# Yersinia enterocolitica: Epidemiological Studies and Outbreaks

Authors: Atiqur Rahman; Tania S. Bonny; Siriporn Stonsaovapak; Chiraporn Ananchaipattana
Journal: Journal of Pathogens
 (2011)

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## 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.


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## Body

## 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.AlthoughY. 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 Yersiniavirulence) [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 pathogenicY. enterocoliticahas 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 ofY. 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 pathogenicY. enterocoliticain 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 forY. 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. enterocoliticacompared to the strains isolated from humans with yersiniosis.Figure 1
Occurrence ofY. enterocoliticain natural samples.Pigs have been shown to be a major reservoir of pathogenicY. enterocoliticainvolved 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, pathogenicY. 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. enterocoliticabecause 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 pathogenicY. enterocolitica in natural samples with PCR and culture methods.
SampleNo. of samplesNo. of culture+vesamplesa (%)No. of PCR+vesamples (%)ReferencesAnimalPig tonsils18548(26)58(31)Fredriksson-Ahomaa et al. [21]252090(36)Boyapalle et al. [22]2415(63)18(75)Nesbakken et al. [23]829411(50)0Martínez et al. [24]630278(44)0Martínez et al. [25]21272(34)186(88)Fredriksson-Ahomaa et al. [26]Pig faeces255080(31)Boyapalle et al. [22]243(13)3(13)Nesbakken et al. [23]2793114(4)345(12)Bhaduri et al. [27]1503(2)0Okwori et al. [10]Mesenteric l. n.2570103(40)Boyapalle et al. [22]241(4)2(8)Nesbakken et al. [23]Submaxillary l. n.241(4)3(13)Fredriksson-Ahomaa et al. [20]Sheep feces2002(1)0Okwori et al. [10]Dog feces44806(1)Wang et al. [28]FoodbPig tongues157(47)10(67)Vishnubhatla et al. [29]9979(80)82(83)Fredriksson-Ahomaa and Korkeala  [11]Pig offalc11038(35)77(70)Fredriksson-Ahomaa et al. [20]Chitterlings3508(2)278(79)Boyapalle et al. [22]Ground pork3500133(38)Fredriksson-Ahomaa et al. [20]10032(32)47(47)Vishnubhatla et al. [29]Ground beef10023(23)31(31)Fredriksson-Ahomaa et al. [20]Minced pork2554(2)63(25)Fredriksson-Ahomaa and Korkeala  [11]Porkd3006(2)50(17)Johannessen et al. [30]916(7)9(10)Lambertz & Danielsson-Tham  [31]62020(32)Grahek-Ogden et al.  [32]Chicken4300Fredriksson-Ahomaa et al. [11]Fish15000Okwori et al. [10]Heated soup1003(3)Okwori et al. [10]Cow milk2503(1)Okwori et al. [10]Lettuce25003(3)Okwori et al. [10]Tofu5006(12)Vishnubhatla et al. [29]Vegetables271(4)4(15)Cocolin & Comi [33]Salad4216(38)16(38)Sakai et al. [34]EnvironmentWater1051(1)11(10)Sandery et al. [35]Slaughterhouse/ Farm895(6)12(13)Fredriksson-Ahomaa et al. [36]4644(96)0Martínez et al. [24]4531(61)0Martínez 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 ofY. 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 ofY. 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 humanY. 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. enterocoliticahave 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 pathogenicY. enterocolitica in pork products by culture methods (partially adapted from Fredriksson-and Korkeala [11]).
SampleNo. ofsamplesNo. of samples positive forCountry oforigin of sampleReferenceO:3O:5,27O:8O:9Tongue3021653BelgiumWauters [37]3711CanadaSchiemann [38]3126USADoyle et al. [39]4726NorwayNesbakken [40]5020JapanShiozawa et al. [41]1258SpainFerrer et al. [42]2928BelgiumWauters et al. [43]4062The Netherlandsde Boer and Nouws [44]5514GermanyKarib and Seeger [45]862Italyde Guisti et al. [46]9979FinlandFredriksson-Ahomaa et al. [47]2015GermanyFredriksson-Ahomaa et al. [48]Tonsil89818BelgiumMartínez et al. [24]1371361ItalyMartínez et al. [24]185185SpainMartínez et al. [24]2126961SwitzerlandFredriksson-Ahomaa et al. [26]Offala3417FinlandFredriksson-Ahomaa et al. [36]165FinlandFredriksson-Ahomaa et al. [47]10046GermanyFredriksson-Ahomaa et al. [48]Porkb9111CanadaSchiemann [38]1271NorwayNesbakken et al. [49]70223JapanShiozawa et al. [41]2676DenmarkChristensen [50]5012BelgiumWauters et al. [43]40031The Netherlandsde Boer and Nouws [44]458NorwayNesbakken et al. [51]6718c3ChinaTsai and Chen [52]4811GermanyKarib and Seeger [45]40241IrelandLogue et al. [53]12786414JapanFukushima et al. [54]2554FinlandFredriksson-Ahomaa et al. [55]3006NorwayJohannessen et al. [30]12014GermanyFredriksson-Ahomaa et al. [36]6020NorwayGrahek-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 ofY. 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 theY. 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].


