Epidemiology of reported Yersinia enterocolitica infections in Germany, 2001-2008
© Rosner et al; licensee BioMed Central Ltd. 2010
Received: 5 January 2010
Accepted: 14 June 2010
Published: 14 June 2010
Yersiniosis is the third most common zoonotic bacterial disease in Germany and the European Union. Sequelae of Yersinia enterocolitica infections, such as reactive arthritis, have been reported. Consumption of pork and its products, especially eaten raw or undercooked, is an important risk factor of yersiniosis. Infection with Y. enterocolitica is notifiable through the national surveillance system for infectious diseases in Germany and several thousands of cases are being reported each year. We present recent data on the epidemiology of reported yersiniosis in Germany.
Surveillance data on yersiniosis, accessed through the national level database (SurvNet), were analyzed with regard to time trends, demographical and geographical distribution, serotypes, and hospitalization, for the time period 2001-2008.
A total of 47,627 cases of yersiniosis were reported. The mean annual incidence of yersiniosis was 7.2/100,000 population. A downward trend in the number of reportable cases has occurred since 2002. Almost all Y. enterocolitica infections were reported as single cases, i.e., with no apparent links to other cases. The number of reported infections showed substantially less seasonal variation than in other zoonotic enteric diseases. The incidence was highest in children under five years (58/100,000 population), in particular in one-year-old children (108/100,000 population). Almost 97% of infections were acquired domestically. High incidences occurred in the eastern German federal states Thuringia, Saxony, and Saxony-Anhalt. Differences in incidences across federal states were driven primarily by incidence differences in children under five years. Hospitalization was reported for 17% of cases, the proportion being highest among teenagers. Almost 90% of Y. enterocolitica strains were diagnosed as serotype O:3, which is the serotype most frequently isolated from pigs.
Yersiniosis is a zoonotic foodborne disease of relevance to public health in Germany because of its high incidence and risk for sequelae. The incidence of reported yersiniosis in Germany varies markedly from state to state, mainly due to incidence difference among young children. More research efforts should be directed towards the elucidation of risk factors of yersiniosis in this age group.
Yersiniosis due to infection with the bacterium Yersinia enterocolitica is a zoonotic gastrointestinal disease in humans. Y. enterocolitica species can be isolated from a variety of domestic and wildlife animals, e.g., pigs, cattle, sheep, goats, dogs, cats, wild boars, and small rodents . Pigs are considered to be the main reservoir of human pathogenic strains, largely because of the high prevalence of these strains in pigs and the high genetic similarity between porcine and human isolates [2–4]. Infections are thought to be primarily transmitted to humans by food, in particular, raw or undercooked pork and pork products [1, 5]. However, other risk factors, such as contaminated drinking water or pet animal contact, have been reported [6–9]. Six different biotypes (biotype 1A, 1B, 2-5) and numerous serotypes of Y. enterocolitica have been described. Eleven of those serotypes have frequently been associated with infections in humans . In Europe, most of the human pathogenic Y. enterocolitica strains are classified as biotype 4, serotype O:3 . Clinical symptoms of yersiniosis first appear after an incubation period of about 5 days (range 1-11 days) and include diarrhea, fever, vomiting, tenesma and abdominal pain. In older children and young adults, abdominal pain in the right lower abdomen can occur, which may be mistaken for appendicitis (pseudoappendicitis). Typically, symptoms disappear within 1-2 weeks after onset. Sequelae such as reactive arthritis or erythema nodosum sometimes occur . Yersiniosis contributes substantially to foodborne diseases in industrialized countries and is therefore notifiable through national surveillance systems in most countries within the European Union (EU), including Germany. After campylobacteriosis and salmonellosis, yersiniosis ranks third among the notifiable bacterial zoonoses in Germany and the EU. In 2007, 8,874 confirmed cases of yersiniosis were reported to the European Centre for Disease Control and Prevention (ECDC), 4,987 (56%) of which were from Germany . There is a paucity of recent comprehensive data on the epidemiology of yersiniosis, e.g., detailed analysis of trends over time or affected population groups.
