Global Prevalence of <i>Yersinia enterocolitica</i> in Cases of Gastroenteritis: A Systematic Review and Meta-Analysis

Riahi, Seyed Mohammad; Ahmadi, Ehsan; Zeinali, Tayebeh

doi:https://doi.org/10.1155/2021/1499869

International Journal of Microbiology

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Abstract Background Methods Results Discussion Conclusion Abbreviations Data Availability Ethical Approval Conflicts of Interest Authors’ Contributions Acknowledgments Supplementary Materials References Copyright Related Articles

Review Article | Open Access

Volume 2021 | Article ID 1499869 | https://doi.org/10.1155/2021/1499869

Global Prevalence of Yersinia enterocolitica in Cases of Gastroenteritis: A Systematic Review and Meta-Analysis

Seyed Mohammad Riahi,¹Ehsan Ahmadi,²and Tayebeh Zeinali³

Academic Editor: Luigi Santacroce

Received27 Apr 2021

Revised15 Aug 2021

Accepted23 Aug 2021

Published03 Sept 2021

Abstract

The prevalence of Yersinia enterocolitica in gastroenteritis is often underestimated. It relates considerably to morbidity and medical expenses around the world. Understanding the cause of gastroenteritis leads to making the appropriate treatment decisions. We systematically searched PubMed, Science Direct, Embase, and Scopus to identify all published studies between Jan. 1, 2000, and Dec. 31, 2019, to assess the prevalence of Y. enterocolitica in gastroenteritis patients. A total of 5039 articles were identified that lead to the extraction of data from 47 of them. The pooled prevalence of Y. enterocolitica in cases of gastroenteritis was estimated as 1.97% (1.32–2.74%) in the culture method and 2.41% (1.07–4.22%) in the molecular method. Among the biotypes of Y. enterocolitica, 1A (62.48%) and 1B (2.14%) had the most and least prevalence, respectively. Serotype O3 Y. enterocolitica with 39.46% had the highest and O5,27 with 0.0% had the least prevalence in gastroenteritis cases. In conclusion, the findings of this systematic review show that Y. enterocolitica is prevalent in gastroenteritis in all age groups. Serotypes O3 and O9 of Y. enterocolitica had the highest prevalence and O5,27 had the least prevalence in diarrheal patients. The prevalence of Y. enterocolitica was similar in both gender and different seasons. It should be noted that to determine the role of the organism, more studies are needed especially in food-borne diseases.

1. Background

Yersiniosis is caused by Gram-negative bacteria Yersinia enterocolitica (Y. enterocolitica) and Y. pseudotuberculosis. Although Y. enterocolitica is a frequent cause of human infection especially in developed countries of temperate zones, Y. pseudotuberculosis human infection is rare [1]. It mainly caused a gastrointestinal infection in humans. Additionally, Y. enterocolitica can cause other clinical manifestations including mesenteric lymphadenitis, endocarditis, and predominantly infects children [2]. Yersiniosis is the third cause of notifiable bacterial zoonosis in the European Union after campylobacteriosis and salmonellosis [3]. Y. enterocolitica is a psychrotrophic organism that can replicate at temperatures ranging from 0 to 44°C. As such, the organism can replicate in the refrigerator and survives in frozen foods and liquids for long periods. Peritrichous flagella causes the motility of Y. enterocolitica. Motility is temperature dependent, as the bacterium is motile at 25°C but is not motile when it grows at 37°C. Pathogenesis of Y. enterocolitica also depends on temperature. The invasive proteins of Y. enterocolitica produce at environmental temperatures of less than 28°C and under acidic conditions at 37°C. The expression of virulence factors necessary to infection initiates by the gradual increase of temperature within the host [2]. Infections caused by Y. enterocolitica pathogenic strains do not belong to a specific age group, but the clinical manifestation is frequently observed in children and younger adults. Adults can be asymptomatic carriers of infection [4]. Fever, abdominal pain, and diarrhea are the common symptoms of yersiniosis in children [2]. The bacterium was isolated from domestic and wild animals. Pigs are regarded as the reservoir of the pathogen [5], but high titers of anti-Yersinia antibodies in domestic animals, such as cattle, goats, and sheep revealed that there are other possible sources [6]. The main method of human infection is through consumption of contaminated food especially raw or undercooked ones [2] though drinking of contaminated water, close exposure to pet animals, and blood transfusion have also been mentioned [2, 7]. Y. enterocolitica had several biotypes and serotypes. Virulent isolates of Y. enterocolitica are attributed to certain biotypes and serotypes. Among the six known biotypes (including 1A, 1B, 2, 3, 4, and 5), 1A is reported as an nonpathogenic biotype in healthy people. Y. enterocolitica serotypes O3, O8, O9, and O5. 27 were isolated from most cases of human yersiniosis [2]. The most serious disease is caused by serotype O8 with extensive ulceration of the gastrointestinal tract and sometimes death of the patients [8].

Patients may defecate Y. enterocolitica for 90 days after the recovery, which shows the importance of early detection of the bacterium in order to prevent transmission and possible outbreak [9]. In order to detect the Y. enterocolitica, a culture method and molecular assays were developed. The conventional culture method is time-consuming and has false-negative results while PCR is not only a sensitive and specific detection method but also is able to identify the pathogenic isolates and further characterization of the isolates [4]. Around the world, there is limited information about the prevalence of yersiniosis due to the clinical presentation of the disease as gastroenteritis so the diagnosis and treatment mainly depend on the clinicians and not on the microbiological culture. The aim of the present study was to estimate the global prevalence of yersiniosis in cases of gastroenteritis. Moreover, the main biotypes and serotypes were determined. The existing data and knowledge were synthesized through a systematic literature review and meta-analysis.