## 2.1. Animal Reservoirs Involved in Zoonosis

Animals have long been suspected of being significant reservoirs forY. 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. enterocoliticacompared to the strains isolated from humans with yersiniosis.Figure 1
Occurrence ofY. enterocoliticain natural samples.Pigs have been shown to be a major reservoir of pathogenicY. enterocoliticainvolved 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, pathogenicY. 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. enterocoliticabecause 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 pathogenicY. enterocolitica in natural samples with PCR and culture methods.
SampleNo. of samplesNo. of culture+vesamplesa (%)No. of PCR+vesamples (%)ReferencesAnimalPig tonsils18548(26)58(31)Fredriksson-Ahomaa et al. [21]252090(36)Boyapalle et al. [22]2415(63)18(75)Nesbakken et al. [23]829411(50)0Martínez et al. [24]630278(44)0Martínez et al. [25]21272(34)186(88)Fredriksson-Ahomaa et al. [26]Pig faeces255080(31)Boyapalle et al. [22]243(13)3(13)Nesbakken et al. [23]2793114(4)345(12)Bhaduri et al. [27]1503(2)0Okwori et al. [10]Mesenteric l. n.2570103(40)Boyapalle et al. [22]241(4)2(8)Nesbakken et al. [23]Submaxillary l. n.241(4)3(13)Fredriksson-Ahomaa et al. [20]Sheep feces2002(1)0Okwori et al. [10]Dog feces44806(1)Wang et al. [28]FoodbPig tongues157(47)10(67)Vishnubhatla et al. [29]9979(80)82(83)Fredriksson-Ahomaa and Korkeala  [11]Pig offalc11038(35)77(70)Fredriksson-Ahomaa et al. [20]Chitterlings3508(2)278(79)Boyapalle et al. [22]Ground pork3500133(38)Fredriksson-Ahomaa et al. [20]10032(32)47(47)Vishnubhatla et al. [29]Ground beef10023(23)31(31)Fredriksson-Ahomaa et al. [20]Minced pork2554(2)63(25)Fredriksson-Ahomaa and Korkeala  [11]Porkd3006(2)50(17)Johannessen et al. [30]916(7)9(10)Lambertz & Danielsson-Tham  [31]62020(32)Grahek-Ogden et al.  [32]Chicken4300Fredriksson-Ahomaa et al. [11]Fish15000Okwori et al. [10]Heated soup1003(3)Okwori et al. [10]Cow milk2503(1)Okwori et al. [10]Lettuce25003(3)Okwori et al. [10]Tofu5006(12)Vishnubhatla et al. [29]Vegetables271(4)4(15)Cocolin & Comi [33]Salad4216(38)16(38)Sakai et al. [34]EnvironmentWater1051(1)11(10)Sandery et al. [35]Slaughterhouse/ Farm895(6)12(13)Fredriksson-Ahomaa et al. [36]4644(96)0Martínez et al. [24]4531(61)0Martínez 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 ofY. 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 ofY. 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 humanY. 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. enterocoliticahave 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 pathogenicY. enterocolitica in pork products by culture methods (partially adapted from Fredriksson-and Korkeala [11]).
SampleNo. ofsamplesNo. of samples positive forCountry oforigin of sampleReferenceO:3O:5,27O:8O:9Tongue3021653BelgiumWauters [37]3711CanadaSchiemann [38]3126USADoyle et al. [39]4726NorwayNesbakken [40]5020JapanShiozawa et al. [41]1258SpainFerrer et al. [42]2928BelgiumWauters et al. [43]4062The Netherlandsde Boer and Nouws [44]5514GermanyKarib and Seeger [45]862Italyde Guisti et al. [46]9979FinlandFredriksson-Ahomaa et al. [47]2015GermanyFredriksson-Ahomaa et al. [48]Tonsil89818BelgiumMartínez et al. [24]1371361ItalyMartínez et al. [24]185185SpainMartínez et al. [24]2126961SwitzerlandFredriksson-Ahomaa et al. [26]Offala3417FinlandFredriksson-Ahomaa et al. [36]165FinlandFredriksson-Ahomaa et al. [47]10046GermanyFredriksson-Ahomaa et al. [48]Porkb9111CanadaSchiemann [38]1271NorwayNesbakken et al. [49]70223JapanShiozawa et al. [41]2676DenmarkChristensen [50]5012BelgiumWauters et al. [43]40031The Netherlandsde Boer and Nouws [44]458NorwayNesbakken et al. [51]6718c3ChinaTsai and Chen [52]4811GermanyKarib and Seeger [45]40241IrelandLogue et al. [53]12786414JapanFukushima et al. [54]2554FinlandFredriksson-Ahomaa et al. [55]3006NorwayJohannessen et al. [30]12014GermanyFredriksson-Ahomaa et al. [36]6020NorwayGrahek-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 ofY. 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.