Yersiniosis surveillance data from Germany were analyzed for the time period 2001-2008. An acute culture-confirmed infection with Yersinia enterocolitica is notifiable to the local health department according to the Protection against Infection Act (Infektionsschutzgesetz, IfSG) of 2001. Each notification has to be electronically forwarded from the local health department via the state health department to the federal public health institute, the Robert Koch Institute (RKI), where the national surveillance database is hosted. To ensure comparability of surveillance data across federal states, surveillance case definitions exist for each notifiable condition. A case of yersiniosis is included in the RKI statistics when the diseased person being reported as a case showed clinical symptoms (i.e. at least one of the following: diarrhea, abdominal pain, tenesma, fever with body temperature of 38.5°C or above, and vomiting) and the Y. enterocolitica infection was either culture-confirmed from stool or some other clinical material, or confirmed epidemiologically. Epidemiological confirmation of a case is defined as contact with another laboratory-confirmed case, contact with an animal infected with Y. enterocolitica, or consumption of food items contaminated with Y. enterocolitica. Prior to 2004, patients with clinical symptoms and serological evidence of infection (agglutination reaction (Widal), confirmation of IgA-, IgG- or IgM-antibodies by ELISA or Western blot) also fulfilled the case definition. Data were accessed through the national level database (SurvNet) at the RKI and analyzed with Microsoft Excel. Data are openly available via SurvStat@RKI http://www3.rki.de/SurvStat/[13, 14].
Annual number of reported Yersinia enterocolitica infections in Germany according to serotype
No information on serotype
Domestically acquired and imported Yersinia enterocolitica infections, 2001-2008
Most likely country
Other European countries
Percentage of reported Yersinia enterocolitica serotypes according to age group, 2001-2008
Age group (years)
0 to 4
5 to 9
10 to 19
20 to 39
40 to 59
60 and older
The causative agent was classified as Y. enterocolitica serotype O:3 in 89% of reported infections that were acquired in Germany or other countries of the EU and the European Free Trade Association (EFTA: EU plus Iceland, Liechtenstein, Norway, Switzerland). This percentage was only 77% when Y. enterocolitica infections were acquired in non-European countries. Y. enterocolitica serotype O:8 infections were more frequently imported from non-European countries than infections due to other serotypes (Table 2).
Symptoms of Yersinia enterocolitica infections
German surveillance data on yersiniosis due to Yersinia enterocolitica infection for the time period 2001-2008 has been analyzed. The incidence of Y. enterocolitica infection was highest among children under 5 years of age, in particular one-year-old children. In addition to consumption of pork, other risk factors of yersiniosis need to be considered for this age group. A recent case-control study conducted in Sweden among children < 7 years of age identified, in addition to pork consumption, contact to domestic animals, in particular dogs and cats, and use of a pacifier as risk factors . Age-specific risk factors, with evidence of environmental transmission, have also been demonstrated in infections with Shiga toxin-producing E. coli (STEC) and Campylobacter spp. [15, 16]. A high incidence of yersiniosis among young children has been reported in other countries, and acute diarrheal illnesses caused by enteric pathogens other than Y. enterocolitica, e.g., infections with Salmonella spp., Campylobacter spp., or E. coli including STEC, also occur at high frequencies among infants [17–20]. Factors that could contribute to the high incidence in reported diarrheal illnesses in this age group may include an increased rate of exposure to enteric pathogens as a result of fecal-oral contamination , predisposition to infection due to an immature and unchallenged immune system , higher frequency of physician consultations among parents of infants , or higher frequency of submission of stool samples for diagnosis by physicians when infants have been affected.
Within Germany, the highest incidences of yersiniosis occurred in the federal states Thuringia, Saxony, and Saxony-Anhalt. Similar results were obtained in a joint spatial analysis of 4 gastrointestinal infectious diseases, including yersiniosis, that took underreporting into account . Although drawing causal inferences from group level data to the individual level is error-prone, it is interesting to note that, according to a recent national nutrition study, consumption of meat products and sausages was relatively high in the states with the highest incidences of yersiniosis (e.g. Saxony and Thuringia). Unfortunately, published data do not specify the type of meat consumed, making it unclear whether these results are also true for pork products . The number of reported Y. enterocolitica infections did not show seasonal variability, which may support the hypothesis that the infection is transmitted via food items that are consumed consistently throughout the year, such as meat and meat products , rather than being associated with unknown environmental factors. Besides, environmental transmission of zoonotic enteric pathogens, direct contact to animals, for example, seems to be more pronounced in the summer, contributing to the seasonal peak incidences associated with warmer months, as in illnesses caused by STEC and Campylobacter spp. [15, 16].
