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Table of Contents
Year : 2020  |  Volume : 3  |  Issue : 2  |  Page : 49-57

Reservoirs of infection with shiga toxin-producing Escherichia coli in Iran: Systematic review

1 Ali-Asghar Clinical Research Development Center, Iran University of Medical Sciences, Tehran, Iran
2 Department of Epidemiology, School of Public Health, Shahid Beheshti University of Medical Sciences, Tehran, Iran
3 Kidney Centre of Excellence, Al Jalila Children's Hospital, Dubai, United Arab Emirates
4 Department of Microbiology, Faculty of Medicine, Kurdistan University of Medical Sciences, Sanandaj, Iran
5 Department of Pediatrics, Faculty of Medicine, Kurdistan University of Medical Sciences, Sanandaj, Iran

Date of Submission13-Feb-2020
Date of Decision15-May-2020
Date of Acceptance18-Jul-2020
Date of Web Publication31-Dec-2020

Correspondence Address:
Nakysa Hooman
Department of Nephrology, Ali-Asghar Children Hospital, Vahid Dasgerdi Street, Tehran
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Source of Support: None, Conflict of Interest: None

DOI: 10.4103/2589-9309.305897

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Introduction: Shiga toxin-producing Escherichia coli (STEC) infection, an important cause of hemorrhagic colitis and hemolytic uremic syndrome, is associated with high mortality and morbidity. The chief sources of STEC are contaminated food and drinking water. Aim: This study aimed to identify relevant sources of STEC transmission in Iran. Methods: Search engines of PubMed, EMBASE, OVID, SCOPUS, Web of Sciences, Google Scholar, and Iranian databases of health.barakatkns.com, IranMedex, MagIran, SID, dociran, PDFiran, and ganj.irandoc were used to review studies published about food and animal sources of STEC in Iran between 1985 and 2018. Quality and risk of bias were assessed to estimate point prevalence and proportions, which are reported with their 95% confidence intervals (CIs). Results: A total of 58 articles describing 17480 specimens were eligible for inclusion in the final analysis. Most studies, except two case control studies, had a cross-sectional design. While 39 studies had good quality, the remainder had poor quality with low to moderate risk of bias. Of 6779 samples positive for E. coli, 1587 were positive for STEC; the pooled prevalence of STEC was 5.7% (95% CI, 3.4–8.6) in food studies and 10.2% (95% CI, 7.0–13.9) in animal studies. Conclusion: A significant proportion of food and animal samples in Iran are contaminated with STEC. Registration Number: PROSPERO 2016: CRD42016033019.

Keywords: Dairy, enterohemorrhagic Escherichia coli, meat, shiga-toxigenic Escherichia coli, vegetables

How to cite this article:
Hooman N, Khodadost M, Bitzan M, Ahmadi A, Nakhaie S, Naghshizadian R. Reservoirs of infection with shiga toxin-producing Escherichia coli in Iran: Systematic review. Asian J Pediatr Nephrol 2020;3:49-57

How to cite this URL:
Hooman N, Khodadost M, Bitzan M, Ahmadi A, Nakhaie S, Naghshizadian R. Reservoirs of infection with shiga toxin-producing Escherichia coli in Iran: Systematic review. Asian J Pediatr Nephrol [serial online] 2020 [cited 2021 Jun 20];3:49-57. Available from: https://www.ajpn-online.org/text.asp?2020/3/2/49/305897

  Introduction Top

Enterohemorrhagic Escherichia coli (EHEC) may produce shiga toxin (Stx), which mediates the pathogenesis of hemorrhagic colitis (HC) and hemolytic uremic syndrome (HUS). While Stx1, Stx2 and their variants have major role in the pathogenicity of Stx-producing E. coli (STEC), not all STEC serovars and Stx subtypes are disease-causing, and Stx2 is linked to HUS more often than Stx1.[1] The attaching/effacement protein (intimin), encoded by eaeA, that colonizes the host intestine is another STEC virulence factor (VF).[1] Following binding to mammalian cell membrane globotriosyl ceramide (Gb3), Stx is internalized and inhibits protein synthesis in susceptible tissues.[2] Due to their stability in the environment and low inoculum required for infection, STEC O157:H7 and certain other serotypes are contagious, leading to person-to-person transmission and foodborne outbreaks of (hemorrhagic) colitis and HUS.[3]