2. Methods

2.1. Search Strategy and Study Selection

A systematic review was performed in PubMed, Science Direct, Embase, and Scopus to identify all published studies between Jan 1, 2000, and Dec 31, 2019, with the search keywords of “gastroenteritis,” “Yersinia enterocolitica,” and “yersiniosis” and related terms without any language restriction. The searched keywords were extracted from the Medical Subject Headings thesaurus. The search strategy was presented in the supplementary file. Titles and abstracts of relevant original articles after the removal of duplicates were screened by two independent reviewers (TZ and EA). The bibliographies of the included articles were hand-searched for additional references. Gray literature was searched by using Google Scholar. PRISMA guidelines were used to perform the systematic reviews.

Selection of studies was carried out by the following criteria: primary research studies including original article either published or in press; studies with a cross-sectional design; case group of case-control studies; studies including detection of Y. enterocolitica on the samples based on culture or PCR; patients having the symptoms of gastroenteritis; studies performed in a specified region or country; having a known number of sample size; and studies with available full texts. Studies with confusing text or incomprehensible analyses that did not report the sample size and number or percent of positive cases toward Y. enterocolitica were excluded. Reviews, letters, or editorial articles without original data were also excluded.

2.2. Data Extraction and Risk of Bias Assessment

A standard dedicated data extraction form was designed in Excel software. Two authors (TZ and SMR) extracted data independently. If provided, the following data were extracted from each study: bibliographic characteristics, including first author, year of publication, start and end year of the study, study design (cross-sectional or case-control), and country (income, HDI and WHO region); population characteristics, including the age of the participants (mean ± standard deviation (SD), minimum and maximum), gender, and total number of tested patients; methodological information, including diagnostic method, number of patients positive for Y. enterocolitica in culture and PCR separately, season of sampling, biotypes and some prevalent pathogenic serotypes of isolated Y. enterocolitica, and geographic location (latitude and longitude). We included samples with both Y. enterocolitica and another pathogen detected (e.g., E. coli or viruses).

Data were stratified by the diagnostic method and age. Regarding age, data were stratified into four categories: younger than 6 years, 6 to 18 years old, 18 to 59 years old, and more than 60 years old. As an indicator of development and epidemiological context, income, WHO region, and human development index were used to categorize the data on the basis of the country in which the study was performed. The eligible studies were qualified independently by two authors (TZ and EA) according to the Joanna Briggs Institute [10].

2.3. Statistical Analysis

In the current study, random-effect models were used for estimating pooled prevalence and 95% confidence intervals (95% CI). Metaprop command was used in Stata software. Pooled prevalence was calculated using a Freeman–Tukey double arcsine transformation [11, 12]. Heterogeneity among studies was examined by I², Cochran’s Q. I2 index ranges between 0 and 100 percent and I² ˃ 70% was considered heterogeneous [13, 14]. A Forest plot in the random-effects model was applied to show pooled prevalence. Subgroup analysis and metaregression were done to identify the sources of heterogeneity [15]. Univariate metaregression analysis was used for assessing the effect of publication year, human development index, geographical location (longitude/latitude), and quality score on the prevalence of Y. enterocolitica. In a subgroup analysis, we estimated the prevalence of Y. enterocolitica in different age groups, type of diagnostic method, study’s type, income, and WHO regions. Publication bias was not examined because the aim of the study is not to determine the association between exposures and outcome [15]. The significance level was considered 0.05 in all analyses. All analyses were done by using STATA 13 (STATA Corp., College Station, Texas). In the metaregression, value <0.1 was considered as a significant level due to the little range of prevalence of Y. enterocolitica and the rare nature of the organism.

3. Results

3.1. Study Characteristics

A total of 5039 articles were identified of which 4845 were not duplicates. According to the title and abstract, 202 articles were included and assessed for eligibility by full texts (Figure 1). From these, 49 articles passed the quality assessment and data were extracted from 47 of them. The final extracted data included 25 countries from all WHO regions (eight from the Americas, 17 from Europe, ten from Eastern Mediterranean, five from Africa, and seven from Western Pacific) except for the South-East Asia region. From these 47 studies, the prevalence of Y. enterocolitica by culture diagnosis method in cases of gastroenteritis was estimated as 1.97% (95% CI 1.32–2.74; I² = 99.19%; test for heterogeneity) (Figure 2(a)). However, by the PCR method the estimate of pooled prevalence for Y. enterocolitica was 2.41 (95% CI 1.07–4.22; I² = 98.39%; test for heterogeneity) (Figure 2(b)). There was significant heterogeneity among the included studies. Table 1 shows the pooled prevalence of Y. enterocolitica by culture and PCR method according to the countries. The highest prevalence of Y. enterocolitica in culture and PCR method was in Madagascar (16.56%). The lowest prevalence of Y. enterocolitica in culture and PCR method was in Australia (0.00%) and Brazil (0.00%), respectively. Table 2 shows the main characteristics of the included studies.