Children were more frequently infected with Y. enterocolitica O:3 than adults, whereas adults ≥ 40 years of age were more frequently infected by Y. enterocolitica serotype O:9 than younger age groups. Prior exposure of children to Y. enterocolitica O:3 may conceivably provide some protection against acute infections due to the same serotype later in life, but not necessarily from other serotypes. Hospitalization was reported for 17% of patients infected with Y. enterocolitica, which is lower than the proportion of hospitalizations among reported Salmonella spp. infections in Germany (24%), but slightly higher than in reported Campylobacter spp. infections (14%) (unpublished data). Hospitalization was longer than the median of 4 days when serotypes other than O:3 were diagnosed. Hospitalization rate was highest and length of hospital stay was twice as long as the median when infection was due to serotype O:8, which may support the findings that the course of disease is more severe with this serotype . However, the total number of reported cases infected with serotype O:8 was low (62 reported cases over the study period) and insufficient for a more detailed analysis. Interestingly, the hospitalization rate was relatively high (28%) among teenagers (10-19 years). Symptoms of yersiniosis can resemble symptoms of appendicitis in this age group (pseudoappendicitis), which may account for more frequent hospitalizations  and unnecessary appendectomies among teenagers .
In Germany, the trend in the number of reportable cases of yersiniosis has been downward since 2002. The reason for this is uncertain, but can be observed for other gastrointestinal infections caused by enteric pathogens, e.g., salmonellosis, as well , with the exception of Campylobacter spp. infections. Improved food safety control measures and better hygiene measures during food preparation at the consumer level are possible explanations for the continuing decrease of Y. enterocolitica infections. Compared to other European countries, the incidence of yersiniosis in Germany remains relatively high. For example, in 2007, the overall incidence was about 2-fold higher (6.1/100,000 population) than the average in all European countries reporting to the European Centre for Disease Control and Prevention (ECDC) (2.9/100,000 population) . Several reasons need to be considered: First, variability in reporting systems, frequency of diagnosis, and degree of underreporting among European countries may contribute to incidence differences. Second, since consumption of pork is a risk factor of yersiniosis, food preferences will play an important role. Pork is the most frequently consumed meat in Germany with an annual consumption of about 40 kg per capita . Third, prevalence and concentration of Y. enterocolitica in food-producing animals and products made therefrom can also result in incidence differences among EU countries.
Surveillance data have their inherent limitations. For example, routine surveillance captures only a fraction of cases occurring in the population. Thus far, the degree of under-ascertainment remains to be systematically addressed in Germany. Based on studies that were conducted in other countries, it is estimated that for each culture-confirmed case of acute diarrheal illness, between 5 and 68 undiagnosed cases occur in the community [22, 30, 31]. Furthermore, a more severe course of disease is more likely to precipitate medical evaluation [32, 33], as is, probably, young age of the patient. Consequently, surveillance data are unlikely to be representative for the entirety of yersiniosis cases within the community. Surveillance data do not typically include detailed clinical information on every reported case, e.g., the presence of chronic diseases, cause of death, or detailed information on the laboratory diagnostic procedures. Despite these limitations, analysis of surveillance data can provide a good overview of the distribution of yersiniosis within the German population. However, identifying the risk factors of Y. enterocolitica infections, in particular among young children, requires analytical epidemiological methods. A case-control study is currently being conducted to elucidate and quantify the most important risk factors of Y. enterocolitica infections in Germany and assess sequelae-associated risk factors, with the aim of recommending effective preventive measures that will improve disease control.
In Germany, yersiniosis is a zoonotic enteric disease with public health relevance because of its high incidence and the possible sequelae. Young children are affected most frequently, in particular one-year-old children, but incidence in this age group varies markedly from state to state. More research effort is required to elucidate risk factors of Yersinia enterocolitica infections, especially in young children.
This work was supported by grant 01KI 07127 (Foodborne Zoonotic Infections of Humans; FBI-Zoo) from the German Federal Ministry of Education and Research (BMBF). The authors would like to thank Dr. Christina Frank for helpful comments on the manuscript.
