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Table of Contents
ORIGINAL ARTICLE
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
Iran
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Source of Support: None, Conflict of Interest: None


DOI: 10.4103/2589-9309.305897

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  Abstract 


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 Jan 24];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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Analysis

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.

Acknowledgments

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

Nil.

Conflicts of interest

There are no conflicts of interest.



 
  References Top

1.
Caprioli A, Morabito S, Brugère H, Oswald E. Enterohaemorrhagic Escherichia coli: Emerging issues on virulence and modes of transmission. Vet Res 2005;36:289-311.  Back to cited text no. 1
    
2.
Bitzan M, Lapeyraque A. Postinfectious hemolytic uremic syndrome. In: Geary DF, Schaefer F, editors. Pediatric Kidney Disease: Springer-Verlag, Berlin, Heidelberg; 2016. p. 653-731.  Back to cited text no. 2
    
3.
Etcheverría AI, Padola NL. Shiga toxin-producing Escherichia coli: Factors involved in virulence and cattle colonization. Virulence 2013;4:366-72.  Back to cited text no. 3
    
4.
Marder Mph EP, Griffin PM, Cieslak PR, Dunn J, Hurd S, Jervis R, et al. Preliminary incidence and trends of infections with pathogens transmitted commonly through food:Foodborne diseases active surveillance network, 10 U.S. Sites, 2006-2017. MMWR Morb Mortal Wkly Rep 2018;67:324-8.  Back to cited text no. 4
    
5.
Rivas M, Miliwebsky E, Chinen I, Deza N, Leotta GA. The epidemiology of hemolytic uremic syndrome in Argentina. Diagnosis of the etiologic agent, reservoirs and routes of transmission. Medicina (B Aires) 2006;66 Suppl 3:27-32.  Back to cited text no. 5
    
6.
Qadri SM, Kayali S. Enterohemorrhagic Escherichia coli. A dangerous food-borne pathogen. Postgrad Med 1998;103:179-80, 185-7.  Back to cited text no. 6
    
7.
Chapman PA. Sources of Escherichia coli O157 and experiences over the past 15 years in Sheffield, UK. Symp Ser Soc Appl Microbiol 2000;29:51S-60S.  Back to cited text no. 7
    
8.
Chekabab SM, Paquin-Veillette J, Dozois CM, Harel J. The ecological habitat and transmission of Escherichia coli O157:H7. FEMS Microbiol Lett 2013;341:1-2.  Back to cited text no. 8
    
9.
Rowell S, King C, Jenkins C, Dallman TJ, Decraene V, Lamden K, et al. An outbreak of Shiga toxin-producing Escherichia coli serogroup O157 linked to a lamb-feeding event. Epidemiol Infect 2016;144:2494-500.  Back to cited text no. 9
    
10.
Rosin P, Niskanen T, Palm D, Struelens M, Takkinen J, Shiga toxin-producing Escherichia coli Experts of European Union Food- and Waterborne Diseases and Zoonoses Network. Laboratory preparedness for detection and monitoring of Shiga toxin 2-producing Escherichia coli O104:H4 in Europe and response to the 2011 outbreak. Euro Surveill 2013;18:20508.  Back to cited text no. 10
    
11.
Kansas Department of Health and Environment Investigation Guidelines. Shiga Toxin-Producing Escherichia coli (STEC), lncluding E. coli O157:H7, investigation Guideline; Updated 2019. Available from: http://www.kdheks.gov ' epi ' STEC_Investigation_Guideline. [Last accessed on 10 May 2020].  Back to cited text no. 11
    
12.
Islam MZ, Musekiwa A, Islam K, Ahmed S, Chowdhury S, Ahad A, et al. Regional variation in the prevalence of E. coli O157 in cattle: A meta-analysis and meta-regression. PLoS One 2014;9:e93299.  Back to cited text no. 12
    
13.
Havelaar AH, Kirk MD, Torgerson PR, Gibb HJ, Hald T, Lake RJ, et al. World Health Organization global estimates and regional comparisons of the burden of foodborne disease in 2010. PLoS Med 2015;12:e1001923.  Back to cited text no. 13
    
14.
World Health Organization. Shiga Toxin-Producing Escherichia coli (STEC) and Food: Attribution, characterization, and monitoring. microbiological risk assessment series; 2018.  Back to cited text no. 14
    