(a)

(b)

3.2. Subgroup Analysis

The type of study did not change the pooled prevalence of Y. enterocolitica, as in the culture method, the pooled prevalence in the cross-sectional and case-control studies is 2.20 and 1.22, respectively (random test for heterogeneity ) (Figure 3(a)). The pooled prevalence of Y. enterocolitica by the PCR method in the cross-sectional and case-control studies is 2.28 and 4.44, respectively (Figure 3(b)). The pooled prevalence of Y. enterocolitica was decreased by the increase in the income of the countries . The pooled prevalence of Y. enterocolitica in low- and high-income countries was 7.17 and 1.35 in culture (Figure 4(a)) and 16.56 and 0.36 in PCR method (Figure 4(b)), respectively. The source of heterogeneity of included studies is income. According to age, the prevalence was not significantly different in younger than 6 years, 6–18 years, and 18–59 years (1.75%; 0.96–2.54; for culture and 1.84%; 0.49–3.19; for PCR; I² = 0.0%) (Figure 5(a)). By gender of participants and season of sampling, the prevalence was similar ( and , respectively) (Figure 5(a)). According to the biotype of Y. enterocolitica isolates, 1A (62.48%; 95% CI 27.56–91.77) and 1B (2.14%; 95% CI 0.04–6.14) had the most and least prevalence, respectively. Among the investigated serotypes of Y. enterocolitica isolates, O3 with 39.46% had the highest and O5,27 with 0.0% had the least prevalence (Figure 5(b)).

(a)

(b)

(a)

(b)

(a)

(b)

3.3. Metaregression

According to Figures 6(a) and 6(b), by the increase of publication year, the prevalence did not have any significant change ( for culture and for PCR). Countries with higher HDI had a lower prevalence of Y. enterocolitica ( for culture and for PCR) (Figures 6(c) and 6(d)). Longitude had not any significant effect on the prevalence of Y. enterocolitica ( for culture and for PCR) (Figures 6(e) and 6(f)). The prevalence of Y. enterocolitica increased slightly with increasing latitude but was not statistically significant in the culture method; in contrast, its prevalence was decreased with the increasing latitude in the PCR method (Figures 6(g) and 6(h)). Metaregression for quality assessment and prevalence was carried out and no relation was observed ( for culture and for PCR).

(a)

(b)

(c)

(d)

(e)

(f)

(g)

(h)

4. Discussion

In the current meta-analysis, we provided the first estimates of the global prevalence of yersiniosis in cases of gastroenteritis. Based on the culture isolation of Y. enterocolitica, Africa [1, 26, 39, 40, 44] and Eastern Mediterranean [17, 22, 42, 46, 48, 53, 56–58] WHO regions had the first and second rank of prevalence of the bacterium, while Europe [4, 16, 19, 21, 24–26, 28, 29, 33–36, 38, 45, 49, 50, 54] had the least prevalence of Y. enterocolitica in gastroenteritis cases. Yersiniosis had a global prevalence and is a reportable disease in some countries, such as Denmark, Norway, and 38 states of USA [59, 60]. According to PCR detection, Africa and Western Pacific [3, 9, 18, 23, 27, 37] had the most, and the Americas [20, 30–32, 41, 51, 52, 55] had the least prevalence of Y. enterocolitica. In the present study, the highest prevalence of Y. enterocolitica in culture and PCR method was in Madagascar (16.56%). The lowest prevalence of Y. enterocolitica in culture and PCR method was in Australia (0.00%) and Brazil (0.00%), respectively, in the current study. Bublitz et al. (2014) reported that the prevalence of Y. enterocolitica is 16.56% in Madagascar and Assiss et al. (2014) reported it is 0.0% in Brazil. In the United States (US), 0.33 per 100000 individuals were infected by Yersinia during 1996 to 2012 in the general population according to Food-borne Diseases Active Surveillance Network, 2012 [61]. In Denmark, Y. enterocolitica was reported as a common cause of bacterial diarrheal disease with 4.9 cases per 100,000 inhabitants in 2016 [62]. Among developed countries, food-borne yersiniosis was higher in most European countries than US [63, 64]. The prevalence of Y. enterocolitica was higher in gastroenteritis patients than in the general healthy population. In the present study, income was the origin of heterogeneity among included studies. As, in the low-income countries, Y. enterocolitica was more prevalent than high-income ones. This can be related to considering hygiene principles. Human yersiniosis is commonly caused by Y. enterocolitica [59]. Yersiniosis caused self-limiting diarrhea that sometimes may be bloody in children younger than four years old. However, fever and abdominal pain accompanied by diarrhea and/or vomiting were reported in older children and adults [9]. The clinical presentation of gastrointestinal disease can be different based on the age and immune status of the host [2]. Diagnosis of yersiniosis is done by isolation of the microbe from human feces or blood or following removal of the appendix, mistakenly [59], although the culture of the bacterium is not a usual procedure for gastrointestinal patients in most hospitals that may lead to underestimates of yersiniosis [59].

Age was not a significant factor regarding gastroenteritis caused by Y. enterocolitica in the current study. Some studies reported that younger children are more susceptible to diarrhea caused by Y. enterocolitica [9, 27, 39, 40]. Al Jarousha et al. reported higher isolation of Y. enterocolitica from diarrheic children with the age of one to six years than children less than one year and more than 6 years [48]. Y. enterocolitica had different biotypes and serotypes. The insignificant effect of age may be due to infection of children, adults, and the elderly with different serotypes that may not necessarily create immunity to other serotypes [65]. Furthermore, limited studies were performed on older ages. Gender difference was not seen in the current study. Men and women did not show different symptoms in yersiniosis [40, 49]. A seasonal variation was not seen in the present study. Some studies reported more cases during the cooler season [46, 66], but according to the report of the European Centre for Disease Prevention and Control, no seasonal pattern was observed for yersiniosis for a period of three years [67]. Some other studies did not also report a significant difference between seasons [9, 47, 68], 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 [65].

