Journal of Infection (I984) 9, 43-5 ° 43

A p r o f i l e o f s k i n s e p s i s in m e a t h a n d l e r s

M. B a r n h a m and J. Kerby

Department of Microbiology, Harrogate General Hospital, Harrogate, North Yorkshire HGz 7ND

Accepted for publication 5 January I984

Summary Four hundred and sixty-seven episodes of sepsis associated with meat handling and poultry processing occupations were seen in two Health Districts of North Yorkshire in a period of just over five years. Altogether 389 patients were infected in 16 outbreaks and 24 sporadic incidents; spread of infection was noted in families of nine workers. The variety of skin infections included septic cuts and scratches, paronychia, abscess, lymphangitis as well as infection in pierced ear lobes and in tattoos. Beta-haemolytic streptococci or Staphylococcus aureus were present in 96 per cent of the 303 episodes that yielded positive cultures. These included 2o3 episodes with Streptococcus pyogenes and I7O with S. aureus. Skin sepsis appears to be common among meat handlers in this part of England.

Introduction

In recent years streptococcal and staphylococcal skin sepsis have become increasingly recognised as an occupational hazard of meat handlers. 1 Reports to the Public Heal th Labora tory Service Communicable Disease Surveillance Centre f rom a few laboratories where there is particular interest in the subject may give the impression that outbreaks of such infections in these workers are uncommon but the true incidence may have been underest imated. 2 A study in Oxfordshire revealed a problem on a wider scale. Relationships between infection in abattoirs and retail butchers was found, and there was possible fur ther involvement of the families of meat workers, restaurateurs and housewives. 3

Our interest in this matter developed in I978 when an outbreak of sepsis arose in a local chicken processing factory. 4 Since then we have been on the alert for fur ther outbreaks and sporadic infections in meat workers. In this report we summarise our experiences to date.

Methods

Infections in meat handlers became known to us f rom details given on routine microbiology request forms. Fur thermore , regular reminders were sent to general practitioners and to doctors in hospital Accident and Emergency depar tments in order to encourage reporting and bacteriological investigation of infection in such patients. Whenever a case was recognised, enquiry was made into the health of colleagues at work. This often led to the discovery of outbreaks of infection. Other suspected outbreaks were reported directly to us by doctors and environmental health officers as our interest in the subject became known.

oi63-4453/84/o4oo43 + I O $02.00/0 © I984 The British Society for the Study of Infection

44 M. BARNHAM AND J. KERBY

T a b l e I Outbreaks and sporadic infections recognised during the study

Number of

Infected Episodes of Outbreaks persons infection

Total work (Percentage force affected)

Chicken slaughter/ 5 277 353 341-425 (24,9,I3,I6,I2) processing factory

Turkey slaughter/ I 5 5 24 (2I) processing factory

Pig slaughter/ I i6 16 i2o (13) processing factory I

Pig slaughter/ i IO IO 248 (4) processing factory I I

Abattoir A 2 22 22 2I (52,52) Abattoir B 1 5 5 12 (42) Abattoir C 1 3 3 8 (38) Abattoir D 1 5 5 7 (71) Abattoir E I 3 3 4o (8) Abattoir F/ I 2 2 5 (4o)

Butcher complex Abattoir G / I 6 7 8 (75)

Butcher complex Families of workers 12 I2 Sporadic infections 23 24

Totals I6 389 467

S w a b s f r o m pa t i en t s w e r e s t r eaked on p la tes o f n o n - s e l e c t i v e h o r s e - b l o o d agar w h i c h were t h e n i n c u b a t e d ae rob ica l ly a n d anae rob i ca l l y o v e r n i g h t at 37 °C. S t r a ins o f Staphyloccus aureus i so la ted in p u r e cu l t u r e w e r e ident i f ied b y the coagu lase r eac t i on a n d w e r e p h a g e - t y p e d a t the L e e d s P u b l i c H e a l t h