15.
Parhizgari N, Gouya MM, Mostafavi E. Emerging and re-emerging infectious diseases in Iran. Iran J Microbiol 2017;9:122-42.  Back to cited text no. 15
    
16.
Moher D, Liberati A, Tetzlaff J, Altman D, Group. TP. Preferred reporting items for systematic reviews and meta-analyses: The PRISMA statement. PLoS Med 2009;6:E1000097.  Back to cited text no. 16
    
17.
Hooman N, Mansour Ghanaei R, Yaghoubi M, Nakhaie S. The prevalence of shiga toxin-producing Escherichia coli in patients with gastroenteritis and sources of infections in Iran: A systematic review study protocol. J Ped Nephrol 2016;4:82-5.  Back to cited text no. 17
    
18.
Hooman N, Khodadost M, Ahmadi A, Nakhaie S, Nagh Shizadian R. The prevalence of shiga toxin-producing Escherichia coli in patients with gastroenteritis in Iran, Systematic review and meta-analysis. Iran J Kidney Dis 2019;13:139-50.  Back to cited text no. 18
    
19.
Vandenbroucke J, von Elm E, Altman D, Gøtzsche P, Mulrow C, Pocock S, et al. Strengthening the reporting of observational studies in epidemiology (STROBE): Explanation and elaboration. Int J Surg 2014;12:1500-24.  Back to cited text no. 19
    
20.
Hoy D, Brooks P, Woolf A, Blyth F, March L, Bain C, et al. Assessing risk of bias in prevalence studies: Modification of an existing tool and evidence of interrater agreement. J Clin Epidemiol 2012;65:934-9.  Back to cited text no. 20
    
21.
DerSimonian R, Laird, N. Meta-analysis in clinical trials. Control Clin Trials 1986;7:177-88.  Back to cited text no. 21
    
22.
Momtaz H, Safarpoor Dehkordi F, Taktaz T, Rezvani A, Yarali S. Shiga toxin-producing Escherichia coli isolated from bovine mastitic milk: Serogroups, virulence factors, and antibiotic resistance properties. ScientificWorldJournal 2012;2012:618709.  Back to cited text no. 22
    
23.
Kazemi Galougahi MH, Kouhian K. Investigation of a case of gastroenteritis outbreak caused by Escherichia coli bacteriological O157: H7 in one of the barracks of the army of the Islamic Republic of Iran in 2010. Nurse Phys War 2012;14:19-21.  Back to cited text no. 23
    
24.
Momtaz H, Safarpoor Dehkordi F, Rahimi E, Ezadi H, Arab R. Incidence of Shiga toxin-producing Escherichia coli serogroups in ruminant's meat. Meat Sci 2013;95:381-8.  Back to cited text no. 24
    
25.
Dehkordi FS, Yazdani F, Mozafari J, Valizadeh Y. Virulence factors, serogroups and antimicrobial resistance properties of Escherichia coli strains in fermented dairy products. BMC Res Notes 2014;7:217.  Back to cited text no. 25
    
26.
Mansouri-Najand L, Mohammad Khalili M. Detection of shiga-like toxigenic Escherichia coli from raw milk cheeses produced in Kerman, Iran. Vet Arhiv 2007;77:515-22.  Back to cited text no. 26
    
27.
Rahimi E, Momtaz H, Hosseini Anari M, Alimoradi M, Momeni M, Riahi M. Isolation and genomic characterization of Escherichia coli O157:NM and Escherichia coli O157:H7 in minced meat and some traditional dairy products in Iran. Afr J Biotechnol 2012;11:2328-32.  Back to cited text no. 27
    
28.
Kargar M, Daneshvar M, Homayoon M. Prevalence of shiga toxins, intimin and hemolysin genes of Escherichia coli O157:H7 strains from industrial ground meat in Shiraz. JSSU 2011;18:512-20.  Back to cited text no. 28
    
29.
Jafareyan-Sedigh M, Rahimi E, Doosti A. Isolation of Escherichia coli O157: H7 in sheep meats using cultural and PCR method. J Shahrekord Univ Med Sci 2011;13:61-8.  Back to cited text no. 29
    