## 2.2.1. 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 humanY. 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. enterocoliticahave 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 pathogenicY. enterocolitica in pork products by culture methods (partially adapted from Fredriksson-and Korkeala [11]).
SampleNo. ofsamplesNo. of samples positive forCountry oforigin of sampleReferenceO:3O:5,27O:8O:9Tongue3021653BelgiumWauters [37]3711CanadaSchiemann [38]3126USADoyle et al. [39]4726NorwayNesbakken [40]5020JapanShiozawa et al. [41]1258SpainFerrer et al. [42]2928BelgiumWauters et al. [43]4062The Netherlandsde Boer and Nouws [44]5514GermanyKarib and Seeger [45]862Italyde Guisti et al. [46]9979FinlandFredriksson-Ahomaa et al. [47]2015GermanyFredriksson-Ahomaa et al. [48]Tonsil89818BelgiumMartínez et al. [24]1371361ItalyMartínez et al. [24]185185SpainMartínez et al. [24]2126961SwitzerlandFredriksson-Ahomaa et al. [26]Offala3417FinlandFredriksson-Ahomaa et al. [36]165FinlandFredriksson-Ahomaa et al. [47]10046GermanyFredriksson-Ahomaa et al. [48]Porkb9111CanadaSchiemann [38]1271NorwayNesbakken et al. [49]70223JapanShiozawa et al. [41]2676DenmarkChristensen [50]5012BelgiumWauters et al. [43]40031The Netherlandsde Boer and Nouws [44]458NorwayNesbakken et al. [51]6718c3ChinaTsai and Chen [52]4811GermanyKarib and Seeger [45]40241IrelandLogue et al. [53]12786414JapanFukushima et al. [54]2554FinlandFredriksson-Ahomaa et al. [55]3006NorwayJohannessen et al. [30]12014GermanyFredriksson-Ahomaa et al. [36]6020NorwayGrahek-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 ofY. 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 theY. 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 withY. 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’smonitoring and control purposes. Molecular methods should be needed with conventional culture methods to provide a better estimation of epidemiology of Y. enterocoliticaparticularly pathogenic strains in natural samplesTable 3
Epidemiological studies of human infection withY. enterocolitica.
YearCountryOutcome of the studyReferences1981–1990GeorgiaReport of 84 clinical isolates ofY. enterocolitica, the most frequently reported serotypes were O:5; O:10,46; O:6,30Sulakvelidze et al.[89]1982–1991The NetherlandsAnalysis of clinical information from 261 Dutch patients with gastrointestinal infections caused byY.  enterocolitica serotypes O:3 and O:9Stolk-Engelaar and Hoogkamp-Korstanje [90]1982aCanadaOutbreak of gastroenteritis among hospitalized patients associated withY. enterocolitica serotype O:5Ratnam et al.