Abstract
Shiga‑toxin‑producing E. coli (STEC) is a foodborne pathogen associated with outbreaks worldwide that can be identified in the feces and in the meat of food‑producing animals. Our study aimed to evaluate the incidence of E. coli O157:H7 in the feces of diarrheic camels (Camelus dromedarius) in Tunisia. From January 2018 to April 2019, 120 unduplicated fecal samples were obtained from diarrheic camels located in southern Tunisia. Non‑sorbitol‑fermenting colonies were confirmed as E. coli O157 via latex agglutination test and were screened for the presence of rfbEO157, fliCH7, stx1, stx2, eaeA, and ehxA genes by PCR. All isolates were examined for their susceptibility to 21 antibiotics. Of the 70 E. coli isolates that were recovered from 120 diarrheic camels, 4 (5.7%) were identified as STEC O157:H7. All isolates harbored ehxA and eae genes. Shiga toxin genes stx2 and stx1 were present in 50% and 25% of isolates, respectively. All E. coli O157:H7 isolates were sensitive to amoxicillin/clavulanic acid, cefotaxime, cefepime, aztreonam, colistin, and sulfamethoxazole‑trimethoprim. All isolates belonged to the phylogroup E. This is the first report of E. coli O157:H7 isolates from diarrheic camels in Tunisia with a prevalence of 4 isolates (3.3%) amongst 120 fecal samples. This study supports the necessity for a platform purposed for regular screening and surveillance programs in food‑producing animals and meat products, to perform early and rapid identification of food‑borne pathogens.
References
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Al Humam NA. 2016. Special biochemical profiles of Escherichia coli strains isolated from humans and camels by the VITEK 2 automated system in Al-Ahsa, Saudi Arabia. African Journal of Microbiology Research 10, 783-790.
Baschera M, Cernela N, Stevens MJ, Liljander A, Jores J, Corman VM, Nüesch-Inderbinen M, and Stephan R. 2019. Shiga toxin-producing Escherichia coli (STEC) isolated from fecal samples of African dromedary camels. One health 7, 100087.
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Coura FM, de Araújo Diniz S, Silva MX, Mussi JMS, Barbosa SM, Lage AP, and Heinemann MB. 2015. Phylogenetic group determination of Escherichia coli isolated from animals samples. The Scientific World Journal 2015.
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Falup-Pecurariu O, Lixandru RI, Cojocaru E, Csutak K, Monescu V, Muhsen K, Falup-Pecurariu C, and Cohen D. 2019. Shiga toxin producing Escherichia coli-associated diarrhea and hemolytic uremic syndrome in young children in Romania. Gut pathogens 11, 1-7.
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Hegde NV, Jayarao BM, and DebRoy C. 2012. Rapid detection of the top six non-O157 Shiga toxin-producing Escherichia coli O groups in ground beef by flow cytometry. Journal of clinical microbiology 50, 2137-2139.
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Mohammed Hamzah A, Mohammed Hussein A, and Mahmoud Khalef J. 2013. Isolation of Escherichia coli 0157: H7 strain from fecal samples of zoo animal. The Scientific World Journal 2013.
Moore J, McCalmont M, Xu J, Nation G, Tinson A, Crothers L, and Harron D. 2002. Prevalence of faecal pathogens in calves of racing camels (Camelus dromedarius) in the United Arab Emirates. Tropical animal health and production 34, 283.
Oliver SP, Murinda SE, and Jayarao BM. 2011. Impact of antibiotic use in adult dairy cows on antimicrobial resistance of veterinary and human pathogens: a comprehensive review. Foodborne pathogens and disease 8, 337-355.
Paton AW, and Paton JC. 1998. Detection and Characterization of Shiga ToxigenicEscherichia coli by Using Multiplex PCR Assays forstx 1, stx 2, eaeA, Enterohemorrhagic E. coli hlyA, rfb O111, andrfb O157. Journal of clinical microbiology 36, 598-602.
Rahimi E. 2012. Prevalence of virulence genes of Escherichia coli O157: H7/NM isolated from the feces of water buffaloes, camels, cattle, sheep and goats in Iran. Philippine Journal of Veterinary Medicine (Philippines).
Rahimi E, Kazemeini HR, and Salajegheh M. Escherichia coli O157: H7/NM prevalence in raw beef, camel, sheep, goat, and water buffalo meat in Fars and Khuzestan provinces, Iran. Proc. Veterinary Research Forum, 2012. Faculty of Veterinary Medicine, Urmia University, Urmia, Iran, 15.
Ranjbar R, Masoudimanesh M, Dehkordi FS, Jonaidi-Jafari N, and Rahimi E. 2017. Shiga (Vero)-toxin producing Escherichia coli isolated from the hospital foods; virulence factors, o-serogroups and antimicrobial resistance properties. Antimicrobial Resistance & Infection Control 6, 1-11.
Sami M, and Adeli M. 2013. Isolation of typical and atypical E. coli O157 strains from camel feces. OJVR 17, 130-136.
