Journal of PathogensVolume 2011 (2011), Article ID 239391, 11 pagesdoi:10.4061/2011/239391

Review Article

Yersinia enterocolitica: Epidemiological Studies and Outbreaks

Atiqur Rahman,¹ Tania S. Bonny,¹ Siriporn Stonsaovapak,² and Chiraporn Ananchaipattana³

¹Department of Microbiology, University of Dhaka, Dhaka 1000, Bangladesh²Applied Microbiology Department, Institute of Food Research and Product Development (IFRPD), Kasetsart University, Bangkok 10903, Thailand³Department of Biology, Faculty of Science and Technology, Rajamangala University of Technology Thanyaburi, Panthumthani 121100, Thailand

Received 1 May 2011; Accepted 20 July 2011

Academic Editor: Latiful Bari

Copyright © 2011 Atiqur Rahman et al. This is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

Abstract.

Yersinia enterocolitica is the most common bacteriological cause of gastrointestinal disease in many developed and developing countries. Although contaminated food is the main source of human infection due to Y. enterocolitica, animal reservoir and contaminated environment are also considered as other possible infection sources for human in epidemiological studies. Molecular based epidemiological studies are found to be more efficient in investigating the occurrence of human pathogenic Y. enterocolitica in natural samples, in addition to conventional culture based studies.

1. Introduction

Foodborne diseases are a widespread and growing public health problem in developed and developing countries [1]. Amongst those, yersiniosis due to infection with the bacterium Yersinia enterocolitica is the frequently reported zoonotic gastrointestinal disease after campylobacteriosis and salmonellosis in many developed countries, especially in temperate zones [2]. Within developed countries, incidences of yersiniosis and foodborne outbreaks are appeared to be lower in the United States than many European countries [3–5]. In European countries, numbers of reported cases of human in England and Wales are lower than those in other European countries where fewer than 0.1 cases of yersiniosis per 100,000 individuals were reported in the United Kingdom in 2005, in contrast to 12.2 in Finland and 6.8 in Germany [6]. On the other hand, the high prevalence of gastrointestinal illness including fatal cases due to yersiniosis is also observed in many developing countries like Bangladesh [7], Iraq [8], Iran [9], and Nigeria [10], which indicates major underlying food safety problems in low- and middle-income countries. Worldwide, infection with Y. enterocolitica occurs most often in infants and young children with common symptoms like fever, abdominal pain, and diarrhea, which is often bloody. Older children and young adults are not out of risk. The predominant symptoms within these age groups are right-sided abdominal pain and fever, sometimes confused with appendicitis. Occasionally, the Y. enterocolitica associated complications such as skin rash, joint pains, or spread of bacteria to the bloodstream can also occur.

Although Y. enterocolitica is a ubiquitous microorganism, the majority of isolates recovered from asymptomatic carriers, infected animals, contaminated food, untreated water, and contaminated environmental samples are nonpathogenic having no clinical importance [11]. At the same time, the epidemiology of Y. enterocolitica infections is complex and remains poorly understood because most sporadically occurred cases of yersiniosis are reported without an apparent source [3, 12–14]. However, most pathogenic Y. enterocolitica strains associated with human yersiniosis belong to bioserotypes 1B/O:8, 2/O:5,27, 2/O:9, 3/O:3, and 4/O:3. Within these reported strains, fully pathogenic strains carry an approximately 70 kb plasmid termed pYV (plasmid for Yersinia virulence) [15] that encodes various virulence genes (tccC, yadA, virF, ysa) with traditional chromosomal virulence genes (inv, ail, yst) whereas other pathogenic strains, having no pYV plasmid, produce a thermostable enterotoxin (ystA) [16–18]. These virulence genes located in chromosome or plasmid of pathogenic Y. enterocolitica has been widely used to identify pathogenic strains in epidemiological studies for example, chromosomal ail gene [19, 20].

2. Epidemiological Studies and Outbreaks

Many factors related to the epidemiology of Y. enterocolitica, such as human and nonhuman sources, and contamination routes in foods remain obscure in developing countries and tropical regions of developed countries. Additionally, epidemiological data on the prevalence of pathogenic Y. enterocolitica in animals in developed countries are missing as the reporting of this pathogen in animals is not mandatory in most European countries [26].

2.1. Animal Reservoirs Involved in Zoonosis

Animals have long been suspected of being significant reservoirs for Y. enterocolitica and, therefore, sources of human infections [3]. Numerous studies have been carried out to isolate Y. enterocolitica strains from a variety of animals (Figure 1) [56]. Interestingly, most of the strains isolated from the animal kingdom carry unique serotypes of Y. enterocolitica compared to the strains isolated from humans with yersiniosis.