L a b o r a t o r y . T h e Lance f i e ld g r o u p o f b e t a - h a e m o l y t i c s t r e p t o c o c c i i so la ted was d e t e r m i n e d in o u r l a b o r a t o r y b y m e a n s o f the P h a d e b a c t S t r e p t o c o c c u s T e s t ( P h a r m a c i a D i a g n o s t i c s ) o r b y S t r e p t e x ( W e l l c o m e R e a g e n t s L t d ) . T h e s e s t ra ins w e r e r e f e r r e d to the D i v i s i o n o f H o s p i t a l I n f e c t i o n , C e n t r a l P u b l i c H e a l t h L a b o r a t o r y , Co l inda l e for f u r t h e r g r o u p i n g a n d t yp ing . A n t i b i o t i c suscep t ib i l i t y p a t t e r n s we re r evea led b y use o f disc d i f fus ion tests .

I n th is r e p o r t , in fec t ions w h i c h cou ld n o t be r e l a t ed to those in any o t h e r p e r s o n are t e r m e d sporad ic . I n f e c t i o n in two or m o r e p e r s o n s w i t h a s u s p e c t e d ep idemio log i ca l l ink is t e r m e d an o u t b r e a k . A p p a r e n t r e c r u d e s c e n c e o f in fec t ion or r e in f ec t i on t o days or m o r e a f t e r an ear l ier a t t ack is c o u n t e d as a f u r t h e r ep i sode . N o n - p y o g e n i c in fec t ions s u c h as c o m m o n war t s , o r f a n d e rys ipe lo id , a re no t i n c l u d e d . Resu l t s o f inves t iga t ions in the H a r r o g a t e a n d N o r t h a l l e r t o n H e a l t h D i s t r i c t s ( p o p u l a t i o n c. 2 4 o o o o ) a re g iven f r o m m i d I978 to t he e n d o f O c t o b e r I983 , a p e r i o d o f jus t ove r five years .

Skin sepsis in meat handlers 45

Chicken factory, outbreak I

2

4

5

Turkey factory

Pork factory I

Pork factory Fr

Abattoir A,

d F M A

Abattoir B

Abattoir C

Abattoir D

Abattoir E

outbreak I

2

A

Month

M J J

I

A S 0 N D

_ , , d m ~

A

Abattoir F/Butchers , ~

Abattoir G/Butchers

SPORADIC infections I 2 I 2 I I 4 8 I

J F M A M J J A S 0 N

Fig. I. Seasonal distribution of outbreaks and sporadic infection.

Results

Dur ing the period of the study, 467 episodes of infection were detected. These involved 389 people in I6 outbreaks as well as 24 sporadic incidents as shown in Table I. Infection spread to i2 contacts in the families of nine meat handlers.

There were five large outbreaks in a chicken slaughter and processing factory which was closely observed and investigated during the study. Three-quarters of the episodes were related to outbreaks at this factory. In the largest outbreak there were IO8 episodes of infection. A sixth outbreak in poultry handlers was seen in a small factory concerned with slaughtering and processing turkeys. T e n outbreaks were in red meat handlers and often affected 4o -70 per cent of the work force of the establishments concerned. Abattoirs, related retail butchers and pig slaughtering and processing factories were affected also. Outbreaks were evident at all t imes of the year but were most commonly seen in the autumn, as shown in Fig. I. The duration of outbreaks was often three to six weeks but at the chicken factory they were more prolonged. Full details have been given elsewhere of outbreaks at abattoir A and pork factory 15 and of the first three outbreaks at the chicken factory. 6

Sporadic infections arose among retail butchers (Io episodes), abattoir workers (four episodes), meat inspectors in two abattoirs and a chicken processing factory (three episodes), workers in a turkey slaughter and processing factory (three episodes), chefs (two episodes), one restaurateur and a man who delivered rusks and seasonings to many meat processors. Two- th irds of these sporadic infections were in the last four months of the year.