30.
Jamshidi A, Bassami M, Khanzadi S, Soltaninejad V. Using multiplex-PCR assay in identification of Escherichia coli O157:H7 isolated from hamburger samples in Mashhad, Iran. FSCT 2012;35:101-7.  Back to cited text no. 30
    
31.
Shah Illi M, Kargar M, Rezaeian A, Homayoon M, Kargar M, Ghorbani-Dalini S. Evaluation of virulance genes of Shiga toxin producing Escherichia coli from juice purchase and vegetables in Shiraz. J Microb World 2010;3:40-7.  Back to cited text no. 31
    
32.
Khandaghi J, Razavilar V, Barzgari A. Isolation of Escherichia coli O157:H7 from manure fertilized farms and raw vegetables grown on it, in Tabriz city in Iran. Afr J Microbiol Res 2010;4:891-5.  Back to cited text no. 32
    
33.
Mehrabiyan S, Tahmasby H, Momtaz H, Khosravi N, Kaboli Boroujeni H, Najafzadeh V, et al. Multiplex PCR detection of stx1, stx2 and eaeA genes in Escherichia coli isolated from lambs in Chaharmahalva Bakhtiari, Iran Biol J Microorg 2013;2:11-8.  Back to cited text no. 33
    
34.
Kargar M, Daneshvar M, Homayoun M. Surveillance of virulence markers and antibiotic resistance of shiga toxin producing E. coli O157:H7 strains from meats purchase in Shiraz. Iran South Medl 2011;14:76-83.  Back to cited text no. 34
    
35.
Mazaheri S, Salmanzadeh-Ahrabi S, Falsafi T, Aslani MM. Isolation of Enteropathogenic Escherichia coli from lettuce samples in Tehran. Gastroenterol Hepatol Bed Bench 2014;7:38-42.  Back to cited text no. 35
    
36.
Mohammadi P, Abiri R, Rezaei M, Salmanzadeh-Ahrabi S. Isolation of Shiga toxin-producing Escherichia coli from raw milk in Kermanshah, Iran. Iran J Microbiol 2013;5:233-8.  Back to cited text no. 36
    
37.
Sami M, Firouzi R, Shekarforoush S. Prevalence of Escherichia coli O157:H7 on dairy farms in Shiraz, Iran by immunomagnetic separation and multiplex PCR. Iran J Vet Res 2007;8:319-24.  Back to cited text no. 37
    
38.
Brenjchi M, Jamshidi A, Farzaneh N, Bassami M. Identification of shiga toxin producing Escherichia coli O157:H7 in raw cow milk samples from dairy farms in Mashhad using multiplex PCR assay. Iran J Vet Res 2011;12:145-9.  Back to cited text no. 38
    
39.
Kargar M, Dianati P, Homayoon M, Jamali H. Isolation, characterization and antibiotic resistance of shiga toxin-producing Escherichia coli in hamburger and evolution of virulence genes stx1, stx2, eaeA and hly by multiplex PCR. J Fasa Univ Med Sci 2013;3:208-14.  Back to cited text no. 39
    
40.
Shams Solari S, Roayaei Ardekani M, Rezatofighi SE. Study of the contamination rate of vegetables by Enterohemorrhagic Escherichia coli (EHEC) using multiplex PCR and cultivation methods in Ahvaz Province. Jundishapur Sci Med J 2017;16:673-82.  Back to cited text no. 40
    
41.
Momtaz H, Jamshidi A. Shiga toxin-producing Escherichia coli isolated from chicken meat in Iran: Serogroups, virulence factors, and antimicrobial resistance properties. Poult Sci 2013;92:1305-13.  Back to cited text no. 41
    
42.
Baghbani Arani F, Salmanzadeh Ahrabi S, Jafari F, Habibi E, Zali M. Isolation of shigatoxin-producing Escherichia coli (STEC) from meat samples by PCR in Tehran and evaluation of antibacterial patterns of isolated strains. Pajoohandeh 2007;12:107-14.  Back to cited text no. 42
    
43.
Bonyadian M, Zahraei Salehi TZ, Mahzounieh MR, Taheri FA. Virulence genes of verotoxigenic E. coli isolated from raw milk and unpasturized cheese. J Vet Res 2011;66:223-8.  Back to cited text no. 43
    