- Bottone EJ: Yersinia enterocolitica: overview and epidemiologic correlates. Microbes and Infection. 1999, 1: 323-333. 10.1016/S1286-4579(99)80028-8.View ArticlePubMedGoogle Scholar
- Fosse J, Seegers H, Magras C: Prevalence and risk factors for bacterial food-borne zoonotic hazards in slaughter pigs: a review. Zoonoses Public Health. 2009, 56: 429-454. 10.1111/j.1863-2378.2008.01185.x.View ArticlePubMedGoogle Scholar
- Fredriksson-Ahomaa M, Hallanvuo S, Korte T, Siitonen A, Korkeala H: Correspondence of genotypes of sporadic Yersinia enterocolitica bioserotype 4/O:3 strains from human and porcine sources. Epidemiol Infect. 2001, 127: 37-47. 10.1017/S0950268801005611.View ArticlePubMedPubMed CentralGoogle Scholar
- Fredriksson-Ahomaa M, Stolle A, Siitonen A, Korkeala H: Sporadic human Yersinia enterocolitica infections caused by bioserotype 4/O:3 originate mainly from pigs. J Med Microbiol. 2006, 55: 747-749. 10.1099/jmm.0.46523-0.View ArticlePubMedGoogle Scholar
- Tauxe RV, Wauters G, Goossens V, Van Noyen R, Vandepitte J, Martin SM, De Mol P, Thiers G: Yersinia enterocolitica infections and pork: the missing link. Lancet. 1987, i:1129-1132.Google Scholar
- Thompson JS, Gravel MJ: Family outbreak of gastroenteritis due to Yersinia enterocolitica serotype O:3 from well water. Can J Microbiol. 1986, 32 (8): 700-701. 10.1139/m86-127.View ArticlePubMedGoogle Scholar
- Ostroff SM, Kapperud G, Hutwagner LC, Nesbakken T, Bean NH, Lassen J, Tauxe RV: Sources of sporadic Yersinia enterocolitica infections in Norway: a prospective case-control study. Epidemiol Infect. 1994, 112: 133-141. 10.1017/S0950268800057496.View ArticlePubMedPubMed CentralGoogle Scholar
- Boqvist S, Pettersson H, Svensson Å, Andersson Y: Sources of sporadic Yersinia enterocolitica infection in children in Sweden, 2004: a case-control study. Epidemiol Infect. 2008, 137 (6): 897-905. 10.1017/S0950268808001209.View ArticlePubMedGoogle Scholar
- Satterthwaite P, Pritchard K, Floyd D, Law B: A case-control study of Yersinia enterocolitica infections in Auckland. Austr N Z J Public Health. 1999, 23: 482-485. 10.1111/j.1467-842X.1999.tb01303.x.View ArticleGoogle Scholar
- European Food|Safety Authority (EFSA): The Community Summary Report on Trends and Sources of Zoonoses and Zoonotic Agents in the European Union in 2007. EFSA J. 2009, 223-Google Scholar
- Cover TL, Aber RC: Yersinia enterocolitica. N Engl J Med. 1989, 321: 16-24. 10.1056/NEJM198907063210104.View ArticlePubMedGoogle Scholar
- European Centre for Disease Control and Prevention (ECDC): Annual Epidemiological Report on Communicable Diseases in Europe 2009. 2009, Stockholm: European Centre for Disease Prevention and ControlGoogle Scholar
- Faensen D, Claus H, Benzler J, Ammon A, Pfoch T, Breuer T, Krause G: SurvNet@RKI - a multistate electronic reporting system for communicable diseases. Euro Surveill. 2006, 11 (4): [http://www.eurosurveillance.org/ViewArticle.aspx?ArticleId=614]Google Scholar
- Faensen D, Krause G: SurvStat@RKI - a web-based solution to query surveillance data in Germany. Euro Surveill. 2004, 8 (22): pii = 2477Google Scholar
- Werber D, Behnke S, Fruth A, Merle R, Menzler S, Glaser S, Kreienbrock L, Prager R, Tschäpe H, Roggentin P, Bockemühl J, Ammon A: Shiga toxin-producing Escherichia coli infection in Germany-different risk factors for different age groups. Am J Epidemiol. 2007, 165: 425-434. 10.1093/aje/kwk023.View ArticlePubMedGoogle Scholar
- Ethelberg S, Simonsen J, Gerner-Smidt G, Olsen KEP, Mølbak K: Spatial distribution and registry-based case-control analysis of Campylobacter infections in Denmark, 1991-2001. Am J Epidemiol. 2005, 162: 1008-1015. 10.1093/aje/kwi316.View ArticlePubMedGoogle Scholar
- Robert Koch-Institut: Infektionsepidemiologisches Jahrbuch meldepflichtiger Krankheiten für 2008. 2009, Berlin: Robert Koch-InstitutGoogle Scholar
- Koehler KM, Lasky T, Fein SB, DeLong SM, Hawkins MA, Rabatsky-Ehr T, Ray SM, Shiferaw B, Swanson E, Vugia DJ, EIP FoodNet Working Group: Population-based incidence of infection with selected bacterial enteric pathogens in children younger than five years of age, 1996-1998. Ped Inf Dis J. 2006, 25: 129-134. 10.1097/01.inf.0000199289.62733.d5.View ArticleGoogle Scholar