46 M. B A R N H A M A N D J. K E R B Y

~-beta streptococci (total 225)

.S.. ou reus ( 170 )

/Other possible pathogens in substantial growth (20)

l 4~ ~.-No significant growth

Fig. 2. Bacteriological findings in 349 episodes of infection: scheme to show purity and mixture of cultures.

Clinical nature o f the infect ions

Cuts and scratches on the hands and arms commonly became infected giving rise to the typical features of erythema, induration and delay in wound healing. Various manifestations in the workers included crusted impetiginous or ecthymatous lesions, pustular rashes, infected eczema and chronic folliculitis. Acute paronychia was seen in Io patients, usually as a result of damage to the nail. In addition infection appeared as an early complication of ear-piercing in five workers and of tattooing in three. The presence of skin-infecting types of Streptococcus pyogenes in the throat was usually asymptomatic, but sore throat was noted in eight patients, Frank abscess was seen only twice but ascending lymphangitis with axillary lymphadenitis, malaise and fever affected eight patients. One family contact with carcinomatosis developed non-fatal streptococcal septicaemia with signs of lower respiratory tract infection. Examples of the various skin infections in meat handlers are shown in the Plates.

Bacteriological findings

In the course of investigating 349 episodes bacteriologically 303 (87 per cent) yielded bacteria that were considered significant. Organisms isolated in pure and mixed cultures are indicated in Fig. 2. Beta-haemolytic streptococci or S. aureus were found in 29I (96 per cent) of those bacteriologically positive. Other likely pathogens were isolated in heavy growth from 2o episodes but as the sole finding in only 12; they included Escherichia coli (I3 episodes), Pseudomonas sp. (five episodes), Proteus sp. (three episodes) and Clostridium perfringens (three episodes). Most of the 46 infections yielding insignificant growth were tested during or after the administration of antibiotics or when the wounds were already healing.

Three-quarters of the episodes with positive bacteriological findings yielded beta-haemolytic streptococci, including group A streptococci in 2o3, group B in two, group C in one, group E in one, group G in six, group L in I I and a haemolytic strain S. milleri that did not appear to belong to any detectable Lancefield group in one. Group E and A streptococci were found together in

Journal of Infection Pla tes I a n d 2

Plate I. S. pyogenes M-type 80 skin infections in poultry processors: (a) infected pierced ear-lobe] (b) infection in antecubital fossa (non-typable S. aureus also present).

Plate 2. Skin infections with S. pyogenes M-type 8o and S. aureus phage type 85 in poultry processors: (a) multiple infected lacerations on the hands; (b) infected tattoo on the arm.

BARNI-IAM AND KERBY (Facing p. 46)

Table I I

Skin sepsis in meat handlers

Typing patterns of S. pyogenes isolated from meat-associated infections

47

N o . o f

N o . o f N o . o f spo rad i c T p a t t e r n M - t y p e isolates o u t b r e a k s infec t ions

3 / I 3 / B 3 2 6 4 33 8 I 2 3 / I 3 / B 3 2 6 4 41 36 i - -

I4 49 9 2 2 i2 66 I - - I

19 74 I I - - *4 8o 73 i 4

3 / I 3 / B 3 2 6 4 8I 73 4 I 3 / I 3 / B 3 2 6 4 * 8 I I 3 / I 3 / B 3 2 6 4 t I - - I

5 / 2 7 / 4 4 * 5 I - -

8/25/Im p 19 * I I I - - 8/25/Imp 19 t 2 I I

* Opac i t y fac tor ( O F ) nega t ive ; t O F posi t ive , a n t i - O F negat ive .

the infected wound of an abattoir worker who handled cattle, sheep and pigs. G r o u p L streptococci were isolated f rom infected wounds on the hand and f rom two patients with paronychia among six workers f rom the two pork factories and among five f rom the chicken factory. Six strains were in pure growth and five were mixed with S. aureus. T y p i n g of zz8 isolates of S. pyogenes (Table I I) showed 12 distinct pat terns; all were of the higher n u m b e r M- t ypes or were M - u n t y p a b l e and six types were encountered in more than one incident. In any single outbreak, streptococci were usually of a single type; recurrent outbreaks were usually caused by different types. Tetracycl ine resistance was seen in 64 per cent of the 2I x isolates of S. pyogenes tested bu t e ry thromycin resistance was not found.

