International Journal of Food Microbiology, 12 (1991) 53-66 © 1991 Elsevier Science Publishers B.V. 0168-1605/91/$03.50

53

FOOD 00364

Yersinia enterocolitica in food hygiene Georg Kapperud Department of Bacteriology, National Institute of Public Health. Oslo, Norway (Received 7 August 1990; accepted 11 September 1990)

Yersinia enterocolitica and Yersinia enterocolitica-like bacteria constitute a fairly heterogenous group of bacteria which includes both well-established pathogens and a range of environmental strains which are ubiquitous in terrestrial and freshwater ecosystems. Pathogenic significance in man is mainly associated with a few serogroups (0:3, 0:9, 0:8. 0:5.27). The pathogenic serogroups show different geographical distributions. The development of isolation procedures which clearly differentiate pathogenic from non-pathogenic variants has been difficult. Of special significance in food hygiene is the ability of Y. enterocolitica to grow in refrigerated foods. There is strong indirect evidence that pigs and food products of porcine origin are the major sources for human infection with Y. enterocolitica serogroups 0 : 3 and 0:9, the dominant human pathogens in most parts of the world. The reservoir(s) for serogroup 0:8, which prevails in the U.S.A., is uncertain. The pig is the only animal consumed by man which regularly harbours pathogenic Y. enterocolitica. Improved isolation methods and DNA colony hybridization using genetic probes has indicated that the prevalence of pathogenic Y. enterocolitica in pork products is substantially higher than previously suggested. Prevention and control measures should focus on information of people involved in food processing and preparation and on the improvement of hygiene during slaughtering of swine. Important critical control points at the stage of slaughter are: (i) circumanal incision and removal of intestines, (ii) excision of the tongue, pharynx, and particularly the tonsils, (iii) post-mortem meat inspection procedures which involve incision of the mandibular lymph nodes, and (iv) deboning of head meat. Key words: Yersinia enterocolitica; Food hygiene; Swine: Review

Introduction

Yersinia enterocofitica is considered to be a foodborne pathogen, even though attempts to isolate the bacterium from a suspected food source have seldom proved successful (Lee et al., 1981; Schiemann, 1989; WHO, 1987). In the past two decades there has been a substantial increase in the frequency of the isolation of this organism from both clinical and non-clinical sources. Y. enterocolitica has been isolated from humans in many countries of the world, but it seems to be found most frequently in cooler climates (WHO, 1983; WHO, 1987). Relatively little is known

Correspondence address: G. Kapperud, Department of Bacteriology, National Institute of Public Health, Geitmyrsveien 75, 0462 Oslo 4, Norway.

54 about the incidence in tropical countries. A clustering of cases during the fall and winter months has been reported in Europe. In developed countries. 1,'. enterocolitica can be isolated from 1-2% of all human cases of acute enteritis, however, when serological methods are also employed~, higher percentages of infection have been found.

Y. enterocolitica and Y. enterocolitica-like bacteria

Bacteria referred to as Y. enterocofitica and Y. enterocolitica-like organisms are quite heterogenous with respect to phenotypic, genotypic and ecological properties. This bacterial group encompasses acknowledged pathogens as well as a range of so-called environmental strains which are ubiquitous in terrestrial and freshwater ecosystems (Kapperud and Bergan, 1984; Mollaret et al., 1979). Strains previously termed 'Y. enterocolitica-like organisms' have now been classified as seven separate species: Y. frederikseniL Y. kristenseniL }I. intermedia, Y. aldovae, Y. rohdei, Y. mollaretii and Y. bercovieri (Aleksic et al., 1987; Bercovier et al., 1984; Brenner et al., 1980; Wauters et al., 1988b). N o n e of these species have been associated with human or animal disease, with the exception of a few atypical cases. All strains capable of causing disease (yersiniosis) belong to Y. enterocolitica sensu stricto. However, not all strains of this species are pathogenic (Mollaret et al., 1979). The phenotypic heterogeniety in Y. enterocolitica has prompted the development of several schemes for routine subdivision of the bacterium on the basis of serogroups, biovars, and phagevars (Kapperud and Bergan, 1984: Mollaret et al., 1979; Wauters et al., 1987). Y. enterocolitica has been classified into approx. 60 serogroups on the basis of O antigens (Wauters, 1981). However, the strains associated with disease in man or animals belong to only a few serogroups. Thus, 0:3, 0:5,27, 0:8, and 0 : 9 are the most important causative agents in man. Serogroup

1

Biovar

Location

Phagevar --~

Europe, Japan, other

3

4

VIII

3

4

IXa

South Africa

3

4

IXb

Canada

3

3

II

9

2

X3

8

lb

Xz

Japan

]

~

Europe

~

USA, Canada

Fig. 1. Interrelationships between serogroup, biovar, phagevar, and geographical distribution of the most common human pathogenic variants of Y. enterocolitica. Biovars are determined according to Wauters et al. (1987). Adapted from Mollaret et al. (1979).