While 2018 data from FoodNet reported a decline in the incidence of human STEC-O157 infections, indicating the efficacy of targeted control measures, the published incidence of non-O157 STEC infections, detected using culture-independent diagnostic tests, appears to have risen.[4] While early outbreaks of HUS associated with STEC O157:H7 were linked to consumption of undercooked beef,[5],[6] there are other modalities of transmission, e.g., through contaminated lamb meat in a 15-year surveillance study from Sheffield,[7] other foods (poultry, dairy products and vegetables) or drinking water, and by direct animal-to-person and person-to-person transmission.[8],[9] Following the German outbreak by the novel Stx-producing enteroaggregative hybrid strain O104:H4 in 2011, concerted efforts to expand capacity of testing for new or atypical STEC strains by laboratories from 32 countries[10] has led to implementation of surveillance protocols for early detection of STEC-contaminated sources as well as reporting of cases of post-diarrheal HUS within 24 h of presentation to prevent disease outbreaks.[10],[11]

A meta-analysis showed a pooled prevalence estimate of 3.1%–6.3% for STEC serotypes in cattle in Iran.[12] STEC causes a median yearly foodborne disease burden of 1.8 million and 13,000 disability adjusted life years.[13] The WHO-reported incidence of STEC is highest in the Eastern Mediterranean sub-region (156/100,000 population).[14] While this data suggests that Iran is located in a high risk region for STEC transmission, the organism is not considered a health hazard, the illness is not listed in the contagious disease catalogue of the Iranian Ministry of Health and Medical Education, and surveillance measures have not yet been implemented in the country.[15] Since there are no published estimates of the frequency of food contamination with STEC for Iran, the present study was planned to estimate its contamination of various foods, to examine regional differences in the distribution of STEC serotypes and rates of STEC food contamination, to determine the presence of pathogenicity genes in STEC isolates, and to uncover seasonal influences on food contamination.

  Methods Top

Protocols and registration

The study was conducted following the Preferred Reporting Items for Systematic Reviews and Meta-Analysis (PRISMA statements).[16] The protocol for the systematic review was registered on PROSPERO (CRD42016033019; available at http://www.crd.york.ac.uk/PROSPERO/display_record.php?ID=CRD42016033019.[17] Since results on the prevalence of STEC in Iranian children and adults with gastroenteritis in Iran were published recently,[17],[18] we focused on the second part of the primary outcome, i.e., the analysis of the possible sources of STEC infections in Iran.

Eligibility criteria

All studies screening for the presence of STEC or STEC-associated genes in drinking water, dairy products, meat, poultry, and other food items, or in domesticated animals were identified for review. The settings were laboratories, hospitals, outpatient facilities, day-care centers, and military institutions, retail stores, restaurants, dairy product factories, farms, and preserved foods. The search was narrowed by limiting the survey to Iran and to publications between 1985 and 2018. The search was re-run just before the final analyses to capture any relevant study not previously found. We searched in PubMed, Google Scholar, OVID, SCOPUS, Web of Sciences, MagIran, health.barakatkns.com, SID.ir, dociran, PDFiran, Ganj.irandoc, and abstract books of congresses. Additionally, we checked the bibliography of included articles for further references. When reports lacked relevant information, we contacted the authors through email. We used the keywords Shiga-toxigenic, enterohemorrhagic, verotoxin-producing Escherichia coli, dysenteria, diarrhea associated hemolytic-uremic syndrome, bloody diarrhea, E.coli O157:H7, food source, and the equivalent Farsi keywords for Iranian databases.

Study selection and data collection process

Three independent reviewers (AA, RN, SN) reviewed the abstracts to select relevant studies; in case of discrepancies “NH” acted as arbiter. The STROBE statement was used to assess the quality of studies and their eligibility. A quality assessment score out of 22 was determined for each study by assigning a point per STROBE item addressed. Papers with a score of 14/22 or higher were qualified as good/fair and those with <14/22 as poor. “MK” evaluated methods and results of meta-analysis.[19]

Bibliography of study, study center, type of study, study period, sample size, specimens (foods, sources of meat, vegetables, dairy products etc.), animal characteristics, bacterial isolation technique, molecular and serological methods, serotypes of E.coli, technique of STEC identification, and funding sources were recorded. The risk of bias in included studies was assessed using the tool developed by Hoy et al.; studies with scores of 8 or more were considered at “low risk” of bias, 5 or lower at “high risk,” and intermediate scores at “moderate risk” of bias.[20]

Data extraction

The following information was extracted from each study: name of the first author, publication year, type of study, province of study, the setting, the population (food, type of food, animals, type of animals, symptoms, age of animal), source of specimen, sample size, season of sampling, period of study, method of detection, report of STEC, stx genes subtypes, and serotype of E. coli considered as outcome.

Data synthesis and analysis

The prevalence of STEC was calculated from the number of STEC-positive samples over the total sample number in each study. The confidence interval (CI) for the prevalence was calculated as the normal approximation interval at the 95% level, separately for each study and for all studies combined. Prevalence was pooled using the random effects model with the inverse variance method of DerSimonian and Laird for between-study variance estimation.[21] We used both the Chi-squared test and the I-squared statistic to assess heterogeneity between the studies in effect measures (I-squared values greater than 75% indicating substantial heterogeneity). Subgroup analysis was performed for different specimens, various regions, seasons, VFs, and study periods. We used MedCalc statistical software version 15.8 and Metaprop command in Stata software (StataCorp, College Station, TX, USA).