44.
Kargar M, Heydari S, Abasiyan F, Shekarfoush S. Survey of different enrichment methods, prevalence and antibiotic resistance of E. coli O157:H7 in raw milk of Jahrom cows. IJIDTM J 2006;11:7-11.  Back to cited text no. 44
    
45.
Bagheri M, Ghanbarpour R, Alizade H. Shiga toxin and beta-lactamases genes in Escherichia coli phylotypes isolated from carcasses of broiler chickens slaughtered in Iran. Int J Food Microbiol 2014;177:16-20.  Back to cited text no. 45
    
46.
Jamshidi A, Bassami M, Rasooli M. Isolation of Escherichia coli O157:H7 from ground beef samples collected from beef markets, using conventional culture and polymerase chain reaction in Mashhad, northeastern Iran. Iran J Vet Res 2008;9:72-6.  Back to cited text no. 46
    
47.
Shekarforoush. S, Tahmtan Y, Pourbakhsh A. Detection and frequency of Stx2 gene in Escherchia coli O157 and O157:H7 strains isolated from sheep carcasses in Shiraz, Iran. Pak J Med Sci 2008;11:1085-92.  Back to cited text no. 47
    
48.
Rahimi E, Momtaz H, Hemmatzadeh F. The prevalence of Escherichia coli O157:H7, Listeria monocytogenes and Campylobacter spp. on bovine carcasses in Isfahan, Iran. Iran J Vet Res 2008;9:365-70.  Back to cited text no. 48
    
49.
Rahimi E, Momtaz H, Nozarpour N. Prevalence of Listeria Spp., Campylobacter spp. and Escherichia coli O157:H7 isolated from camel carcasses during processing. Bulg J Vet Med 2010;13:179-85.  Back to cited text no. 49
    
50.
Sakhaie Shahreza M, Rahimi E, Momtaz H. Shiga-toxigenic Escherichia coli in ready-to-eat food staffs: Prevalence and distribution of putative virulence factors. Microbiol Res 2017;8:88-92.  Back to cited text no. 50
    
51.
Ranjbar R, Masoudimanesh M, Dehkordi FS, Jonaidi-Jafari N, Rahimi E. Shiga (Vero)-toxin producing Escherichia coli isolated from the hospital foods; virulence factors, o-serogroups and antimicrobial resistance properties. Antimicrob Resist Infect Control 2017;6:4.  Back to cited text no. 51
    
52.
Jeddi MZ, Yunesian M, Gorji ME, Noori N, Pourmand MR, Khaniki GR. Microbial evaluation of fresh, minimally-processed vegetables and bagged sprouts from chain supermarkets. J Health Popul Nutr 2014;32:391-9.  Back to cited text no. 52
    
53.
Mashak Z. Virulence genes and phenotypic evaluation of the antibiotic resistance of vero toxin producing Escherichia coli recovered from milk, meat, and vegetables. Jundishapur J Microbiol 2018;11:E62288.  Back to cited text no. 53
    
54.
Moori Bakhtiari N, Fazlara A, Hafezizade Jolge T. Risk of shiga toxin-producing Escherichia coli infection in humans due to consuming unpasteurized dairy products. Int J Enteric Pathog 2018;6:14-7.  Back to cited text no. 54
    
55.
Ranjbar R, Safarpoor Dehkordi F, Sakhaei Shahreza MH, Rahimi E. Prevalence, identification of virulence factors, O-serogroups and antibiotic resistance properties of Shiga-toxin producing Escherichia coli strains isolated from raw milk and traditional dairy products. Antimicrob Resist Int 2018;7:53.  Back to cited text no. 55
    
56.
Shakerian A, Rahimi E, Emad P. Vegetables and restaurant salads as a reservoir for shiga toxigenic Escherichia coli: Distribution of virulence factors, O-serogroups, and antibiotic resistance properties. J Food Prot 2016;79:1154-60.  Back to cited text no. 56
    
57.
Jajarmi M, Askari Badouei M, Imani Fooladi AA, Ghanbarpour R, Ahmadi A. Pathogenic potential of Shiga toxin-producing Escherichia coli strains of caprine origin: Virulence genes, Shiga toxin subtypes, phylogenetic background and clonal relatedness. BMC Vet Res 2018;14:97.  Back to cited text no. 57
    