55 Likewise, O:1 and O:2 have been associated with disease in chinchillas and hares, respectively. The serogroups commonly involyed in pathological processes in man or animals belong to distinct serogroup-biovai'~phagevar combinations (Mollaret et al., 1979; Fig. 1). The environmental strains, on the contrary, constitute a spectrum of phenotypic variants which display a variety of antigenic factors. As a group, these bacteria usually lack clinical significance and are ubiquitous. A correlation exists between geographic areas and the serogroups associated with disease in man (Mollaret et al., 1979; Fig. 1). The serogroups most frequently causing human yersiniosis in Europe are 0:3 followed by 0:9. Other serogroups have only exceptionally been encountered in pathological processes in this region. A high rate of 0:3 has also been reported from Japan. In the U.S.A., 0:3 and 0:9 have been sparsely represented. The most frequently isolated serogroups are 0:8 followed by 0:5,27. In Canada, 0:3 dominates in Ontario, Quebec, and the four eastern provinces, whereas in the western provinces the serogroups pattern parallels that observed in the U.S.A.

Differentiation between pathogens and non-pathogens Since the pathogenic significance of Y. enterocolitica is mainly associated with only a few serogroup-biovar combinations, differentiation between pathogens and non-pathogens has relied upon serogrouping and biotyping of the isolates. However, complete serological and biochemical classification lies outside the scope of most routine laboratories. Accordingly, a number of different in vitro and in vivo tests have been proposed for differentiation of pathogenic and non-pathogenic variants (Prpic et al., 1985; Robins-Browne et al., 1989; Schiemann, 1989; Wachsmuth et al., 1984). These tests include: autoagglutination at 37°C, calcium-dependent growth restriction at 37°C, resistance to the bactericidal activity of normal human serum, various animal and cell culture models, binding of Congo Red dye, use of DNA probes, and biochemical parameters. Many of these tests are based on properties associated with a 40-50-MDa plasmid which is a prerequisite, but not sufficient in itself, for virulence within the genus Yersinia (Cornelis et al., 1987; Portnoy and Martinez, 1985). However, the properties concerned are subject to problems of gene expression in vitro, and the sensitivity and specificity of several of the tests have been questioned (Prpic et al., 1985; Wachsmuth et al., 1984). Moreover, the possibility of the plasmid being lost during the course of a protracted isolation procedure cannot be excluded. Wauters et al. (1987) have put forward a revised biotyping scheme for Y. enterocolitica comprising a test for pyrazinamidase activity. This test is simple, reproducible, and shows a striking correlation between potential pathogenicity and lack of pyrazinamidase activity, independent of the occurrence of the virulence plasmid.

Clinical manifestations Y. enterocolitica is associated with a spectrum of clinical syndromes in man (Bottone, 1977; Cover and Aber, 1989; Mollaret et al., 1979). Gastroenteritis is by

56 far the most frequently encountered manifestation. Acute non-complicated enteritis is observed most often in children below 7 years of age. Occasionally, the infection is confined to the right iliac fossa in the form of acute terminal ileitis or acute mesenteric lymphadenitis, giving rise to.symptoms resembling appendicitis. Post-infection manifestations, including arthritis and erythema nodosum, occur mainly in adults, the latter most commonly in women. In Europe, there is a high incidence of both reactive arthritis and erythema nodosum. The causative agents belong to serogroups 0 : 3 or 0:9. These manifestations have been virtually absent in North America. This observation has been related to the geographical distribution of serogroups. Y. enterocolitica has been associated with a broad range of atypical clinical manifestations, mostly affecting immunocompromised patients (Bottone, 1977; Cover and Aber, 1989; Mollaret et al., 1979). Y. enterocolitica may cause focal infection in numerous extraintestinal sites. Yersinia strains similar to those isolated from environmental sources have been occasionally recovered from human clinical specimens. However, the clinical significance of environmental yersiniae have been convincingly established in only a few cases, mainly in patients with compromised host defence due to underlying illness or immunosuppressive therapy. The incubation period of Y. enterocolitica enterocolitis ranges from 1 to 11 days. The minimal infective dose for humans has not been determined (Cover and Aber, 1989).