  Results Top

STEC isolation and identification involved growth on Sorbitol-MacConkey agar, followed by serotyping. Most laboratories used any of the recognized techniques such as latex, slide, or tube agglutination, and/or confirmation by polymerase chain reaction (PCR) targeting rfbO157, stx or other STEC-defining genes. [Figure 1] shows the flow diagram of publications reporting food sources and animal reservoirs relevant for human STEC infection, and reasons for exclusion from analysis. We included 58 studies with a total of 17480 specimens; E. coli was isolated from 6779 samples of which 361 were confirmed as STEC. The study design was cross-sectional in all but two case-controls studies. The median time frame of 37 studies was 11 months (range: 2–24 months); duration of the collection period was not indicated in the remaining 21 studies. [Table 1] summarizes findings on foods contaminated with STEC. Antibiotic resistance and VFs were investigated in 13 studies,[22],[34],[39],[45],[53],[55],[56],[58],[59],[60],[61] virulence genes were reported in ten,[28],[31],[33],[43],[45],[57],[62],[63],[64],[65] the detection of STEC was reported in 11 studies,[66],[67] and only one study reported outcomes.[23] Foods examined include meats in 17 articles, vegetables in five, dairy products in eight, and one study reported both meat and dairy products. [Table 2] summarizes studies examining STEC infection (or colonization) in animals. Antibacterial susceptibility was detailed in three animal studies,[22],[59],[60],[78] and STEC virulence genes were presented in three reports.[59],[65],[73] One of the studies, with a sample size of 10, reported an outbreak of bloody diarrhea due to E. coli O157:H7 in a military unit, wherein the investigators randomly tested samples from food items in the kitchen of the military unit.[23]
Figure 1: Flowchart of selection of relevant studies about shiga toxin-producing Escherichia coli

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Table 1: Food source of infection for Shiga toxin producing Escherichia coli in cross-sectional studies

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Table 2: Animal studies for Shiga toxin producing Escherichia coli carriage in cross-sectional studies

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The pooled prevalence of food supply contamination with STEC was 5.7% (95% CI, 3.3%–8.8%; I2 = 96%). The pooled prevalence of STEC in animal reservoirs was 10.2% (95% CI, 7.0%–13.9%; I2 = 95%) [Figure 2]. A subgroup analysis focused on the description of major virulence and pathogenicity factors of 5277 E. coli isolates. We noted that 14.3% were serotyped as O157:H7 (95% CI, 10.1%–19.1%; I2 = 94%). The pooled prevalence of St1 (stx 1) was 13% (95% CI, 8.4%–18.6%; I2 = 97%), of stx 2, 9.9% (95% CI, 6.2%–14.3%; I2 = 96%) and of stx 1 and stx 2 combined, 3.1% (95% CI, 1.7%–4.9%; I2 = 91%). Expression of stx 1 and eaeA genes was observed in 2.9% (95% CI, 1.3%–3.9%; I2 = 94%) cases, stx 2 and eaeA in 1.7% (95% CI, 0.8%–2.9%; I2 = 88%), and stx 1, stx 2 and eaeA in 1.3% (95% CI, 0.7%–2.1%; I2 = 79%) cases. Expression of stx 1, stx 2 and the hemolysine gene ehxA was described in 0.2% (95% CI, 0.1%– 0.3%; I2 = 2.5%), and stx 1, eaeA and ehxA in 0.7% (95% CI, 0.3%–1.3%; I2 = 2.5%).
Figure 2: The pooled prevalence of shiga toxin-producing Escherichia coli in reservoirs in Iranian studies between 1998 and 2018

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The frequency of STEC detection in food varied with the season. STEC was found in 4.0% of all samples (95% CI 0.9%-9%; I2 = 42.5%) collected during spring time, 11% (9.7%–16.2%; I2 = 0) in summer, 4.9% (0.9%–11.8%; I2 = 64.6) in autumn, and 1.1% (0.1%–3.2%, I2 = 0) in winter. The odds of food contamination in the summer were greater than in winter (OR 9.2 [95% CI 2.1–40.8]). The odds of contamination in spring was more than in winter (OR: 3.0 [95% CI 6.5–16.8]).