Schwidder M, Heinisch L, and Schmidt H. 2019. Genetics, toxicity, and distribution of enterohemorrhagic Escherichia coli hemolysin. Toxins 11, 502.
Sjöling Å, Sadeghipoorjahromi L, Novak D, and Tobias J. 2015. Detection of major diarrheagenic bacterial pathogens by multiplex PCR panels. Microbiological research 172, 34-40.
Sperandio V, and Nguyen Y. 2012. Enterohemorrhagic E. coli (EHEC) pathogenesis. Frontiers in cellular and infection microbiology 2, 90.
Tanzifi P, Bahrami AR, and Rahimi E. 2015. Study on antimicrobial resistance of Escherichia coli O157: H7/NM isolated from raw bovine, camel, water buffalo, caprine and ovine milk. Research Journal of Recent Sciences ISSN 2277, 2502.
Tayh G, Sallem RB, Yahia HB, Gharsa H, Klibi N, Boudabous A, and Slama KB. 2016. First report of extended-spectrum β-lactamases among clinical isolates of Escherichia coli in Gaza Strip, Palestine. Journal of global antimicrobial resistance 6, 17-21.
Tenaillon O, Skurnik D, Picard B, and Denamur E. 2010. The population genetics of commensal Escherichia coli. Nature reviews microbiology 8, 207-217.
Al-Ajmi D, Rahman S, and Banu S. 2020. Occurrence, virulence genes, and antimicrobial profiles of Escherichia coli O157 isolated from ruminants slaughtered in Al Ain, United Arab Emirates. BMC microbiology 20, 1-10.
Al-Gburi NM. 2016. Prevalence of Escherichia coli O157: H7 in camels fecal samples. J Genet Environ Resour Conserv 4, 46-50.
Al Humam NA. 2016. Special biochemical profiles of Escherichia coli strains isolated from humans and camels by the VITEK 2 automated system in Al-Ahsa, Saudi Arabia. African Journal of Microbiology Research 10, 783-790.
Baschera M, Cernela N, Stevens MJ, Liljander A, Jores J, Corman VM, Nüesch-Inderbinen M, and Stephan R. 2019. Shiga toxin-producing Escherichia coli (STEC) isolated from fecal samples of African dromedary camels. One health 7, 100087.
Bosilevac JM, Gassem MA, Al Sheddy IA, Almaiman SA, Al-Mohizea IS, Alowaimer A, and Koohmaraie M. 2015. Prevalence of Escherichia coli O157: H7 and Salmonella in camels, cattle, goats, and sheep harvested for meat in Riyadh. Journal of food protection 78, 89-96.
Clermont O, Christenson JK, Denamur E, and Gordon DM. 2013. The C lermont E scherichia coli phylo‐typing method revisited: improvement of specificity and detection of new phylo‐groups. Environmental microbiology reports 5, 58-65.
Control CfD, and Prevention. 2019. Outbreak of E. coli infections linked to romaine lettuce. US Department of Health and Human Services, Centers for Disease Control and Prevention, Atlanta.
Coura FM, de Araújo Diniz S, Silva MX, Mussi JMS, Barbosa SM, Lage AP, and Heinemann MB. 2015. Phylogenetic group determination of Escherichia coli isolated from animals samples. The Scientific World Journal 2015.
El-Hewairy H, Awad W, and Ibrahim A. 2009. Serotyping and molecular characterization of Escherichia coli isolated from diarrheic and in-contact camel calves. Egyptain Journal of Comparative Pathology and Clinical Pathology 22.
El-Sayed A, Ahmed S, and Awad W. 2008. Do camels (Camelus dromedarius) play an epidemiological role in the spread of Shiga Toxin producing Escherichia coli (STEC) infection? Tropical animal health and production 40, 469-473.
Falup-Pecurariu O, Lixandru RI, Cojocaru E, Csutak K, Monescu V, Muhsen K, Falup-Pecurariu C, and Cohen D. 2019. Shiga toxin producing Escherichia coli-associated diarrhea and hemolytic uremic syndrome in young children in Romania. Gut pathogens 11, 1-7.
Feng P, and Monday S. 2000. Multiplex PCR for detection of trait and virulence factors in enterohemorrhagic Escherichia coli serotypes. Molecular and cellular probes 14, 333-337.
Ferens WA, and Hovde CJ. 2011. Escherichia coli O157: H7: animal reservoir and sources of human infection. Foodborne pathogens and disease 8, 465-487.
Fu S, Bai X, Fan R, Sun H, Xu Y, and Xiong Y. 2018. Genetic diversity of the enterohaemolysin gene (ehxA) in non-O157 Shiga toxin-producing Escherichia coli strains in China. Scientific reports 8, 1-8.
Grispoldi L, Bertero F, Franceschini S, Mastrosimone F, Sechi P, Iulietto MF, Ceccarelli M, and Cenci-Goga BT. 2017. Prevalence and characterisation of shigatoxigenic Escherichia coli isolated from beef cattle fed with prebiotics. Italian journal of food safety 6.
Hajian S, Rahimi E, and Mommtaz H. A 3-year study of Escherichia coli O157: H7 in cattle, camel, sheep, goat, chicken and beef minced meat. Proc. Int Conf Food Eng Biotechnol, 2011. 163-165.