Growth and survival in food Y. enterocolitica is able to multiply at temperatures approaching 0°C, a circumstance which means that it can grow in refrigerated foods. Several investigations have documented the growth of Y. enterocolitica on raw and cooked meat and in milk at low temperatures (Hanna et al., 1977; Lee et al., 1981). The bacterium is also able to multiply in vacuum packed meat during refrigerated storage (Hanna et al., 1976). As refrigeration is now being increasingly applied in preservation of perishable foods, the ability to propagate at 4°C is of considerable significance in food hygiene. Y. enterocolitica can survive in frozen foods for long periods (Schiemann, 1989). Some results indicate that the ability of Y. enterocolitica to compete with other psychrotrophic organisms normally present in foods may be poor (Schiemann, 1989; Stern et al., 1980). It has been suggested that D F D ( " D a r k Firm Dry") meat may favour the growth of Y. enterocolitica, not only because of the elevated pH level, but primarily due to the low sugar content, a factor which may result in reduced competition with the lactobacillary flora (Skjelkv~de, 1981). The heat resistance, salt tolerance, and pH tolerance of Y. enterocolitica is comparable to that of other Enterobacteriaceae (Lee et al., 1981).

57 Reservoir Y. enterocolitica and Y. enterocofitica-like bacteria are frequently encountered in terrestrial and freshwater ecosystems, and in animals, foods and water. However, the vast majority of the strains isolated from these sources are apathogenic variants (Mollaret et al., 1979). Although the bacteria have been isolated from nearly all of the vertebrate species examined, without any evidence of disease, the pig is the only animal consumed by man which regularly harbours pathogenic Y. enterocolitica (Hurvell, 1981; Kapperud and Bergan, 1984; Schiemann, 1989). Dogs, cats, and rats may occasionally be faecal carriers of 0:3 and 0:9. The relative intimate contact between man and pets suggests a potential reciprocal transmission, although such an epidemiological link has not yet been clearly confirmed. There is strong indirect evidence that swine constitute an important reservoir for human infection with Y. enterocolitica (Hurvell, 1981; Schiemann, 1989). Numerous surveys have shown that swine may be healthy carriers of 0:3 and O:9, belonging to the same biovars and phagevars as those engaged in human disease. In contrast, 0:8, the predominant human pathogen in the U.S.A., appears to be rare in swine. 0:8 may have entirely different reservoir(s) and ecology (Schiemann, 1989). In addition to their function as faecal commensals, 0:3 and 0:9 also inhabit the oral cavity of swine, especially the tongue and tonsils. The bacteria are also frequently encountered as a surface contaminant on freshly slaughtered pig carcasses. The prevalence of 0:9 among swine reflects the importance of this serogroup in human illness. High percentages of 0:9 have been reported from swine in the Netherlands, corresponding to the importance of this serogroup in human yersiniosis (Esseveld and Goudzwaard, 1973). In contrast, 0:9 has not been isolated from the buccal cavity of swine in Denmark or Norway, where human infections with this serogroup are rare (Christensen, 1987; Nesbakken and Kapperud, 1985). In Belgium, which is the country with the highest reported incidence of Y. enterocolitica infection, a case-control study has shown that the infection was strongly associated with eating raw pork (Tauxe et al., 1987). The apparent rarity of Y. enterocolitica infection in Moslem countries also supports the potential role of pork as a vehicle of Y. enterocolitica infection. It has not been possible to demonstrate any phenotypical or genotypical difference between human and porcine isolates. The finding that porcine and human isolates harbour virulence plasmids with identical restriction patterns, provides additional support for the role of swine in the epidemiology of human Y. enterocolitica infection (Nesbakken et al., 1987). Restriction analysis of chromosomal DNA has supported this suggestion (Andersen and Saunders, 1990; Kapperud et al., 1990a). In contrast to the frequent occurrence of the bacterium in swine and on freshly slaughtered carcasses, pathogenic Y. enterocolitica have only exceptionally been recovered from pork products at the stage of retail sale, with the exception of fresh tongues (Schiemann, 1989; WHO, 1987; Fig. 2). This phenomenon might be explained by the lack of proper selective methodology for the isolation of patho-

