No ET4/ in-flesh contamination. Others have reported inac-serotype 4 isolates, which comprise 22% of human tivation of L. monocytogenes in the presence ofisolates, were found in fish. The most common ET liquid smoke (Messina et al., 1988; Faith et al.,from clinical cases, ET1, was only sporadically 1992).found in fish samples. No connection between fish In one smokehouse, L. monocytogenes and otherisolates and patients could be demonstrated because Listeria spp. were found in fish samples after alldifferentiation within ETs by other typing methods processing steps except after smoking, and beforewas not performed. In a study (Rørvik et al., 1996) further handling was completed (Rørvik et al., 1995).of 46 isolates from 25 smoked salmon processing Further investigations were therefore done to see ifplants, 14 ETs were represented, several being found smoking had an effect on L. monocytogenes inin more than one plant (up to six). Three ETs were naturally contaminated salmon (Aase and Rørvik,found in both smoked salmon and patients, and on 1997). Salted fillets from four smokehouses werethree occasions isolates with the same ET and REA examined for L. monocytogenes just before theytype were found in both smoked salmon or the were put into the smoke oven (Table 1). The smokedsmoked salmon processing environment and patients fillets were sampled when the oven was opened andin the same region. Possible connections between examined for L. monocytogenes the next day andcontaminated smoked salmon and illness were not after 1 week of storage in sealed plastic bags at 48C.further investigated, as the study was done some The study included five smoking conditions, withtime after the disease outbreak. temperatures ranging from 19 to 228C and exposure

Particular clones of L. monocytogenes do not seem times from 3 to 10 h. Of 200 samples taken beforeto be adapted to smoked salmon. A range of clones smoking, 108 (54%) were L. monocytogenes posi-have been found in the smoked salmon industry, and tive, the corresponding figure for 200 samples takensome of them are also found in samples from other after smoking was 19 (9.5%). Eleven pre-smokingsources. Some subclones are isolated both from samples contained 10–300 cfu /g, while all post-smoked salmon and patients. Smoked salmon may smoking samples contained , 10 cfu /g.therefore be a possible source for human listeriosis. The results showed that cold-smoking has an

effect on L. monocytogenes. L. monocytogenes wasfound in two post-smoking samples after 1 week of

5. Effect of the smoking process on L. storage. This indicates that L. monocytogenes, dam-monocytogenes aged during the smoking process, may recover

during storage.The temperatures used in cold-smoking are too Hot-smoking is performed at temperature and time

low to eliminate L. monocytogenes; Guyer and combinations expected to be bactericidal for L.Jemmi (1991) showing that cold-smoking had no monocytogenes. This was confirmed in a study byeffect on the bacteria. Salmon fillets were inoculated Jemmi and Keusch (1992); L. monocytogenes waswith from 23 to 23,000 cfu /g, and salted in a eliminated after smoking to a core temperature ofmarinade of 6% NaCl for 24 h, before smoking for 658C for 20 min, and was not found during storage


Table 1Occurrence of Listeria monocytogenes (L.m.) before and after smoking in naturally-contaminated salmon fillets under different smokingconditions, in four smokehouses (A–D). The results are based on two trials, in smokehouse C with different smoking conditions (Aase andRørvik, 1997)

Processing Time Temperature No. of L.m. pos. L.m. pos.aplant (h) (8C) samples before smoking after smoking

A 3 20 25 6 0B 10 19 65 52 6C 4 20 30 24 9C 7 20 30 21 4D 6 22 50 5 0

a Equal numbers of samples before and after smoking.

for 20 days. Recently, Poysky et al. (1997) found monocytogenes during processing. Hot-smokingthat if smoke was applied during the entire heating seems to eliminate L. monocytogenes when smoke isprocess, the lethal temperature for L. monocytogenes applied during the whole heating process. The pre-was 67.28C. The temperature was higher when vention of recontamination of both cold-smoked andsmoke was applied after drying the surface of the hot-smoked salmon is therefore of great importance.salmon fillets. Reduced growth ability of damaged L.monocytogenes after cold- or hot-smoking mayinfluence recovery, both in growth media and in the 6. Growth of L. monocytogenes in smokedproducts during storage. salmon

Challenge tests show that cold-smoking does noteliminate L. monocytogenes at temperatures between Several investigations have shown that growth of22.2 and 308C, but that it does so at temperatures L. monocytogenes in experimentally contaminatedfrom 17.1 to 21.18C. L. monocytogenes injected with smoked salmon (or trout) may occur during storagecontaminated brine can grow during the smoking at refrigeration temperatures, even with low inocu-process. Under natural cold-smoking conditions, the lum doses (Table 2). The levels of L. monocytogenesfrequency and level of L. monocytogenes seem to were considerably higher at 8–108C than at 48C afterdecrease, and smoking may thus help to reduce L. 20 days of storage (Guyer and Jemmi, 1991; Jemmi

Table 2Growth of Listeria monocytogenes (L.m.) in experimentally cold-smoked salmon and hot-smoked trout during storage

Reference Product Strains Inoculum Storage Storage Increase (log )10

(cfu (L.m.) /g) temperature time in number(8C) (days) of (L.m.)