58.
Momtaz H, Dehkordi FS, Hosseini MJ, Sarshar M, Heidari M. Serogroups, virulence genes and antibiotic resistance in Shiga toxin-producing Escherichia coli isolated from diarrheic and non-diarrheic pediatric patients in Iran. Gut Pathog 2013;5:39.  Back to cited text no. 58
    
59.
Shahrani M, Dehkordi FS, Momtaz H. Characterization of Escherichia coli virulence genes, pathotypes and antibiotic resistance properties in diarrheic calves in Iran. Biol Res 2014;47:28.  Back to cited text no. 59
    
60.
Yaghobzadeh N, Ownagh A, Mardani K, Khalili M, Tokmechi A, Nikbakhsh P. Molecular Identification, antibiotic resistance profile of shiga toxin-producing Escherichia coli (STEC) and antibacterial activity of Zataria multiflora (Boiss) and Carum Copticum essential oil against them. Urmia Med J 2011;22:262-9.  Back to cited text no. 60
    
61.
Zahraei Salehi T, Askari Badouei M, Mehdizadeh Gohari I. Molecular detection and antibacterial susceptibility of enteropathogenic Escherichia coli (EPEC) and shigatoxigenic Escherichia coli (STEC) strains isolated from healthy and diarrhoeic dogs. Comp Clin Pathol 2011;20:585-9.  Back to cited text no. 61
    
62.
Tahamtan Y, Hayati M, Namavari M. Prevalence and distribution of the stx, stx genes in Shiga toxin producing E. coli (STEC) isolates from cattle. Iran J Microbiol 2010;2:8-13.  Back to cited text no. 62
    
63.
Staji H, Salimi Bejestani M, Changizi E, Javaheri Vayeghan A. Distribution of Escherichia coli Shiga toxin encoding genes (stx1, stx2) in Sangesari lambs suffering from diarrhea by Multiplex PCR technique. Koomesh 2015;17:84-91.  Back to cited text no. 63
    
64.
Staji H, Tonelli A, Javaheri-Vayeghan A, Changizi E, Salimi-Bejestani MR. Distribution of Shiga toxin genes subtypes in B1 phylotypes of Escherichia coli isolated from calves suffering from diarrhea in Tehran suburb using DNA oligonucleotide arrays. Iran J Microbiol 2015;7:191-7.  Back to cited text no. 64
    
65.
Zahraei-saleh T, Safarchi A, Rabbani Khorasgani M. Identification of virulence genes in isolated Escherichia coli from diarrheic calves and lambs by multiplex polymerase chain reaction. PJBS 2006;9:191-6.  Back to cited text no. 65
    
66.
Dastmalchi SH, Ayremlou N. Characterization of shiga toxin-producing Escherichia coli (STEC) in feces of healthy and diarrheic calves in Urmia region, Iran. Iran J Microbiol 2012;4:63-9.  Back to cited text no. 66
    
67.
Jamshidi A, Rad M, Zeinali T. Detection of shiga toxin-producing Escherichia coli (STEC) in faeces of healthy calves in Mashhad, Iran. Arch Razi Inst 2015;70:179-85.  Back to cited text no. 67
    
68.
Doregiraee F, Alebouyeh M, Nayeri Fasaei B, Charkhkar S, Tajedin E, Zali MR. Isolation of atypical enteropathogenic and shiga toxin encoding Escherichia coli strains from poultry in Tehran, Iran. Gastroenterol Hepatol Bed Bench 2016;9:53-7.  Back to cited text no. 68
    
69.
Tahamtan Y, Pourbakhsh S, Hayati M, Namdar N, Shams Z, Namvari M. Prevalence and molecular characterization of verotoxin-producing Escherichia coli O157:H7 in cattle and sheep in Shiraz-Iran. Arch Razi Inst 2011;66:29-36.  Back to cited text no. 69
    
70.
Koochakzadeh A, Zahraei Salehi T, Nayeri Fasaei B, Askari Badouei M. Detection of verotoxin (Shiga-like toxin)-producing and eae harboring Escherichia coli in some wild captive and domestic Equidae and Canidae. Arch Razi Inst 2014;69:157-63.  Back to cited text no. 70
    
71.
Sepehriseresht. S, Zahraie –Salehi T, Satar M, Tajbakhsh H, Aslani M. The source of shigatoxin gene in enterohemorrhagic Escherchia coli. SJKUMS 2008;13:45-52.  Back to cited text no. 71
    