Figure 1: Occurrence of Y. enterocolitica in natural samples.

Pigs have been shown to be a major reservoir of pathogenic Y. enterocolitica involved in human infections, particularly for strains of bioserotype 4/O:3 which has been almost exclusively isolated in European countries like Denmark, Italy, Belgium, Spain, and Sweden [24, 64]. The rate of isolation of Y. enterocolitica including bioserotype 4/O:3 from tonsils and tongues of pigs is generally greater than the rate of isolation from cecal or fecal materials [20].

Occasionally, pathogenic Y. enterocolitica strains, mostly of bioserotype 4/O:3, have also been isolated from dogs and cats [82]. Although pigs are the primary source of human infection with Y. enterocolitica throughout world, these pets may also be a potential source of human infection with pathogenic Y. enterocolitica because of their intimate contact with people, especially young children [28].

In addition with mostly isolated bioserotype 4/O:3, Y. enterocolitica strains of biotypes 2 and 3 and serotypes O:5,27, O:8, and O:9 have also been isolated from slaughter pigs, cows, sheep, and goats; however, the reservoir of these bioserotypes is not clearly established [81, 83–85]. In above cases, contamination of pluck sets (tongue, tonsils, and trachea hanging together with thoracic organs such as lungs, liver, and heart) and carcasses with enteropathogenic Yersinia from tonsils and feces may occur during the slaughtering stage [5, 82, 86–88]. On the other hand, strains of very rare bioserotypes, such as bioserotype 5/O:2,3, have been isolated from sheep, hares, and goats and bioserotype 3/O:1,2a,3 from chinchillas (small rodent). Thus, the patterns of the pathogenic strains isolated from humans with yersiniosis compared to those from the animals suggest that the human infection due to Y. enterocolitica originated from the animals.

2.2. Contaminated Food Involved in Infections

Food has been proposed to be the main source of intestinal yersiniosis although pathogenic isolates have seldom been recovered from food samples [105]. The low recovery rates of pathogenic Y. enterocolitica in food samples may be due to limited sensitivity of culture methods [11]. However, Y. enterocolitica has been isolated from milk and milk products, egg products, raw meats (beef, pork, and lamb) and poultry, vegetables, and miscellaneous prepared food products. The occurrence of pathogenic Y. enterocolitica in natural sample including foods has been estimated by both culture- and molecular-based methods (Table 1, Figures 2 and 3).

Table 1: Detection of pathogenic Y. enterocolitica in natural samples with PCR and culture methods.

Sample
No. of samples
No. of culture+vesamplesa (%)
No. of PCR+vesamples (%)
References

Animal

Pig tonsils
185
48
(26)
58
(31)
Fredriksson-Ahomaa et al. [21]

252
0

90
(36)
Boyapalle et al. [22]

24
15
(63)
18
(75)
Nesbakken et al. [23]

829
411
(50)
0

Martínez et al. [24]

630
278
(44)
0

Martínez et al. [25]

212
72
(34)
186
(88)
Fredriksson-Ahomaa et al. [26]

Pig faeces
255
0

80
(31)
Boyapalle et al. [22]

24
3
(13)
3
(13)
Nesbakken et al. [23]

2793
114
(4)
345
(12)
Bhaduri et al. [27]

150
3
(2)
0

Okwori et al. [10]

Mesenteric l. n.
257
0

103
(40)
Boyapalle et al. [22]

24
1
(4)
2
(8)
Nesbakken et al. [23]

Submaxillary l. n.
24
1
(4)
3
(13)
Fredriksson-Ahomaa et al. [20]

Sheep feces
200
2
(1)
0

Okwori et al. [10]

Dog feces
448
0

6
(1)
Wang et al. [28]

Food b

Pig tongues
15
7
(47)
10
(67)
Vishnubhatla et al. [29]

99
79
(80)
82
(83)
Fredriksson-Ahomaa and Korkeala [11]

Pig offalc
110
38
(35)
77
(70)
Fredriksson-Ahomaa et al. [20]

Chitterlings
350
8
(2)
278
(79)
Boyapalle et al. [22]

Ground pork
350
0

133
(38)
Fredriksson-Ahomaa et al. [20]

100
32
(32)
47
(47)
Vishnubhatla et al. [29]