- Verhaegen J, Charlier J, Lemmens P, Delmée M, Van Noyen R, Verbist L, Wauters G: Surveillance of human Yersinia enterocolitica infections in Belgium: 1967-1996. Clin Infect Dis. 1998, 27: 59-64. 10.1086/514636.View ArticlePubMedGoogle Scholar
- Centers for Disease Control and Prevention: Preliminary Food Net data on the incidence of infection with pathogens transmitted commonly through food-10 States, 2008. MMWR Weekly. 2009, 58 (13): 333-337.Google Scholar
- Cohen MB: Etiology and mechanisms of acute infectious diarrhea in infants in the United States. J Pediatr. 1991, 118: S34-S39. 10.1016/S0022-3476(05)81423-4.View ArticlePubMedGoogle Scholar
- Scallan E, Jones TF, Cronquist A, Thomas S, Frenzen P, Hoefer D, Medus C, Angulo FJ, The Foodnet Working Group: Factors associated with seeking medical care and submitting a stool sample in estimating the burden of foodborne illness. Foodborne Pathog Dis. 2006, 3: 432-438. 10.1089/fpd.2006.3.432.View ArticlePubMedGoogle Scholar
- Held L, Graziano G, Frank C, Rue H: Joint spatial analysis of gastrointestinal infectious diseases. Stat Methods Med Res. 2006, 15: 465-480.PubMedGoogle Scholar
- Max Rubner-Institute, Federal Research Centre for Nutrition and Food: National Nutrition Survey II, part 2. 2008, [http://www.was-esse-ich.de/]Google Scholar
- Bottone EJ: Yersinia enterocolitica: The charisma continues. Clin Microbiol Rev. 1997, 10: 257-276.PubMedPubMed CentralGoogle Scholar
- Perdikogianni C, Galanakis E, Michalakis M, Giannoussi E, Maraki S, Tselentis Y, Charissis G: Yersinia enterocolitica infection mimicking surgical conditions. Pediatr Surg Int. 2006, 22: 589-592. 10.1007/s00383-006-1703-y.View ArticlePubMedGoogle Scholar
- Van Noyen R, Selderslaghs R, Bekaert J, Wauters G, Vandepitte J: Causative role of Yersinia and other enteric pathogens in the appendicular syndrome. Eur J Clin Microbiol Infect Dis. 1991, 10: 735-741. 10.1007/BF01972498.View ArticlePubMedGoogle Scholar
- Frank C, Käsbohrer A, Stark K, Werber D: Marked decrease in reporting incidence of salmonellosis driven by lower rates of Salmonella Enteritidis infections in Germany in 2008 - a continuing trend. Euro Surveill. 2009, 14: 1-2.Google Scholar
- Statistisches Bundesamt: Vom Erzeuger zum Verbraucher, Fleischversorgung in Deutschland, 2008. 2008, Wiesbaden: Statistisches Bundesamt, [https://www-ec.destatis.de/csp/shop/sfg/bpm.html.cms.cBroker.cls?cmspath=struktur,vollanzeige.csp&ID=1022244]Google Scholar
- Voetsch AC, Van Gilder TJ, Angulo FJ, Farley MM, Shallow S, Marcus R, Cieslak PR, Deneen VC, Tauxe RV, Emerging Infections Program FoodNet Working Group: FoodNet estimate of the burden of illness caused by nontyphoidal Salmonella infections in the United States. Clin Infect Dis. 2004, 38: S127-S134. 10.1086/381578.View ArticlePubMedGoogle Scholar
- Wheeler JG, Sethi D, Cowden JM, Wall PG, Rodrigues LC, Tompkins DS, Hudson MJ, Roderick PJ, Infectious Intestinal Disease Study Executive: Study of infectious intestinal disease in England: rates in the community, presenting to general practice, and reported to national surveillance. BMJ. 1999, 318: 1046-1050.View ArticlePubMedPubMed CentralGoogle Scholar
- De Wit MAS, Kortbeek LM, Koopmans MPG, De Jager CJ, Wannet WJB, Bartelds AIM, Van Duynhoven YTHP: A comparison of gastroenteritis in a general practice-based study and a community-based study. Epidemiol Infect. 2001, 127: 389-397. 10.1017/S0950268801006082.View ArticlePubMedPubMed CentralGoogle Scholar
- Tam CC, Rodrigues LC, O'Brien SJ: The study of infectious intestinal disease in England: what risk factors for presentation to general practice tell us about potential for selection bias in case-control studies of reported cases of diarrhoea. Int J Epidemiol. 2003, 32: 99-105. 10.1093/ije/dyg007.View ArticlePubMedGoogle Scholar
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