Among the six biotypes of Y. enterocolitica, 1A was the most prevalent biotype. As biotype 1A is a nonpathogenic biotype mostly found in the environment, it had a higher prevalence in most studies and was isolated from human, animals, and gastroenteritis [49, 50, 69]. Among the virulent biotypes, biotypes II and III had a prevalence of 33.06% and 12.89%, respectively. In the current study, serotypes O3 and O9 had the most prevalence. They were reported in other studies as the main serotypes of Y. enterocolitica in diarrheal patients [4, 39, 43]. Serotype O8 was the third serotype in gastroenteritis patients of the current study. It was observed as the most pathogenic serotype in biotype 1B that was correlated to four of six food poisoning outbreaks in the US [41]. A total of 18% of the patients were infected with pathogenic Y. enterocolitica [49]. A total of 0.6% of acute diarrhea cases were because of Y. enterocolitica and all of them were serotype O3 [54]. In Nigeria, Y. enterocolitica bioserotype 2/O9 was the only isolated pathogenic in human samples. Bioserotype 4/O3 of Y. enterocolitica is the major isolated one from humans globally [63] and was isolated in some European countries, including Denmark, Italy, Belgium, Spain, Finland, and Sweden [50, 64]. According to Stephen et al., biotypes II and IV were only diagnosed in diarrheal patients, but strains of biotype 1A were isolated from both asymptomatic and diarrheal patients which shows the biotype 1A is not the etiologic agent of gastroenteritis [45]. Y. enterocolitica serotype O3 was commonly isolated from children, whereas Y. enterocolitica serotype O9 was frequently isolated from adults (≥40 years of age). Exposure of children to Y. enterocolitica O3 may conceivably provide some immunity against acute infections due to the same serotype during their life, but not necessarily from other serotypes [65]. According to HDI, the prevalence of Y. enterocolitica was increased with the decrease of HDI that can be related to a higher level of hygienic standards in these countries. In the current study, latitude had a different effect on the prevalence of Y. enterocolitica in culture and molecular diagnosis. Y. enterocolitica is a psychrotrophic bacterium and can replicate in cooler climates [59]. A study on seroprevalence of Y. enterocolitica in wild boars showed that the prevalence was higher in cold climates [70]. Similar results were seen in pigs [71]. The viable organisms were detected in the culture method, but in PCR, the not viable ones were also detected which may be the reason for the higher prevalence of Y. enterocolitica in the temperate zone in the molecular diagnosis compared to culture. The range of prevalence was narrow in the current study which may be the reason for different observations in culture and PCR method, although, in culture, it was not significant.

4.1. Strengths and Limitations

This was the first systematic review and meta-analysis to gain a global prevalence of Y. enterocolitica in gastroenteritis patients. We considered both the culture and PCR isolation of the organism. There was high heterogeneity among the studies especially due to income but mostly reduced by the application of subgroup analysis and metaregression. Additionally, this study has some limitations that must be acknowledged: first, in some analyses, the number of included studies was low, especially in the older ages (e.g., >60 years); second, there were not sufficient related studies for assessing risk factors; third, the age of participants was not reported clearly in some included studies. Forth, the transmission method of the organism was not reported in the studies. However, estimating the global prevalence of Y. enterocolitica is challenging as most of the studies were performed in hospitalized patients with gastrointestinal symptoms. We encourage further studies, especially in the western Pacific and southeast WHO regions to produce and share local data about yersiniosis. An update of our study should be done due to the availability of additional data.

5. Conclusion

In conclusion, the findings of this systematic review show that Y. enterocolitica is prevalent in gastroenteritis in all age groups. Y. enterocolitica was not prevalent in high-income countries and countries with higher HDI values. Serotypes O3 and O9 of Y. enterocolitica had the highest prevalence and O5,27 had the least prevalence in diarrheal patients. The prevalence of Y. enterocolitica was similar in both gender and different seasons. It should be noted that to determine the role of the organism, more studies are needed especially in food-borne diseases.

Abbreviations

Y. enterocolitica:	Yersinia enterocolitica
PRISMA:	Preferred Reporting Items for Systematic Reviews and Meta-Analyses
TZ:	Tayebeh Zeinali
SMR:	Seyed Mohamad Riahi
EA:	Ehsan Ahmadi
HDI:	Human development index
WHO:	World Health Organization
SD:	Standard deviation
PCR:	Polymerase chain reaction
Fig:	Figure
USA:	United States of America.

Data Availability

The data are available from the corresponding author on reasonable request.

Ethical Approval

The study was approved by the ethical committee of Birjand University of Medical Sciences (Ir.bums.rec.1399.176).

Conflicts of Interest

The authors declare that there are no conflicts of interest about the results of the present study.

Authors’ Contributions

SMR, EA, and TZ designed the research. SMR, EA, and TZ conducted the meta-analysis and drafted the manuscript. SMR and TZ analyzed the data. SMR, EA, and TZ revised the manuscript. All the authors read and approved the final manuscript.

Acknowledgments

The authors acknowledge the research and technology deputy of Birjand University of Medical Sciences for support of this study (Grant no. 5434).