Subgroup analysis of two time periods “before and after 2010” revealed that asymptomatic animal carrier status and dissemination of the microorganism increased slightly in the second era while the rate of STEC detection in food samples almost tripled. Dairy products had a higher contamination rate (7.6% [95% CI 1.7%–17.0%]) compared to meats (4.6% [CI 2%–8%; I2 = 96]) or vegetables (CI 1%–9%; I2 = 69). Lamb in the meat category, and carrots and salad among vegetables, revealed the highest contamination rates. The odds of STEC infection in animals with diarrhea was 1.4 (95% CI 1.0–2.0; I2 = 23) compared with random animal screening.[61],[66],[69],[75]

Sensitivity analysis

Sensitivity analysis, performed to test the robustness of our results, indicated that the lower pooled prevalence of animals carrying STEC after omitting the study of Shahrani et al.[59] was 9.4% (95% CI 6.9%–11.8%) and the highest pooled prevalence calculated after omitting the study by Tahamtan et al.[62] was 10.9% (95% CI, 7.8%–14.0%). The lower pooled prevalence of food contamination with STEC, calculated after omitting the study by Shakerian et al.,[56] was 5.1% (95% CI 4.0–6.2), and the higher pooled prevalence was 6.4% (95% CI 5.0%–7.8%) after omitting the study by Sami et al.[37] These results made it unlikely that the pooled prevalence was influenced by a particular study.

  Discussion Top

To our knowledge, this is the first comprehensive report on the presence of STEC in food items in Iran. The analysis used data from 31 cross–sectional studies, 84% of which were of good or fair quality. The prevalence of food contamination with STEC amounts to 5.7%. STEC are widely distributed among various foods and domesticated animals raised for meat consumption. This information substantiates that Iran is a high-risk territory for STEC infections in humans. This foodborne pathogen causes sporadic infections and outbreaks of diarrhea, HC and HUS. The latter illnesses are associated with substantial morbidity and mortality.[80],[81] About 30% of HUS survivors are left with some degree of residual disease, including chronic kidney disease and cardiovascular, neurologic, endocrine, gastrointestinal, behavioral or cognitive dysfunction.[82] Only one of the analyzed studies[51] looked for risk factors of contamination. Contamination rates were higher in undercooked versus well-done meat (20% vs. 6%) and fresh versus prepared chicken (16.6% vs. 3%); interestingly, the reverse was noted for cooked (2.72%) versus raw fish (1.4%).

Some interesting findings were highlighted by our subgroup analysis. Northern (11%) and Western (8.4%) regions of Iran revealed above average STEC detection rates; however, data of some of the remaining provinces of Iran are missing. Considering studies across the whole of Iran, the prevalence of STEC in the examined samples was 5.73%. This high rate of STEC detection and contamination of foods warrants immediate attention of the Ministry of Health and provincial Health Departments, and enlisting STEC surveillance for better food safety in Iran. It is of note that dairy products had a 1.5-times higher contamination rate compared with meat or vegetables. The occurrence of STEC in raw milk was between 0 and 2% in studies performed since the year 2000. Previous work revealed an increase in STEC counts during cheese making, e.g., by examining milk filters used to separate whey from curds.[83] The prevalence of raw milk contamination in our study was 4.4% (95% CI 0.2%–11.7%; I2 = 94%). Milk contamination by stx 2 (2.2%) was more common than by stx 1 (1.0%).[83] The contamination rate of cheese was 2.6% (0.2%–12.7%; I2 = 88%).

While E. coli O157:H7 has been implicated in the majority of foodborne outbreaks of HC and HUS worldwide, other STEC serotypes are well known to produce human disease and occasional outbreaks with or without an epidemiological link to contaminated food.[84] Contamination of retail meat and other food with non-O157 STEC serotypes have been reported.[84],[85],[86] but not all of these strains are found in symptomatic humans. In our review, non-O157 STEC strains were isolated twice as often as E. coli O157:H7. The predominant non-O157 serotype was O26. Infections by STEC O26:H11 and nonmotile O26 strains have been well documented in sporadic and epidemic (typical) HUS and HC.

Most studies had a low score of external validity but a good score for internal validity. The least total score of bias was 6 which classified the study as moderate risk of bias. Sensitivity analysis revealed that the high heterogeneity is not influenced by a specific study. Different sample size, non-homogeneous populations, the period of sampling, and diverse STEC detection the techniques must be considered as a source of heterogeneity. A limitation of our findings is that none of the included studies has tried to correlate STEC contamination of foods with human disease. Although the majority of the studies used PCR to detect virulence genes, none looked for stx subtypes, specifically stx 2. In addition, not all regions of Iran are represented. For example, no data are available from the Northwest, South or Southeast Iran.

  Conclusions Top

These findings confirm that Iran presents a high-risk environment for infections with O157 and non-O157 STEC strains. Adequately equipped laboratories and active surveillance are needed in Iran to detect and track these pathogens.


The authors would like to thank Ali Asghar Clinical Research Development Center for Editorial/Statistical/Search Assistance through the period of study. This work has been supported by the Center for international scientific studies and collaborations, ID number 376 dated the 1st June 2016.

Financial support and sponsorship


Conflicts of interest

There are no conflicts of interest.

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