Staphylococcus aureus was the sole pa thogen in 66 infections and was present in 46 per cent of the episodes yielding beta-haemolyt ic streptococci. Phage- typing of I I I strains of S. aureus isolated f rom wounds in nine outbreaks and from three sporadic infections revealed seven of group I (6 per cent), 3 of group II (2"5 per cent), 55 of group I I I (5o per cent), I3 miscellaneous (I I '5 per cent) and 33 untypable (3o per cent). Fif ty strains isolated f rom seven outbreaks and f rom one sporadic infection were of phage type 85 or 53/85. Phage type 94/96 was seen in five outbreaks. These phage types came f rom bo th poul t ry and red meat handlers ; together they accounted for 54 per cent of the total strains isolated. Antibiot ic resistance of strains was as follows: penicillin (77 per cent), tetracycline (9 per cent), c l indamycin (3 per cent), e ry thromycin (I .7 per cent) and fusidic acid (o.6 per cent).

Respiratory tract carriage

In the chicken factory outbreaks, throat carriage of S. pyogenes was found in 25 per cent and nasal carriage in 6 per cent of workers with skin infection, bu t only be tween I and 2 per cent of healthy workers were carriers of the epidemic

48 M. B A R N H A M A N D J. K E R B Y

strains. In the course of five years 12 workers were found to carry non-epidemic serotypes of S. pyogenes in the throat. P re -employmen t screening of 5o0 new workers at the factory showed io (~ per cent) throat carriers of S. pyogenes. Following the use of antibiotics aimed at abolishing the organisms, cross- infection was not seen with these strains. Nasal carriage of S. aureus was assessed in only two outbreaks. In the chicken factory 8 per cent of healthy workers carried organisms of the epidemic phage types. The re was an overall S. aureus carriage rate of ~o per cent bu t in abattoir A 5o per cent o f persons were S. aureus carriers al though none harboured the epidemic types.

D i s c u s s i o n

Labora to ry workers wi thout an active approach to infection in meat handlers would recognise only a few incidents as such persons do not complain and doctors often treat them without taking specimens. T he n u m b e r of infections repor ted here is almost certainly an underes t imate of those actually in the district. W e heard anecdotal accounts of outbreaks said to have taken place early on in the s tudy in several abattoirs and processing factories bu t these could not be confirmed and have not been included. I t was not possible to apply certain special measures that others have found helpful in case finding, such as fur ther quest ioning about w o u n d swabs f rom all out-pat ients and the typing of all streptococci isolated in the laboratory, 3,7 Infect ion on the scale we have seen is p robab ly typical of what is to be found elsewhere in England as N o r t h Yorkshire does not have any greater n u m b e r of meat- and poul t ry-handl ing establ ishments than many other parts of the country.

The series of large outbreaks at the chicken factory accounted for three- quarters of the episodes of infection which we encountered. Infect ion at this factory was the first to be repor ted in poul t ry processors, 4 bu t such infections have now been recognised in at least two other parts of England ( P H L S Working Party on Streptococcal Infect ion in Mea t Handlers , personal com- munication). Skin sepsis in turkey processors, however appears not to have been repor ted until now. The prob lem of infection in poul t ry processors seems to be similar to that in red meat handlers.

Infect ion was seen most often in the cuts and scratches caused in meat handlers by sharp bone and knives. 5,s Reduc ing the risk of injury, perhaps by more mechanisat ion or by iml~l;~ements in protect ive clothing, might help to reduce the problem. Skin lnfe" "~ction in the handlers was often mild and prolonged; only a minori ty suffered more serious disease such as abscess formation or lymphangitis. We did not meet with any post-s t reptococcal nephrit is or rheumatic fever. Sore throat is u n c o m m o n in outbreaks of streptococcal infection in meat handlers 1 and was a feature in only one of the outbreaks.