58 % OF ISOLATES SO-r

SO



PIG TONSILS (N = 206)

[]

PORKPROOUCTS (N = SO)

40

20

YE 0:3

YE

YK

YI

YF

Fig. 2. Isolation of Y. enterocolitica and related bacteria from pig tonsils (206 isolates) and pork products (60 isolates) in Norway. Key to the abbreviations: YE O:3. Y. enterocolitica serogroup O:3; YE, non-pathogenic Y. enterocolitica; YK. Y. kristensenii; YI, Y. intermedia; YF, Y. frederiksenii. The figure illustrates the inefficiency of conventional isolation procedures to detect pathogenic variants (YE 0:3) against a large background of environmental yersiniae (YE. YK, YI, and YF) present in pork--a problem which may be solved by the use of genetic probes (Fig. 3) or improved selective methodology. Adapted from Nesbakken and Kapperud (1985) and Nesbakken et al. (1985). genic strains. Recent studies have indicated that Y. enterocolitica is more common in pork products than previously documented (Wauters et al., 1988a; see below).

Detection in food and water

In foods, including both meat and milk products, and in water, one can expect to find a broad spectrum of bacteria belonging to several species within the genus Yersinia, and a number of serogroups within the species Y. enterocolitica (Mollaret et al., 1979). The vast majority of these have no medical importance whatsoever. The development of isolation procedures which clearly differentiate pathogenic from non-pathogenic variants has been difficult. The problem with all selective agar media described thus far is that they provide inadequate differentiation between pathogenic Y. enterocolitica and other microbes (WHO, 1987). These media allow the growth of a number of Yersinia variants to which no medical significance is currently attributed. These non-pathogenic variants are common in many foods, and their colony morphologies make them difficult to distinguish from the pathogenic types. It is important to bear in mind that such environmental yersiniae may conceal the presence of pathogenic variants, with underestimation of the latter as a likely consequence (WHO, 1987; Fig. 2). The different serogroups vary in their tolerance to selective components and other factors during the isolation process (Lee et al., 1981; Schiemann, 1989). Variations in tolerance even exist between the different pathogenic serogroups. As these serogroups show different geographical distributions (Fig. 1), a method which

59

A

¢i,

B

-

~o, "~ • ",h "o • 4m

-. ",ab''. O ,,,,i,*

oo-

j

.

°

B

"

Fig. 3. Autoradiograms of colony hybridization filters inoculated with minced pork experimentally contaminated with 103 (A) and 102 (B) cells of a virulent Y. enterocolitica 0:3 strain. The figure illustrates the ability of DNA hybridization assays to detect virulent Y. enterocolitica against a large background (3 × 104 cfu per filter) of indigenous bacteria. From Kapperud et al. (1990b). works well in one part of the world may not necessarily be applicable in other countries. A number of isolation methods are currently in use in different parts of the world, and there is a great need for a universally acceptable reference method. Most methods require time-consuming enrichments to achieve optimal isolation. Moreover, no method currently available allows optimal recovery of all pathogenic serogroups (Wauters et al., 1988a). Developments in gene technology now permit the production of genetic probes which enable rapid detection and enumeration of all pathogenic Y. e n t e r o c o l i t i c a serogroups. Using a synthetically produced oligonucleotide probe (Kapperud et al., 1990b) and an improved enrichment method, Nesbakken et al. (manuscript in preparation) found that the prevalence of pathogenic yersiniae in Norwegian pork products was substantially higher than previously demonstrated (Fig. 3).

Prevention

and control

Preventive and control measures should not be different, in general, from those which are intended to prevent and control zoonotic salmonellosis (WHO, 1987). They include three main lines of defence: (i) the pathogen-free breeding and rearing of slaughter animals; (ii) the improvement of hygiene during transportation, slaughtering, and processing, including different means of decontamination, and (iii) education of all categories of people involved in production, processing and final preparation of food products.

60 Strict hygiene is particularly necessary during food processing and preparation because Y. enterocolitica is able to propagate at temperatures approaching 0°C. Therefore, chilling of food products should not be considered as an effective control measure for this microbe. At the farm level, new-born piglets are easily colonized and become long-term intestinal and pharyngeal carriers without any signs of illness (Schiemann, 1989). This observation as well as the widespread occurrence of pathogenic Y. enterocolitica in herds of pigs indicate that the organism may be difficult to control efficiently at this stage (Andersen, 1984; Andersen, personal communication). Since swine are healthy carriers of Y. enterocolitica, its detection during the routine meat inspection is considered practically impossible. The visual inspection routines currently employed are inadequate to detect contamination with Y. enterocolitica.