Farber (1991) Cold-smoked salmon Scott A ca. 100 4 15 2.4Shrimp isolate ca. 100 4 15 2.0

Guyer and Jemmi (1991) Cold-smoked salmon SLCC 2755 23 4/10 30 0SLCC 2755 23,000 4/10 30 2.5Salmon isolate 650 4/10 30 4.5

Rørvik et al. (1991) Cold-smoked salmon NCTC 7973 1 2 salm. isol. 6 4 28 4.8NCTC 7973 1 2 salm. isol. 600 4 28 3.7

Jemmi and Keusch (1992) Hot-smoked trout Trout isolate 450 4 20 0Trout isolate 450 8–10 20 7SLCC 2755 310 4 20 0SLCC 2755 310 8–10 20 7.4

Rosso et al. (1996) Cold-smoked salmon ATCC 19115 10,000 4 21 0.2ATCC 19115 16,000 8 21 3.7


and Keusch, 1992; Rosso et al., 1996). Niedziela et 7. Preservatives to inhibit growth of L.al. (1998), however, concluded that traditional cold- monocytogenes during storagesmoking had a bacteriostatic effect on L. monocyto-genes, and thus slowed down growth during storage. The use of preservatives to prevent growth of L.

The levels of L. monocytogenes found in smoked monocytogenes in smoked salmon is a possibility.salmon are usually low, regardless of storing time. While preservatives are allowed in smoked salmon inJørgensen and Huss (1998) examined the occurrence some countries, the general desire is for naturaland levels of L. monocytogenes in naturally-contami- foods without additives. Some work has been donenated smoked salmon after production and after on the preservative effect of certain bacteriocins instorage. They found higher prevalence after storage smoked salmon. Nisin and ALTAE combined withand also moderate growth of the bacteria. The fact CO atmosphere packaging or vacuum packaging2

that multiplication of L. monocytogenes occurs to a have been shown to be effective in controlling L.lesser extent in naturally than in experimentally monocytogenes in smoked salmon (Nilsson et al.,contaminated smoked salmon was supported by 1997; Szabo and Cahill, 1999). Duffes et al. (1999)Cortesi et al. (1997) and Guyer and Jemmi (1990). reported that strains of bacteriocin-producing Car-Blomsø (1992) examined smoked salmon from nobacterium spp. inhibited L. monocytogenes in aseveral processing plants after packaging and at the cold-smoked salmon system within a storage time ofend of storage. In plants where samples contained less than 21 days., 100 cfu /g after processing, only , 100 cfu /g The use of preservatives in smoked salmon iswere found at the end, whereas in a plant where undesirable. Work is needed on the sensory quality300–400 cfu /g were detected in samples after and safety of these additives, including the possi-processing, up to 22,500 cfu /g were found after 3 bility for the development of resistance, before theirweeks of storage. use can be recommended.

Dalgaard and Jorgensen (1998) showed that L.monocytogenes grew more slowly in naturally-con-taminated smoked salmon than in challenge tests, 8. Contamination routes for L. monocytogenesand slower than estimated by predictive modelling. to the smoked salmonThe differences in the growth potential of L. mono-cytogenes in naturally and experimentally contami- If contamination of smoked salmon with L. mono-nated smoked salmon may be due to differences in cytogenes is to be prevented, it is essential thatgrowth ability between strains which may be injured contamination routes for the bacteria be elucidated.after the brining and smoking procedures, and strains Eklund et al. (1995) concluded that the surface of thegrown in broth. Growth to high levels in naturally- raw salmon was the main source of the bacteria.contaminated smoked salmon may be caused by After testing samples from three smokehouses,recontamination after smoking by undamaged cells. Guyer and Jemmi (1990) reported that raw salmonThis possibility underlines the importance of avoid- before filleting was frequently contaminated with L.ing post-smoking recontamination, and thus provides monocytogenes, but that the incidence decreasedthe rationale for rigid separation of the processing during processing. However, no typing beyondfacilities. serotyping was done in these studies to compare