T h e autumnal predominance of outbreaks and sporadic infections in the workers may reflect the seasonal increase in slaughter and meat handling. 2 In poul t ry processing plants there is little seasonal variation in workload and our outbreaks there may have been influenced by the regular spring and au tumn influx of new employees as we have seen a disproport ionate amount of infection in this group, e

Skin sepsis in meat handlers 49

We have been unable to define the routes by which strains of S. pyogenes causing outbreaks are introduced, but human beings rather than animals are almost certainly the source. 2 In one report, an outbreak of streptococcal infection in an abattoir followed the employment of a man with an infected ear. x° One-quarter of the new employees at the chicken factory had had previous experience of meat handling and it was thought that they might have brought with them strains endemic in other establishments. Respiratory carriers detected by the pre-employment screening examination were treated; subsequent outbreaks caused by the serotypes detected did not arise. The finding of workers with early infection complicating ear-piercing or tattooing suggested that these procedures might be a means by which new strains might be introduced. Pyogenic infection is a rare complication of professional tattooingfl but we saw infection after workers had been to non-professional artists, untrained in basic hygiene. Infection within the families of workers may later lead to the re-introduction of strains to the workplace by reinfection of the worker or spread to other establishments by involvement of other meat workers in the household.

Serotypes of S. pyogenes isolated from skin infections in meat handlers have mostly been of the higher number M-types but, although there is not any particular type that appears to be confined to infection in meat handlers, some types are rarely found elsewhere. 2 Our findings show that even on a local scale several different serotypes are seen to cause sepsis in meat handlers. Our most common M-types, 49, 80 and 8I, have also been commonly found in meat handlers elsewhere in England. Recurrent outbreaks may be caused by single serotype endemic within an establishment 2 but the recurrences we saw were usually caused by different serotypes. The significance of group E streptococci in the wound of an abattoir worker is unclear; these organisms can cause cervical abscess, pneumonia and septicaemia in the pig. 11 We found group L streptococci in the obviously infected wounds of r r workers, and similar infections have recently been noted elsewhere in butchers, abattoir workers and a pig farmer (Communicable Disease Surveillance Centre, unpublished). In view of their being commonly present in the environment of chicken and pork processing factories 5,6 the potential of these streptococci to produce wound infection in human beings appears to be low.

Staphylococus aureus has been considered a less important cause of sepsis that S. pyogenes in meat handlers 2 but in some obviously infected wounds it is the sole finding. This organism is more commonly carried in the respiratory tract of workers than is S. pyogenes, and some sepsis may result from auto-infection. Bacteriophage typing patterns of strains isolated in our series showed a high proportion of non-typable strains as well as commonly occurring strains with the patterns 85 and 53/85. Others have noted infection with these types in meat handlers 3 but it is unclear whether there is some special association with meat or whether they originate from the animals.

In the management of outbreaks we aimed for rapid recognition of infection and treatment of patients on clinical suspicion once swabs had been taken. Patients with more serious infection sometimes required exclusion from work, but we did not recommend it as a routine. Standard treatment with oral flucloxacillin, or with penicillin or erythromycin for infection with organisms