During commercial slaughtering and processing, bacteria from the oral cavity or intestinal contents may easily contaminate the carcasses and the environment in the slaughterhouse. Although some contamination is unavoidable on a highly mechanized slaughterline, improved hygiene at critical control points (HACCP) should be attempted. Special attention should be paid during: (i) circumanal incision and removal of the intestines, (ii) excision of the tongue, pharynx, and particularly the tonsils, (iii) post mortem meat inspection procedures which involve incision of the mandibular lymph nodes, and (iv) deboning of head meat (Fig. 4). Contamination should be strictly avoided during these activities. Changes in slaughtering procedures, including technological improvements, may be required to achieve this. Some of the points mentioned above deserve further comments. In Norway and Denmark, the plucks (tongue, tonsils, trachea, oesophagus, lungs, heart, diaphragm, and liver) are removed as a whole and hooked up, allowing the possibility of the tongue and tonsils to contaminate the remaining organs. After removal of the tonsils, pieces of the surrounding pharyngeal tissue remain on the head. During the removal procedure the knife of the slaughterman is contaminated with Y. enterocolitica (Nesbakken, 1988). Excision of the tongue and tonsils as a separate operation, after removal of the remaining organs, has been found to significantly reduce contamination of the plucks (Danish Meat Research Institute, 1989). Another critical point on the slaughterline is the meat inspection (Nesbakken, 1988). Incision of the mandibular lymph nodes is compulsory according to the meat inspection procedures in most countries and thus represents a cross-contamination risk. After inspection, any remaining tonsillary tissue is removed in connection with dressing of the head. Y. enterocolitica may be transmitted from the tonsillary region to other parts of the carcass by the knives and hands of the personnel involved. Likewise, the knife of the slaughterman and the carcass may be contaminated during circumanal incision and removal of the intestines. Andersen (1988) found that faecal contamination was of major importance for the spread of Y. enterocolitica 0 : 3 to the carcass. He reported that the frequency of isolation from pig carcass surfaces varied greatly with the evisceration technique. Manual evisceration caused the greatest incidence of Y. enterocolitica 0 : 3 on the carcass surface, whereas the use of a bung cutter reduced the incidence markedly, particularly when

61 ~

Breeding & rearing

Other pigs



i

Transporting & holding [ Stunning & killing 1 Scalding & dehairing

I Singeing & polishing

I

~

[ Removal of intestines

e]

I Excision of tongue & tonsils

• 1

Evisceration

Meat InspecUon

~-

I Incison of Lnn. mandibulares

e ]

Cutting / debonlng t Chilling

~.~

[ Removal of head meat

e l

Food processing / preparation

.j

Fig. 4. Flow diagram for production and processing of pork products. Sites where major contamination with Y. enterocolitica 0:3 is expected to occur are indicated ( e ) . % CONTAMINATED 35 30

25 2O 15 10

RECTUM

MEDIALH/hIDUMB

SPLITSTERNUM

[ ] MANUALEVISCERATION(N = 419) [ ] BUNGClJHI::8(N = 526)

• BUNGCUTLER+ CLOSINGRECTUM(N = 315) FiB. 5. Isolation of Y. enterocolitica 0:3 from the rectum, medial hind limb. and split sternum of pig carcasses. Three different evisceration procedures are compared: manual (419 carcasses), use of bung cutter (526 carcasses), and bung cutter supplemented by enclosing the anus and rectum in a plastic bag (315 carcasses). The figure illustrates the importance of faecal contamination for the dissemination of 0 : 3 to the carcasses. Adapted from Andersen (1988).