Supplementary Materials

The search strategy is presented in the supplementary material. (Supplementary Materials)

References

A. E. J. Okwori, P. O. Martínez, M. Fredriksson-Ahomaa, S. E. Agina, and H. Korkeala, “Pathogenic Yersinia enterocolitica 2/O : 9 and Yersinia pseudotuberculosis 1/O : 1 strains isolated from human and non-human sources in the Plateau State of Nigeria,” Food Microbiology, vol. 26, no. 8, pp. 872–875, 2009.
View at: Publisher Site | Google Scholar
E. J. Bottone, “Yersinia enterocolitica: revisitation of an enduring human pathogen,” Clinical Microbiology Newsletter, vol. 37, no. 1, pp. 1–8, 2015.
View at: Publisher Site | Google Scholar
R. Duan, J. Liang, J. Zhang et al., “Prevalence of Yersinia enterocolitica Bioserotype 3/O : 3 among children with Diarrhea, China, 2010–2015,” Emerging Infectious Diseases, vol. 23, no. 9, pp. 1502–1509, 2017.
View at: Publisher Site | Google Scholar
M. Bucher, C. Meyer, B. Grötzbach, S. Wacheck, A. Stolle, and M. Fredriksson-Ahomaa, “Epidemiological data on pathogenic Yersinia enterocolitica in southern Germany during 2000–2006,” Foodborne Pathogens and Disease, vol. 5, no. 3, pp. 273–280, 2008.
View at: Publisher Site | Google Scholar
M. Fredriksson-Ahomaa, A. Stolle, and H. Korkeala, “Molecular epidemiology of Yersinia enterocolitica infections,” FEMS Immunology and Medical Microbiology, vol. 47, no. 3, pp. 315–329, 2006.
View at: Publisher Site | Google Scholar
K. Nikolaou, A. Hensel, C. Bartling et al., “Prevalence of anti-Yersinia outer protein antibodies in goats in lower saxony,” Journal of Veterinary Medicine Series B, vol. 52, no. 1, pp. 17–24, 2005.
View at: Publisher Site | Google Scholar
S. Boqvist, H. Pettersson, Å. Svensson, and Y. Andersson, “Sources of sporadic Yersinia enterocolitica infection in children in Sweden, 2004: a case-control study,” Epidemiology and Infection, vol. 137, no. 6, pp. 897–905, 2008.
View at: Publisher Site | Google Scholar
L. A. Lee, J. Taylor, G. P. Carter, B. Quinn, J. J. Farmer, and R. V. Tauxe, “Yersinia enterocolitica O : 3: an emerging cause of pediatric gastroenteritis in the United States,” Journal of Infectious Diseases, vol. 163, no. 3, pp. 660–663, 1991.
View at: Publisher Site | Google Scholar
H. Zheng, Y. Sun, S. Lin, Z. Mao, and B. Jiang, “Yersinia enterocolitica infection in diarrheal patients,” European Journal of Clinical Microbiology & Infectious Diseases, vol. 27, no. 8, pp. 741–752, 2008.
View at: Publisher Site | Google Scholar
Z. Munn, S. Moola, D. Riitano, and K. Lisy, “The development of a critical appraisal tool for use in systematic reviews addressing questions of prevalence,” International Journal of Health Policy and Management, vol. 3, no. 3, pp. 123–128, 2014.
View at: Publisher Site | Google Scholar
M. F. Freeman and J. W. Tukey, “Transformations related to the angular and the square root,” The Annals of Mathematical Statistics, vol. 21, no. 4, pp. 607–611, 1950.
View at: Publisher Site | Google Scholar
R. Harris, M. Bradburn, J. Deeks, R. Harbord, D. Altman, and J. Sterne, “Metan: fixed-and random-effects meta-analysis,” STATA Journal, vol. 8, no. 3, 2008.
View at: Publisher Site | Google Scholar
S. M. Riahi and Y. Mokhayeri, “Methodological issues in a meta-analysis,” Current Medical Research and Opinion, vol. 33, no. 10, p. 1813, 2017.
View at: Publisher Site | Google Scholar
J. Higgins, in Assessing Risk of Bias in Included Studies, UK: The Cochrane Collaboration, Wiley-Blackwell, Chichester, UK, 2008.
Y. Mokhayeri, S. M. Riahi, S. Rahimzadeh, M. A. Pourhoseingholi, and S. S. Hashemi-Nazari, “Metabolic syndrome prevalence in the Iranian adult’s general population and its trend: a systematic review and meta-analysis of observational studies,” Diabetes & Metabolic Syndrome: Clinical Research Reviews, vol. 12, no. 3, pp. 441–453, 2018.
View at: Publisher Site | Google Scholar
A. Calderaro, M. Martinelli, M. Buttrini et al., “Contribution of the FilmArray gastrointestinal panel in the laboratory diagnosis of gastroenteritis in a cohort of children: a two-year prospective study,” International Journal of Medical Microbiology, vol. 308, no. 5, pp. 514–521, 2018.
View at: Publisher Site | Google Scholar
Y. A. Hawash, K. A. Ismail, and M. Almehmadi, “High frequency of enteric Protozoan, viral, and bacterial potential pathogens in community-acquired acute diarrheal episodes: evidence based on results of luminex gastrointestinal pathogen panel assay,” Korean Journal of Parasitology, vol. 55, no. 5, pp. 513–521, 2017.
View at: Publisher Site | Google Scholar
X. Wang, J. Wang, H. Sun et al., “Etiology of childhood infectious diarrhea in a developed region of China: compared to childhood diarrhea in a developing region and adult diarrhea in a developed region,” PLoS One, vol. 10, no. 11, Article ID e0142136, 2015.