72.
Bakhshi B, Najibi S, Sepehri-Seresht S. Molecular characterization of enterohemorrhagic Escherichia coli isolates from cattle. J Vet Med Sci 2014;76:1195-9.  Back to cited text no. 72
    
73.
Mazhaheri Nejad Fard R, Behzadian Nezhad G, Zahraei Salehi T, Atash Parvar N. Evaluation of ehxA, st×1, and st×2 virulence gene prevalence in cattle Escherichia coli isolates by. Arch Razi Ins 2005;60:55-66.  Back to cited text no. 73
    
74.
Askari Badouei M, Zahraei Salehi T, Rabbani Khorasgani M, Tadjbakhsh H, Nikbakht Brujeni G. Occurrence and characterisation of enterohaemorrhagic Escherichia coli isolates from diarrhoeic calv. Comp Clin Pathol 2010;19:296-300.  Back to cited text no. 74
    
75.
Sepehriseresht S, Zahraei Salehi T, Sattari M, Tadjbakhsh H, Aslani M. Detection of shigatoxigenic Escherichia coli from fecal samples of calves and cattle by molecular and serological methods. Comp Clin Path 2009;18:53-7.  Back to cited text no. 75
    
76.
Tabatabaei M, Mokarizadeh A, Foad-Marashi N. Detection and Molecular characterization of sorbitol negative shiga toxigenic Escherichia coli in chicken from northwest of Iran. Vet Res Forum 2011;2:183-8.  Back to cited text no. 76
    
77.
Yaghobzadeh N, Ownagh A, Mardani K., Khalili M. Prevalence, molecular characterization and serology of Shiga toxin producing Escherichia coli isolated from buffaloes in West Azerbaijan, Iran Int J Vet Res. 2011;5:113-7.  Back to cited text no. 77
    
78.
Askari Badouei M, Lotfollahzadeh S, Arman M, Haddadi M. Prevalence and resistance profiles of enteropathogenic and shiga toxin-producing Escherichia coli in diarrheic calves in Mashhad and Garmsar districts, Iran. Avicenna J Clin Microb Infec 2014;1:E22802.  Back to cited text no. 78
    
79.
Asadi S, Shams N, Nayebaghaee S. Isolation and Frequency of Escherichia coli O157:H7 from fecal samples of lorestan ostrich farms using culture and multiplex PCR. J Veterinary Microbiol 2017;13:97-107.  Back to cited text no. 79
    
80.
Otukesh H, Hoseini R, Golnari P, Fereshtehnejad SM, Zamanfar D, Hooman N, et al. Short-term and long-term outcome of hemolytic uremic syndrome in Iranian children. J Nephrol 2008;21:694-703.  Back to cited text no. 80
    
81.
Hooman N, Otukesh H, Delshad S, Farhood P. Surgical complications of hemolytic uremic syndrome: Single center experiences. J Indian Assoc Pediatr Surg 2007;12:129-32.  Back to cited text no. 81
  [Full text]  
82.
Spinale JM, Ruebner RL, Copelovitch L, Kaplan BS. Long-term outcomes of Shiga toxin hemolytic uremic syndrome. Pediatr Nephrol 2013;28:2097-105.  Back to cited text no. 82
    
83.
Farrokh C, Jordan K, Auvray F, Glass K, Oppegaard H, Raynaud S, et al. Review of Shiga-toxin-producing Escherichia coli (STEC) and their significance in dairy production. Int J Food Microbiol 2013;162:190-212.  Back to cited text no. 83
    
84.
Yang SC, Lin CH, Aljuffali IA, Fang JY. Current pathogenic Escherichia coli foodborne outbreak cases and therapy development. Arch Microbiol 2017;199:811-25.  Back to cited text no. 84
    
85.
Frank C, Milde-Busch A, Werber D. Results of surveillance for infections with Shiga toxin-producing Escherichia coli (STEC) of serotype O104:H4 after the large outbreak in Germany, July to December 2011. Euro Surveill 2014;19:20760.  Back to cited text no. 85
    
86.
Martin A, Beutin L. Characteristics of Shiga toxin-producing Escherichia coli from meat and milk products of different origins and association with food producing animals as main contamination sources. Int J Food Microbiol 2011;146:99-104.  Back to cited text no. 86
    


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