62 % POSITIVEISOLATES 100 80 / /

60 40 20

// //



40C

[]

220C

[]

37 *C

// // // // // //

0

YE 0:3

YE

YK

YF

YI

YA

Fig. 6. Production of heat-stable enterotoxin (YEST) in vitro by Y. enterocolmca and related species at 4. 22, and 37°C, as deterrmned by the infant mouse assay. Key to the abbreviations: YE 0:3. Y. enterocolittca serogroup 0:3; YE, non-pathogenic Y. entercolitica: YK, Y. kristensenii: YF. Y. frederiksenii: YI, Y. interrnedia: YA, Y. aldooae. The figure illustrates the unique properties of !,'. krtstensem~. According to Kapperud (1982).

the use of bung cutter was supplemented by enclosing the anus and rectum in a carefully closed plastic bag (Fig. 5). New technologies for closing the rectum of pig carcasses, including the insertion of a pre-frozen ( - 1 9 0 ° C ) plug into the anus before rectum-loosening and gut removal, are currently being evaluated (Danish Meat Research Institute, 1989).

Enterotoxin production Production of heat-stable enterotoxin (YEST) after cultivation in vitro is widespread among Y. enterocolitica and Y. enterocolitica-like bacteria (Kapperud and Bergan, 1984; Schiemann, 1989: Fig. 6). The physiochemical, biological, and antigenic characteristics of YEST closely resemble those of the heat-stable enterotoxin of E. coli. Although there is no evidence thus far to support the involvement of YEST in the pathogenesis of Y. enterocolitica enteritis, the possibility still remains that enterotoxigenic strains may produce foodborne intoxication by means of preformed entertoxins. This assumption is based on the fact that YEST is able to resist gastric acidity as well as temperatures used in food processing and storage, without losing activity.

Foodborne outbreaks Although it is theoretically possible for virulent Y. enterocolitica to contaminate and then grow in many types of refrigerated foods, actual foodborne outbreaks caused by Y. enterocolitica are comparatively rare (WHO, 1987). It has been observed that in some countries extensive outbreaks have occurred (U.S.A., Japan),

63

while in other countries only sporadic cases have been detected (Cover and Abet, 1989; Schiemann, 1989). In Japan, several large outbreaks have been reported. In all cases, Y. enterocolitica serogroup 0:3 was the causative agent. The source of the infection was not detected in any of these cases. The endemic level of yersiniosis in the U.S.A. is lower than in European and many other countries. However, six major foodborne outbreaks have been documented in the U.S.A. during the recent years. The food vehicles were identified as chocolate milk, powdered milk and chow mein probably contaminated by a foodhandler, 'tofu' (soybean curd) manufactured with contaminated water, pasteurized milk indirectly involving swine, bean sprout immersed in well water, and chitterlings (a dish made from pig intestines). Four outbreaks involved 0:8, one involved O:13a, 13b, whereas the fifth outbreak, which implicated chitterlings, was caused by O:3, a serogroup which has so far been rare in the U.S.A. (Lee et at., 1990).

Recommendations

The following topics have been recommended for future research activities (WHO, 1987): (1) Epidemiological investigations, including case-control studies, should be conducted to assess the relative importance of potential risk factors for Y. enterocolitica infection, including food and water consumption and animal contacts. (2) Investigations are required to identify factors related to hygiene and husbandry practices at the farm which determine introduction of Y. enterocolitica into swine herds, and factors which influence colonization of the animals. (3) Critical control points (HACCP) at the stage of slaughter should be identified, and the efficiency of specific and non-specific control and preventive measures should be evaluated. (4) Universally acceptable isolation methods should be developed, which allow optimal recovery of all pathogenic serogroups, and which provide adequate differentiation between pathogenic and non-pathogenic variants. (5) The potential ability of Y. enterocolitica and Y. enterocolitica-like bacteria to produce preformed enterotoxin(s) in foods and cause foodborne intoxication, deserves further investigation.

References Aleksic, S., Steigerwait, A.G.. Bockemiihl, J., Huntley-Carter, G.P. and Brenner, D.J. (1987) Yersinia rohdei sp. nov. isolated from human and dog feces and surface water, int. J. Syst. Bact. 37, 327-332. Andersen, J.K. (1984) Humanpatogene Yersinia enterocolitica i danske svinebesa,'tninger. En epidemiologisk undersogelse. Thesis. Institute of Hygiene and Microbiology, Royal Veterinary and Agricultural University, Copenhagen. Andersen. J.K. (1988) Contamination of freshly slaughtered pig carcasses with pathogenic Yersinia enterocolitica. Int. J. Food Microbiol. 7, 193-202.

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Yersinia enterocolitica in food hygiene.

Yersinia enterocolitica and Yersinia enterocolitica-like bacteria constitute a fairly heterogenous group of bacteria which includes both well-establis...
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