View at: Publisher Site | Google Scholar
K. Fiedoruk, T. Daniluk, D. Rozkiewicz et al., “Conventional and molecular methods in the diagnosis of community-acquired diarrhoea in children under 5 years of age from the north-eastern region of Poland,” International Journal of Infectious Diseases, vol. 37, pp. 145–151, 2015.
View at: Publisher Site | Google Scholar
F. E. A. Assis, S. Wolf, M. Surek et al., “Impact of Aeromonas and diarrheagenic Escherichia coli screening in patients with diarrhea in Paraná, southern Brazil,” The Journal of Infection in Developing Countries, vol. 8, no. 12, pp. 1609–1614, 2014.
View at: Publisher Site | Google Scholar
I. Hilmarsdóttir, G. E. Baldvinsdóttir, H. Harðardóttir, H. Briem, and S. I. Sigurðsson, “Enteropathogens in acute diarrhea: a general practice-based study in a Nordic country,” European Journal of Clinical Microbiology & Infectious Diseases, vol. 31, no. 7, pp. 1501–1509, 2012.
View at: Publisher Site | Google Scholar
I. A. El Qouqa, M. A. E. Jarou, A. S. A. Samaha, A. S. A. Afifi, and A. M. K. Al Jarousha, “Yersinia enterocolitica infection among children aged less than 12 years: a case-control study,” International Journal of Infectious Diseases, vol. 15, no. 1, pp. e48–e53, 2011.
View at: Publisher Site | Google Scholar
X. Wang, Z. Cui, H. Wang et al., “Pathogenic strains of Yersinia enterocolitica isolated from domestic dogs (Canis familiaris) belonging to farmers are of the same subtype as pathogenic Y. enterocolitica strains isolated from humans and may Be a source of human infection in Jiangsu province, China,” Journal of Clinical Microbiology, vol. 48, no. 5, pp. 1604–1610, 2010.
View at: Publisher Site | Google Scholar
H. C. Maltezou, A. Zafiropoulou, M. Mavrikou et al., “Acute diarrhoea in children treated in an outpatient setting in Athens, Greece,” Journal of Infection, vol. 43, no. 2, pp. 122–127, 2001.
View at: Publisher Site | Google Scholar
S. Huhulescu, R. Kiss, M. Brettlecker et al., “Etiology of acute gastroenteritis in three sentinel general practices,” Infection, vol. 37, no. 2, pp. 103–108, 2007.
View at: Google Scholar
D. C. Bublitz, P. C. Wright, J. R. Bodager, F. T. Rasambainarivo, J. B. Bliska, and T. R. Gillespie, “Epidemiology of pathogenic enterobacteria in humans, livestock, and peridomestic rodents in rural Madagascar,” PLoS One, vol. 9, no. 7, Article ID e101456, 2014.
View at: Publisher Site | Google Scholar
A. Ehara, K. Egawa, F. Kuroki, O. I. a. M. Okawa, and M. Okawa, “Age-dependent expression of abdominal symptoms in patients with Yersinia enterocolitica infection,” Pediatrics International, vol. 42, no. 4, pp. 364–366, 2000.
View at: Publisher Site | Google Scholar
A. Ternhag, A. Törner, A. Svensson, K. Ekdahl, and J. Giesecke, “Short- and long-term effects of bacterial gastrointestinal infections,” Emerging Infectious Diseases, vol. 14, no. 1, pp. 143–148, 2008.
View at: Publisher Site | Google Scholar
C. Gijsbers, M. Benninga, and H. Büller, “Clinical and laboratory findings in 220 children with recurrent abdominal pain,” Acta Paediatrica, vol. 100, no. 7, pp. 1028–1032, 2011.
View at: Publisher Site | Google Scholar
J. R. Rees, M. A. Pannier, A. McNees, S. Shallow, F. J. Angulo, and D. J. Vugia, “Persistent diarrhea, arthritis, and other complications of enteric infections: a pilot survey based on California FoodNet surveillance, 1998–1999,” Complications of Enteric Infections, vol. 38, no. 3, pp. S311–S317, 2004.
View at: Publisher Site | Google Scholar
L. Vernacchio, R. M. Vezina, A. A. Mitchell, S. M. Lesko, A. G. Plaut, and D. W. K. Acheson, “Diarrhea in American infants and young children in the community setting,” The Pediatric Infectious Disease Journal, vol. 25, no. 1, pp. 2–7, 2006.
View at: Publisher Site | Google Scholar
D. A. Talan, G. J. Moran, M. Newdow et al., “Etiology of bloody diarrhea among patients presenting to United States emergency departments: prevalence of Escherichia coli O157 : H7 and other enteropathogens,” Clinical Infectious Diseases, vol. 32, no. 4, pp. 573–580, 2001.
View at: Publisher Site | Google Scholar
M. A. S. de Wit, M. P. G. Koopmans, L. M. Kortbeek, N. J. van Leeuwen, J. Vinje, and Y. T. H. P. van Duynhoven, “Etiology of gastroenteritis in sentinel general practices in the Netherlands,” Clinical Infectious Diseases, vol. 33, pp. 280–288, 2001.
View at: Google Scholar
C. Karsten, S. Baumgarte, A. W. Friedrich et al., “Incidence and risk factors for community-acquired acute gastroenteritis in north-west Germany in 2004,” European Journal of Clinical Microbiology & Infectious Diseases, vol. 28, no. 8, pp. 935–943, 2009.
View at: Publisher Site | Google Scholar
B. Svenungsson, A. Lagergren, E. Ekwall et al., “Enteropathogens in adult patients with diarrhea and healthy control subjects: a 1-year prospective study in a Swedish clinic for infectious diseases,” Clinical Infectious Diseases, vol. 30, no. 5, pp. 770–778, 2000.