5 ° M. B A R N H A M A N D J. K E R B Y

k n o w n to be su scep t i b l e r e s u l t ed in r a p i d r e s p o n s e s , a n d t h e r e a p p e a r e d to be a low inc idence o f t r e a t m e n t fa i lure . R e s i s t a n c e to t e t r acyc l i ne m a d e this an u n s u i t a b l e d r u g for t r e a t m e n t . F u r t h e r ep i sodes o f i n fec t ion in s o m e w o r k e r s a rose a f t e r a m e d i a n in te rva l o f 26 days a n d w e r e o f t en caused b y d i f f e ren t o r g a n i s m s . s t ra ins is n o t c lear , a n d we h a v e f o u n d few h e a l t h y s t r e p t o c o c c a l ca r r i e r s in the o u t b r e a k s . S c r e e n i n g o f s ta f f fo r r e s p i r a t o r y ca r r i age in la rge e s t a b l i s h m e n t s is e x p e n s i v e , t i m e c o n s u m i n g a n d p r o b a b l y n o t w o r t h w h i l e . Su rve i l l ance b y h a n d i n s p e c t i o n w h e n a n i n f ec t ed i ndex case has b e e n d i s c o v e r e d in an e s t a b l i s h m e n t o f t en revea ls o t h e r w o r k e r s w i t h i n f ec t i on ; such i n s p e c t i o n m a y n e e d to b e r e p e a t e d w h e n an o u t b r e a k pe r s i s t s de sp i t e t he t r e a t m e n t o f k n o w n infec t ions . T h e va lue o f r o u t i n e h a n d su rve i l l ance is less c lear , b u t th is m i g h t b e bes t a p p l i e d in t he a u t u m n in e s t a b l i s h m e n t s w h e r e t h e r e h a v e b e e n r e c u r r e n t o u t b r e a k s .

(We thank the staff of the Leeds Public Heal th Labora tory and the Division of Hospital Infection, Central Public Heal th Laboratory, Colindale for typing the organisms, as well as medical, environmental health and laboratory colleagues for their kind co-operation.)

R e f e r e n c e s

r. Fraser CAM, Ball LC, Maxted WR, Parker MT. Streptococcal skin sepsis among meat handlers. In Parker MT, ed. Pathogenic Streptococci. Chertsey: Reedbooks, r979: r x5-i x6.

2. Public Health Laboratory Service Working Group on Streptococcal Infection in Meat Handlers. The epidemiology and control of streptococcal sepsis in meat handlers. Environ Health I982; IO: 256-258.

3. Slack MPE, Saunders FC, Mayon-White RT. Streptococcal skin infections in meat workers in Oxfordshire. In Holm SE, Christensen P, eds. Basic concepts of streptococci and streptococcal diseases. Chertsey: Reedbooks, I982:28-29.

4. Barnham M, Kerby J, Skillin J. An outbreak of streptococcal infection in a chicken factory. ff Hyg (Camb) I98o; 84: 71-75.

5. Barnham M, Kerby J. Skin sepsis in meat handlers: observations on the causes of injury with special reference to bone. J Hyg (Camb) I98I ; 87: 465-476.

6. Barnham M, Kerby J, Skillin J. Streptococcal skin sepsis in chicken factory workers. In Holm SE, Christensen P, eds. Basic concepts of streptococci and streptococcal diseases. Chertsey: Reedbooks, I982: 26-27.

7. Mayon-White RT, Perks EM. Why type streptococci? The epidemiology of group A streptococci in Oxfordshire I976-I980. ff Hyg (Camb) 1982; 88:439--452.

8. Working Group on Streptococcal Infection in Meat Handlers. A survey of streptococcal skin sepsis among meat handlers and other workers. In Parker MT, ed. Pathogenic Streptococci. Chertsey: Reedbooks, x 979: I x 7-I 18.

9. Scutt RWB. The medical hazards of tattooing. Br ff Hosp Med I972; 8: I94-2o2. to. Tsai TF, Watson WN, Hayes PS, Facklam R_R, Fraser DW. Mode of spread of group A

streptococci in an abattoir outbreak of wound sepsis. In Parker MT, ed. Pathogenic Streptococci. Chertsey: Reedbooks, I979: I 18-I 19-

1 I. Parker MT. Streptococcus and Lactobacillus. In: Wilson GS, Miles AA, Parker MT, eds. Topley and Wilson's principles of bacteriology, virology and immunity. London: Edward Arnold, x983 : 2: I73-2x7.