Ground beef
100
23
(23)
31
(31)
Fredriksson-Ahomaa et al. [20]

Minced pork
255
4
(2)
63
(25)
Fredriksson-Ahomaa and Korkeala [11]

Porkd
300
6
(2)
50
(17)
Johannessen et al. [30]

91
6
(7)
9
(10)
Lambertz & Danielsson-Tham [31]

62
0

20
(32)
Grahek-Ogden et al. [32]

Chicken
43
0

0

Fredriksson-Ahomaa et al. [11]

Fish
150
0

0

Okwori et al. [10]

Heated soup
100
3
(3)

Okwori et al. [10]

Cow milk
250
3
(1)

Okwori et al. [10]

Lettuce
250
0

3
(3)
Okwori et al. [10]

Tofu
50
0

6
(12)
Vishnubhatla et al. [29]

Vegetables
27
1
(4)
4
(15)
Cocolin & Comi [33]

Salad
42
16
(38)
16
(38)
Sakai et al. [34]

Environment

Water
105
1
(1)
11
(10)
Sandery et al. [35]

Slaughterhouse/ Farm
89
5
(6)
12
(13)
Fredriksson-Ahomaa et al. [36]

46
44
(96)
0

Martínez et al. [24]

45
31
(61)
0

Martínez et al. [25]

aPathogenicity of isolates confirmed, ball meat samples are raw, cliver, heart, kidney, dexcept pig offal & tongues, and +vepositive.

Figure 2: Methods used for epidemiological studies of Y. enterocolitica-1. Selective enrichment methods [43]; selective agar media [11]; cold enrichment method [57]; biochemical & serological identification methods [58–63]. (PBS: Phosphate buffered saline; PSB: Phosphate-buffered saline with sorbitol and bile salts; MRB: Modified Rappaport broth containing magnesium chloride, malachite green, and carbenicillin; ITC: Modified Rappaport base supplemented with irgasan, ticarcillin, and potassium chlorate; BOS: Bile-oxalate-sorbose medium; TSB: Tryptic soy broth; TSPN: TSB with polymyxin and novobiocin; CIN: Cefsulodin-irgasan-novobiocin; SSDC: Salmonella-Shigella deoxycolate calcium chloride; VYE: Virulent Yersinia enterocolitica; SSI: Statens Serum Institute, Copenhagen, Denmark, enteric medium).

Figure 3: Methods used for epidemiological studies of Y. enterocolitica-2. DNA colony hybridization assays [51, 65–70]; PCR based detection methods [11, 71–81]. (inv: gene for invasin, an outer membrane protein that is required for efficient translocation of bacteria across the intestinal epithelium; ail: gene for adhesin, an outer membrane protein that may contribute to adhesion, invasion and resistance to complement-mediated lysis; yst: gene for heat-stable enterotoxin that may contribute to the pathogenesis of diarrhea associated with acute yersiniosis; virF: gene for transcriptional activator; yadA, gene for Yersinia adhesin A; PFGE: pulsed field gel electrophoresis).

2.2.1. Contaminated Meat and Poultry Products Correlated with yersiniosis

Indirect evidence considering food, particularly pork and pork products, indicates that there is an important link between consumption of raw, undercooked, or improperly handled pork product and human Y. enterocolitica infections [20]. This positive correlation between the consumption of raw or undercooked pork and the prevalence of yersiniosis has been demonstrated in case-control studies [32, 64, 106–109]. Using molecular techniques, ail-positive Y. enterocolitica strains were detected in raw pork samples (loin, fillet, chop, ham, and minced meat) and in ready-to-eat pork products [31]. However, the isolation rates of pathogenic bioserotypes of Y. enterocolitica have been low in raw pork, except for in edible pig offal, with the most common type isolated being bioserotype 4/O:3 (Table 2). In other studies, pathogenic yst-positive Y. enterocolitica strains have been isolated from ground beef [29] but not detected in chicken food samples [110].

Table 2: Detection of pathogenic Y. enterocolitica in pork products by culture methods (partially adapted from Fredriksson-and Korkeala [11]).