View at: Publisher Site | Google Scholar
B. Olesen, J. Neimann, B. Böttiger et al., “Etiology of diarrhea in young children in Denmark: a case-control study,” Journal of Clinical Microbiology, vol. 43, no. 8, pp. 3636–3641, 2005.
View at: Publisher Site | Google Scholar
M. I. Sinclair, M. E. Hellard, R. Wolfe, T. Z. Mitakakis, K. Leder, and C. K. Fairley, “Pathogens causing community gastroenteritis in Australia,” Journal of Gastroenterology and Hepatology, vol. 20, no. 11, pp. 1685–1690, 2005.
View at: Publisher Site | Google Scholar
A. Jansen, K. Stark, J. Kunkel et al., “Aetiology of community-acquired, acute gastroenteritis in hospitalised adults: a prospective cohort study,” BMC Infectious Diseases, vol. 8, no. 1, p. 143, 2008.
View at: Publisher Site | Google Scholar
A. E. J. Okwori, G. O. A. Agada, A. O. Olabode, S. E. Agina, E. S. Okpe, and J. Okopi, “The prevalence of pathogenic Yersinia enterocolitica among diarrhea patients in Jos, Nigeria,” African Journal of Biotechnology, vol. 6, no. 8, pp. 1031–1034, 2007.
View at: Google Scholar
A. I. Omoigberale and P. O. Abiodun, “Prevalence of Yersinia enterocolitica among diarrhoeal patients attending university of Benin teaching hospital, Benin city, Nigeria,” Sahel Medical Journal, vol. 5, no. 4, pp. 182–185, 2002.
View at: Publisher Site | Google Scholar
N. M. Abdel-Haq, R. Papadopol, B. Asmar, and W. Brown, “Antibiotic susceptibilities of Yersinia enterocolitica recovered from children over a 12-year period,” International Journal of Antimicrobial Agents, vol. 27, no. 5, pp. 449–452, 2006.
View at: Publisher Site | Google Scholar
C. Perdikogianni, E. Galanakis, M. Michalakis et al., “Yersinia enterocolitica infection mimicking surgical conditions,” Pediatric Surgery International, vol. 22, no. 7, pp. 589–592, 2006.
View at: Publisher Site | Google Scholar
H. Zheng, J. Wang, Y. Sun, and B. Jiang, “Clinical isolation and characterization of Yersinia enterocolitica in China using real-time PCR and culture method,” Digestion, vol. 75, no. 4, pp. 199–204, 2007.
View at: Publisher Site | Google Scholar
N. J. Gasco, M. Vargas, D. Schellenberg, H. Urassa, C. Casals, and E. Kahigwa, “Diarrhea in children under 5 years of age from Ifakara, Tanzania: a case-control study,” Journal of Clinical Microbiology, vol. 38, no. 12, pp. 4459–4462, 2000.
View at: Google Scholar
R. Stephan, S. Joutsen, E. Hofer et al., “Characteristics of Yersinia enterocolitica biotype 1A strains isolated from patients and asymptomatic carriers,” European Journal of Clinical Microbiology & Infectious Diseases, vol. 32, no. 7, pp. 869–875, 2013.
View at: Publisher Site | Google Scholar
E. Garveriani, M. M. Aslani, S. Habibzadeh, and A. Fathi, “Role of Yersinia enterocolitica in acute diarrhea of childern under 5 years old in cold seasons in Ardabil,” Journal of Ardabil University of Medical Sciences, vol. 7, no. 4, pp. 387–391, 2008.
View at: Google Scholar
F. GhasemiKebria, B. Khodabakhshi, H. Kouhsari, M. SadeghiSheshpoli, N. Behnampoor, and S. Livani, “Yersinia enterocolitica in cases of diarrhea in Gorgan, northern Iran,” Medical Laboratory Journal, vol. 4, no. 1, 2010.
View at: Google Scholar
A. M. K. Al Jarousha, M. A. El Jarou, and I. A. El Qouqa, “Bacterial enteropathogens and risk factors associated with childhood diarrhea,” Indian Journal of Pediatrics, vol. 78, no. 2, pp. 165–170, 2011.
View at: Publisher Site | Google Scholar
E. Huovinen, L. M. Sihvonen, K. Haukka, A. Siitonen, M. Kuusi, and M. Kuusi, “Symptoms and sources of Yersinia enterocolitica-infection: a case-control study,” BMC Infectious Diseases, vol. 10, no. 1, p. 122, 2010.
View at: Publisher Site | Google Scholar
L. M. Sihvonen, K. Haukka, K. Haukka, M. Kuusi, M. J. Virtanen, and A. Siitonen, “Yersinia enterocolitica and Y. enterocolitica-like species in clinical stool specimens of humans: identification and prevalence of bio/serotypes in Finland,” European Journal of Clinical Microbiology & Infectious Diseases, vol. 28, no. 7, pp. 757–765, 2009.
View at: Publisher Site | Google Scholar
P. P. Orlandi, T. Silva, G. F. Magalhães et al., “Enteropathogens associated with diarrheal disease in infants of poor urban areas of Porto Velho, Rondônia: a preliminary study,” Memórias do Instituto Oswaldo Cruz, vol. 96, no. 5, pp. 621–625, 2001.
View at: Publisher Site | Google Scholar
N. M. Abdel-Haq, B. I. Asmar, W. M. Abuhammour, and W. J. Brown, “Yersinia enterocolitica infection in children,” The Pediatric Infectious Disease Journal, vol. 19, no. 10, pp. 954–958, 2000.
View at: Publisher Site | Google Scholar
L. F. Nimri and M. Meqdam, “Enteropathogens associated with cases of gastroenteritis in a rural population in Jordan,” Clinical Microbiology and Infections, vol. 10, no. 7, pp. 634–639, 2004.