L. monocytogenes can multiply considerably in isolates from samples taken at various stages ofsmoked salmon during storage. Growth is faster in production. In a study of a smokehouse (Rørvik etchallenge tests than in naturally-contaminated al., 1995), one ET was found to colonize thesmoked salmon and it is faster at 8–108C than at processing facilities over time, and was the only48C. The actual shelf-life under refrigeration should clone found in the vacuum-packed smoked salmon.be shorter than that customarily stipulated by many Other ETs were sporadically found in the processingproducers and the importance of preventing tempera- environment or in the raw fresh or thawed salmon.ture abuse must be emphasized. Freezing would of Recently, Autio et al. (1999) found that somecourse prevent growth, but is probably less accept- pulsotypes of L. monocytogenes predominated in aable to the consumer. plant, while other pulsotypes were found sporadical-


ly. They also observed that the most critical point in tion. Measures taken to eliminate L. monocytogenesthe process was the brining step, recirculated brine from the processing environment and the smokedsolution being mechanically injected into the fish. salmon would lead to a better hygienic quality inBoth of these studies concluded that raw fish was not general. Good production practices should be intro-a major source of contamination, and that smoked duced, with the application of HACCP programmes.salmon is contaminated with L. monocytogenes Processing facilities, production lines and equip-during processing. Autio also concluded that air- ment should be designed to facilitate good workingborne contamination with L. monocytogenes was routines, and to ensure an effective sanitation pro-probably of little significance. cess. Processing equipment such as brine injection

Slaughtered salmon from particular slaughter- machines, skin removers, or slicers, are often com-houses may be frequently contaminated with L. plicated constructions which are difficult to clean andmonocytogenes (Rørvik, unpublished data). As in disinfect. Conveyer belts are usually made of materi-smoked salmon processing plants, some slaughter- als which support the adhesion of L. monocytogenes,houses may be colonized by L. monocytogenes, and may be critical points as a reservoir for thewhile others are free of the bacteria. Raw material bacteria. In a study of risk factors for L. monocyto-from particular producers may be heavily contami- genes in smoked salmon production, well-maintainednated, and thus introduce L. monocytogenes into the facilities had a hazard ratio of 0.31 (P 5 0.064)smokehouse facilities. It is therefore important to compared to less-well or badly maintained facilitiesavoid L. monocytogenes contamination of slaughter- (Rørvik et al., 1997). As L. monocytogenes willhouses and slaughtered salmon. probably attach more easily to worn surfaces, it is

Other ways in which L. monocytogenes may be important to avoid such surfaces in the productionintroduced into smokehouses have not been deter- line.mined, but the bacteria are ubiquitous and probably Access to the processing facilities should beenter the processing plants via various routes. The strictly controlled, and the facilities should be sepa-bacteria have been found on transport vehicles rated into zones. Processing after smoking should beentering the processing environment (Rørvik, un- done in specially restricted areas, in order to avoidpublished data). Other possible vectors may be recontamination after smoking. Transport of rawequipment, packing materials etc. People may also materials, product etc. should be performed withbe carriers (Schuchat et al., 1991). different vehicles outside and within the production

The ways in which L. monocytogenes may be areas. Personnel should have different clothing,introduced into the smoked salmon processing plants footwear and equipment according to the area theyare probably numerous, L. monocytogenes being an work in, and the wardrobes should be separate. Theubiquitous bacteria, which may also be carried by risk study (Rørvik et al., 1997) showed that jobman. Raw salmon does not seem to be an important rotation was the strongest expressed risk factor in thesource, although slaughtered fish from colonized smokehouses, with a hazard ratio of 11 (P 5 0.002).slaughterhouses may introduce the bacteria into a If job rotation has to be employed, strong precau-plant. Whatever the initial source of L. monocyto- tions must be taken to reduce the associated risk.genes might be in each case, the main issue for the Colonization of the processing environment by L.producer is to avoid colonization of the processing monocytogenes must be prevented. Good cleaningenvironment and spread to the product. and disinfection routines, with detailed programmes

for the sanitation of the processing environment ingeneral and the production line in particular, must

9. Prevention of colonization in the processing therefore be implemented, with special emphasis onenvironment by L. monocytogenes and spread to surfaces in contact with the product. Routines shouldthe products include frequent changing of equipment and gloves

and careful cleaning of the production line during theThe potential for improvement of processing day. Room temperature should be kept low in the

hygiene in the fish industry seems to be considerable, processing areas, and final product should be re-the production of smoked salmon being no excep- moved for storage as quickly as possible.


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listeria monocytogenes in the smoked salmon industry

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