[91]1982–1985CanadaExamination of 125 isolates ofY. enterocolitica, serotypes O:7,8; O:5; O:6,30, were frequently obtained from symptomatic patientsNoble et al.[92]1983FinlandReport of 46 fecal isolates ofY. enterocolitica, including two serotypes O:7; O:6, associated with occurrenceSkurnik et al. [60]1984aBangladeshCase report of a fatal diarrheal illness associated with serotypes O:7; O:8Butler et al.[7]1984aHong KongReport ofY. enterocolitica-associated septicemia in four patients regarding serotypes O:17Seto and Lau [93]1984-1985UKReport of two nosocomial outbreaks ofY. enterocolitica serotypes O:10; O:6 infections in hospitalized childrenGreenwood and Hooper [94]1986aUKCase report of nosocomial transmission of serotypes O:6,30 associated with gastroenteritisMcIntyre and Nnochiri [95]1986–1992CanadaReport of 79 symptomatic children with culture-proven infection, including serotypes O:5; O:6,30; O:7,8Cimolai et al.[96]1987UKReport of 77Y. enterocolitica strains from patients, including serotypes O:6,30; O:7Greenwood and Hooper  [97]1987-1988AustraliaReport of 11 cases ofY. enterocolitica enteritis, including most frequently serotypes O:6,30Butt et al.[98]1987–1989ChileA prospective case-control study of infants with diarrhoea in Chile, showing a significantly reported serotypes O:6; O:7,8; O:7; O:10Morris et al.[99]1988–1991NigeriaOf nine strains ofY. enterocolitica obtained from stool samples of children with diarrhoeaOnyemelukwe [100]1988–1993New ZealandOf 918 isolates ofY. enterocolitica from symptomatic patientsFenwick and McCarthy [101]1968–2000BrazilOf 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 foodFalcão et al. [102]2002IranReport of 8 cases ofY. enterocolitica infection out of 300 children with acute diarrhoea aged 0–12 years who were attending a pediatric hospital in TehranSoltan-Dallal and Moezardalan [9]2002–2004NigeriaDetection ofY. enterocoliticabelonging to bioserotype 2/O:9 in investigating 500 human samplesOkwori et al. [10]2004JapanReport of 16 cases food poisoning due toY. enterocolitica serotype O:8Sakai et al. [34]2005–2006NorwayInvestigation of an outbreak involving 11 persons infected withYersinia enterocolitica O:9Grahek-Ogden et al.[32]2001-2008GermanyAlmost 90% ofY. enterocolitica strains were diagnosed as serotype O:3Rosner et al. [103]2009aIraqIdentification of three children with diarrhoea caused byY. enterocolitica infectionKanan and Abdulla [8]2009AustraliaReport of 1 outbreak with 3 cases due to consumption of roast pork contaminated withY. enterocoliticaOzFoodNet sites [104]aYear of publication.



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*Source: 239391-2011-10-16.xml*