View at: Publisher Site | Google Scholar
S. Maraki, A. Georgiladakis, Y. Tselentis, and G. Samonis, “A 5-year study of the bacterial pathogens associated with acute diarrhoea on the island of Crete, Greece, and their resistance to antibiotics,” European Journal of Epidemiology, vol. 18, pp. 85–90, 2003.
View at: Publisher Site | Google Scholar
M. E. Torres, M. C. Pı́rez, F. Schelotto et al., “Etiology of children’s diarrhea in montevideo, Uruguay: associated pathogens and unusual isolates,” Journal of Clinical Microbiology, vol. 39, no. 6, pp. 2134–2139, 2001.
View at: Publisher Site | Google Scholar
M. M. Dallal, M. R. Khorramizadeh, and K. MoezArdalan, “Occurrence of enteropathogenic bacteria in children under 5 years with diarrhoea in south Tehran,” Eastern Mediterranean Health Journal, vol. 12, no. 6, pp. 792–797, 2006.
View at: Google Scholar
M. M. Soltan-Dallal and K. Moezardalan, “Frequency of Yersinia species infection in paediatric acute diarrhoea in Tehran,” Eastern Mediterranean Health Journal, vol. 10, no. 1, pp. 152–158, 2004.
View at: Google Scholar
A. A. Soleymani-Rahbar, F. Fayaz, A. Zargarizadeh, and R. Nikazma, “Surveying the prevalence and pattern of antimicrobial resistance of Yersinia enterocolitica among diarrheal children attending health care centers in Qom,” Iranian Journal of Clinical Infectious Diseases, vol. 2, no. 3, pp. 143–147, 2007.
View at: Google Scholar
N. Drummond, B. P. Murphy, T. Ringwood, M. B. Prentice, J. F. Buckley, and S. Fanning, “Yersinia enterocolitica: a brief review of the issues relating to the zoonotic pathogen, public health challenges, and the pork production chain,” Foodborne pathogens and disease, vol. 9, no. 3, pp. 179–189, 2012.
View at: Publisher Site | Google Scholar
A. Chakraborty, K. Komatsu, M. Roberts et al., “The descriptive epidemiology of yersiniosis: a multistate study, 2005–2011,” Public Health Reports, vol. 130, no. 3, pp. 269–277, 2015.
View at: Publisher Site | Google Scholar
Foodborne Diseases Active Surveillance Network (FoodNet), “Incidence and trends of infection with pathogens transmitted commonly through food —foodborne diseases active surveillance Network, 10 U.S. Sites, 1996–2012,” Morbidity and Mortality Weekly Report, vol. 62, no. 15, pp. 283–287, 2013.
View at: Google Scholar
(ECDC) European Centre for Disease Prevention and Control Yersiniosis, ECDC Annual Epidemiological Report for 2016, ECDC, Stockholm, Sweden, 2018.
M. Fredriksson-Ahomaa, N. Lindstrom, and H. Korkeala, Pathogens and Toxins in Food: Challenges and Interventions, ASM Press, Washington, DC, USA, 2010.
A. Rahman, T. S. Bonny, S. Stonsaovapak, and C. Ananchaipattana, “Yersinia enterocolitica: epidemiological studies and outbreaks,” Journal of Pathogens, vol. 2011, Article ID 239391, 11 pages, 2011.
View at: Publisher Site | Google Scholar
B. M. Rosner, K. Stark, and D. Werber, “Epidemiology of reported Yersinia enterocolitica infections in Germany, 2001–2008,” BMC Public Health, vol. 10, no. 1, p. 337, 2010.
View at: Publisher Site | Google Scholar
S. M. Ray, S. D. Ahuja, P. A. Blake, M. M. Farley, M. Samuel, and T. Rabatsky-Ehr, “Population-based surveillance for yersiniaenterocolitica infections in FoodNet sites, 1996–1999: higher risk of disease in infants and minority populations,” Clinical Infectious Diseases, vol. 38, no. 3, pp. 181–189, 2004.
View at: Publisher Site | Google Scholar
(ECDC) European Centre for Disease Prevention and Control, Surveillance Report: Annual Epidemiological Report on Communicable Diseases in Europe 2010, (ECDC) European Centre for Disease Prevention and Control, Stockholm, Sweden, 2010.
M. M. Soltan-Dallal, “Diarrhea caused by enteropathogenic bacteria in children,” Archives of Iranian Medicine, vol. 4, no. 4, pp. 201–203, 2001.
View at: Publisher Site | Google Scholar
N. Bhagat and J. S. Virdi, “The Enigma of Yersinia enterocolitica biovar 1A,” Critical Reviews in Microbiology, vol. 37, no. 1, pp. 25–39, 2011.
View at: Publisher Site | Google Scholar
M. Arrausi-Subiza, X. Gerrikagoitia, V. Alvarez, J. C. Ibabe, and M. Barra, “Prevalence of Yersinia enterocolitica and Yersinia pseudotuberculosis in wild boars in the Basque Country, northern Spain,” Acta Veterinaria Scandinavica, vol. 58, no. 4, 2016.
View at: Publisher Site | Google Scholar
J. Liang, X. Wang, Y. Xiao et al., “Prevalence of Yersinia enterocolitica in pigs slaughtered in Chinese abattoirs,” Applied and Environmental Microbiology, vol. 78, no. 8, pp. 2949–2956, 2012.
View at: Publisher Site | Google Scholar

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Copyright © 2021 Seyed Mohammad Riahi 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.

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