Sample
No. ofsamples
No. of samples positive for
Country oforigin of sample
Reference

O:3
O:5,27
O:8
O:9

Tongue
302
165

3
Belgium
Wauters [37]

37
11

Canada
Schiemann [38]

31
2

6

USA
Doyle et al. [39]

47
26

Norway
Nesbakken [40]

50
20

Japan
Shiozawa et al. [41]

125
8

Spain
Ferrer et al. [42]

29
28

Belgium
Wauters et al. [43]

40
6

2
The Netherlands
de Boer and Nouws [44]

55
14

Germany
Karib and Seeger [45]

86
2

Italy
de Guisti et al. [46]

99
79

Finland
Fredriksson-Ahomaa et al. [47]

20
15

Germany
Fredriksson-Ahomaa et al. [48]

Tonsil
89
81

8
Belgium
Martínez et al. [24]

137
136
1

Italy
Martínez et al. [24]

185
185

Spain
Martínez et al. [24]

212
69
6

1
Switzerland
Fredriksson-Ahomaa et al. [26]

Offala
34
17

Finland
Fredriksson-Ahomaa et al. [36]

16
5

Finland
Fredriksson-Ahomaa et al. [47]

100
46

Germany
Fredriksson-Ahomaa et al. [48]

Porkb
91
1

1

Canada
Schiemann [38]

127
1

Norway
Nesbakken et al. [49]

70
22

3
Japan
Shiozawa et al. [41]

267
6

Denmark
Christensen [50]

50
12

Belgium
Wauters et al. [43]

400
3

1
The Netherlands
de Boer and Nouws [44]

45
8

Norway
Nesbakken et al. [51]

67
1
8c
3

China
Tsai and Chen [52]

48
1

1
Germany
Karib and Seeger [45]

40
2
4

1
Ireland
Logue et al. [53]

1278
64
14

Japan
Fukushima et al. [54]

255
4

Finland
Fredriksson-Ahomaa et al. [55]

300
6

Norway
Johannessen et al. [30]

120
14

Germany
Fredriksson-Ahomaa et al. [36]

60

20
Norway
Grahek-Ogden et al. [32]

aOffal, excluding tongue, bother pork products, excluding offal, cisolates belonging to serotype O:5 and showing autoagglutination activity and calcium-dependent growth.

2.2.2. Contaminated Milk and Milk Products Associated with Human Disease

Y. enterocolitica has been isolated from raw milk in many countries, like Australia, Canada, Czechoslovakia, and USA. There were also a few reports on the isolation of this pathogenic strain associated with human disease from pasteurized milk [4, 111]. It may be due to the malfunction in the pasteurization process leading to inadequate treatment or postprocess contamination, or it may be due to the contamination with heat-resistant strains of Y. enterocolitica. So, the presence of this pathogen in pasteurized milk should be a cause for concern. However, heat-resistant strains of Y. enterocolitica have not been still reported in milk samples.

2.2.3. Other Contaminated Foods Involved in Outbreaks

Strains of Y. enterocolitica have been isolated from oysters, mussels, shrimp, blue crab, fish, salad, stewed mushrooms, cabbage, celery, and carrots [112]. In Korea, Lee et al. [113] isolated ail-positive Y. enterocolitica strain of bioserotype 3/O:3 from ready-to-eat vegetables, which indicate that vegetables can be a source of human infection. Furthermore, Sakai et al. [34] reported an outbreak of food poisoning by Y. enterocolitica serotype O:8 in Japan where salad was proposed the cause of infection. Recently, Y. enterocolitica 2/O:9 has been isolated from chicken eggshell surfaces in Argentina [114]. Contamination of the egg surface might have occurred from contact with other Y. enterocolitica-contaminated animal products, such as pork product, during collection on farms or during transportation or handling in retail shops.

2.3. Contaminated Environment Reported as Source of Infection

Most of the Y. enterocolitica isolates recovered from environmental samples, including the slaughterhouse, fodder, soil, and water, have been nonpathogenic [89, 115–119]. Occasionally, strains of bioserotype 4/O:3 have been isolated from the slaughterhouse [120, 121] and sewage water [50]. Within the environmental sampling sites, drinking water has been relatively widely investigated and revealed to be a significant reservoir for nonpathogenic Y. enterocolitica. However, Sandery et al. [35] detected pathogenic Y. enterocolitica in environmental water by molecular studies. In a case-control study, untreated drinking water has been reported to be a risk factor for sporadic Y. enterocolitica infections in Norway [107]. Recently, Falcão et al. [122] tested 67 Y. enterocolitica strains isolated in Brazil from untreated water for the presence of virulence genes. They found that all 38 strains of serotype O:5,27 possessed inv, ail, and yst genes, suggesting that untreated water may be responsible for the human infection with Y. enterocolitica. In another study, Y. enterocolitica O:8 strains have been isolated from stream water in Japan, which indicate that stream water may be a possible infection source for human Y. enterocolitica O:8 infections [84, 123].