Hegde NV, Jayarao BM, and DebRoy C. 2012. Rapid detection of the top six non-O157 Shiga toxin-producing Escherichia coli O groups in ground beef by flow cytometry. Journal of clinical microbiology 50, 2137-2139.
Heininger A, Binder M, Schmidt S, Unertl K, Botzenhart K, and Döring G. 1999. PCR and blood culture for detection ofEscherichia coli bacteremia in rats. Journal of clinical microbiology 37, 2479-2482.
Hudson JA, Frewer LJ, Jones G, Brereton PA, Whittingham MJ, and Stewart G. 2017. The agri-food chain and antimicrobial resistance: A review. Trends in Food Science & Technology 69, 131-147.
Jo M-Y, Kim J-H, Lim J-H, Kang M-Y, Koh H-B, Park Y-H, Yoon D-Y, Chae J-S, Eo S-K, and Lee JH. 2004. Prevalence and characteristics of Escherichia coli O157 from major food animals in Korea. International journal of food microbiology 95, 41-49.
Manning SD, Motiwala AS, Springman AC, Qi W, Lacher DW, Ouellette LM, Mladonicky JM, Somsel P, Rudrik JT, and Dietrich SE. 2008. Variation in virulence among clades of Escherichia coli O157: H7 associated with disease outbreaks. Proceedings of the National Academy of Sciences 105, 4868-4873.
Meng J, LeJeune JT, Zhao T, and Doyle MP. 2012. Enterohemorrhagic Escherichia coli. Food microbiology: Fundamentals and frontiers, 287-309.
Mohammed Hamzah A, Mohammed Hussein A, and Mahmoud Khalef J. 2013. Isolation of Escherichia coli 0157: H7 strain from fecal samples of zoo animal. The Scientific World Journal 2013.
Moore J, McCalmont M, Xu J, Nation G, Tinson A, Crothers L, and Harron D. 2002. Prevalence of faecal pathogens in calves of racing camels (Camelus dromedarius) in the United Arab Emirates. Tropical animal health and production 34, 283.
Oliver SP, Murinda SE, and Jayarao BM. 2011. Impact of antibiotic use in adult dairy cows on antimicrobial resistance of veterinary and human pathogens: a comprehensive review. Foodborne pathogens and disease 8, 337-355.
Paton AW, and Paton JC. 1998. Detection and Characterization of Shiga ToxigenicEscherichia coli by Using Multiplex PCR Assays forstx 1, stx 2, eaeA, Enterohemorrhagic E. coli hlyA, rfb O111, andrfb O157. Journal of clinical microbiology 36, 598-602.
Rahimi E. 2012. Prevalence of virulence genes of Escherichia coli O157: H7/NM isolated from the feces of water buffaloes, camels, cattle, sheep and goats in Iran. Philippine Journal of Veterinary Medicine (Philippines).
Rahimi E, Kazemeini HR, and Salajegheh M. Escherichia coli O157: H7/NM prevalence in raw beef, camel, sheep, goat, and water buffalo meat in Fars and Khuzestan provinces, Iran. Proc. Veterinary Research Forum, 2012. Faculty of Veterinary Medicine, Urmia University, Urmia, Iran, 15.
Ranjbar R, Masoudimanesh M, Dehkordi FS, Jonaidi-Jafari N, and Rahimi E. 2017. Shiga (Vero)-toxin producing Escherichia coli isolated from the hospital foods; virulence factors, o-serogroups and antimicrobial resistance properties. Antimicrobial Resistance & Infection Control 6, 1-11.
Sami M, and Adeli M. 2013. Isolation of typical and atypical E. coli O157 strains from camel feces. OJVR 17, 130-136.
Schwidder M, Heinisch L, and Schmidt H. 2019. Genetics, toxicity, and distribution of enterohemorrhagic Escherichia coli hemolysin. Toxins 11, 502.
Sjöling Å, Sadeghipoorjahromi L, Novak D, and Tobias J. 2015. Detection of major diarrheagenic bacterial pathogens by multiplex PCR panels. Microbiological research 172, 34-40.
Sperandio V, and Nguyen Y. 2012. Enterohemorrhagic E. coli (EHEC) pathogenesis. Frontiers in cellular and infection microbiology 2, 90.
Tanzifi P, Bahrami AR, and Rahimi E. 2015. Study on antimicrobial resistance of Escherichia coli O157: H7/NM isolated from raw bovine, camel, water buffalo, caprine and ovine milk. Research Journal of Recent Sciences ISSN 2277, 2502.
Tayh G, Sallem RB, Yahia HB, Gharsa H, Klibi N, Boudabous A, and Slama KB. 2016. First report of extended-spectrum β-lactamases among clinical isolates of Escherichia coli in Gaza Strip, Palestine. Journal of global antimicrobial resistance 6, 17-21.
Tenaillon O, Skurnik D, Picard B, and Denamur E. 2010. The population genetics of commensal Escherichia coli. Nature reviews microbiology 8, 207-217.