3. Conclusion

Epidemiological studies of human infection with Y. enterocolitica (Table 3) constitute an important element in the exploitation of apparent sources and contamination routes of human yersiniosis and in the development and implementation of effective control strategies to prevent future outbreaks. Efficient laboratory methods used for epidemiological study are also a vital requirement in Y. enterocolitica’s monitoring and control purposes. Molecular methods should be needed with conventional culture methods to provide a better estimation of epidemiology of Y. enterocolitica particularly pathogenic strains in natural samples

Table 3: Epidemiological studies of human infection with Y. enterocolitica.

Year
Country
Outcome of the study
References

1981–1990
Georgia
Report of 84 clinical isolates of Y. enterocolitica, the most frequently reported serotypes were O:5; O:10,46; O:6,30
Sulakvelidze et al. [89]

1982–1991
The Netherlands
Analysis of clinical information from 261 Dutch patients with gastrointestinal infections caused by Y. enterocolitica serotypes O:3 and O:9
Stolk-Engelaar and Hoogkamp-Korstanje [90]

1982a
Canada
Outbreak of gastroenteritis among hospitalized patients associated with Y. enterocolitica serotype O:5
Ratnam et al. [91]

1982–1985
Canada
Examination of 125 isolates of Y. enterocolitica, serotypes O:7,8; O:5; O:6,30, were frequently obtained from symptomatic patients
Noble et al. [92]

1983
Finland
Report of 46 fecal isolates of Y. enterocolitica, including two serotypes O:7; O:6, associated with occurrence
Skurnik et al. [60]

1984a
Bangladesh
Case report of a fatal diarrheal illness associated with serotypes O:7; O:8
Butler et al. [7]

1984a
Hong Kong
Report of Y. enterocolitica-associated septicemia in four patients regarding serotypes O:17
Seto and Lau [93]

1984-1985
UK
Report of two nosocomial outbreaks of Y. enterocolitica serotypes O:10; O:6 infections in hospitalized children
Greenwood and Hooper [94]

1986a
UK
Case report of nosocomial transmission of serotypes O:6,30 associated with gastroenteritis
McIntyre and Nnochiri [95]

1986–1992
Canada
Report of 79 symptomatic children with culture-proven infection, including serotypes O:5; O:6,30; O:7,8
Cimolai et al. [96]

1987
UK
Report of 77 Y. enterocolitica strains from patients, including serotypes O:6,30; O:7
Greenwood and Hooper [97]

1987-1988
Australia
Report of 11 cases of Y. enterocolitica enteritis, including most frequently serotypes O:6,30
Butt et al. [98]

1987–1989
Chile
A prospective case-control study of infants with diarrhoea in Chile, showing a significantly reported serotypes O:6; O:7,8; O:7; O:10
Morris et al. [99]

1988–1991
Nigeria
Of nine strains of Y. enterocolitica obtained from stool samples of children with diarrhoea
Onyemelukwe [100]

1988–1993
New Zealand
Of 918 isolates of Y. enterocolitica from symptomatic patients
Fenwick and McCarthy [101]

1968–2000
Brazil
Of 106 strains (selected from the collection of the Yersinia Reference Laboratory in Brazil), 71 were bioserotype 4/O:3, isolated from human and animal clinical material, and 35 were of biotype 1A or 2, isolated from food
Falcão et al. [102]

2002
Iran
Report of 8 cases of Y. enterocolitica infection out of 300 children with acute diarrhoea aged 0–12 years who were attending a pediatric hospital in Tehran
Soltan-Dallal and Moezardalan [9]

2002–2004
Nigeria
Detection of Y. enterocolitica belonging to bioserotype 2/O:9 in investigating 500 human samples
Okwori et al. [10]

2004
Japan
Report of 16 cases food poisoning due to Y. enterocolitica serotype O:8
Sakai et al. [34]

2005–2006
Norway
Investigation of an outbreak involving 11 persons infected with Yersinia enterocolitica O:9
Grahek-Ogden et al. [32]

2001-2008
Germany
Almost 90% of Y. enterocolitica strains were diagnosed as serotype O:3
Rosner et al. [103]

2009a
Iraq
Identification of three children with diarrhoea caused by Y. enterocolitica infection
Kanan and Abdulla [8]

2009
Australia
Report of 1 outbreak with 3 cases due to consumption of roast pork contaminated with Y. enterocolitica
OzFoodNet sites [104]

aYear of publication.

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