Prevalence of diarrheagenic Escherichia coli in animal products in Duhok province, Iraq

Document Type : Full paper (Original article)

Authors

1 Department of Pathology and Microbiology, College of Veterinary Medicine, University of Duhok, Duhok, Iraq

2 Department of Microbiology, College of Medicine, University of Duhok, Duhok, Iraq

Abstract

Background: Diarrheagenic Escherichia coli (DEC) is regarded as a great public health concern all around the world causing diarrhoea which can be transmitted through food chain. Aims: This study aimed to determine the contamination level and exact distribution rate of DEC in food products consumed by human. Methods: Seven hundred and twenty samples of food from animal origin and fishes were analysed by conventional and molecular method for the presence of E. coli and two multiplex polymerase chain reaction (mPCR) for detection of DEC. Results: Two hundred and eighty-three E. coli isolates were detected. The classification of DEC by two multiplex PCR assay yielded 84 DEC pathotypes. Enterotoxigenic E. coli (ETEC) was detected at high rates (75%) followed by shiga-toxigenic E. coli (STEC) and enterohemorrhagic E. coli (EHEC) (each of 9.5%), enteroaggregative E. coli (EAEC) (3.5%) and atypical enteropathogenic E. coli (aEPEC) (about 2.3%). The highest number of DEC (n=26; 21.6%) was observed from beef carcasses in abattoir while the lowest number (n=7; 5.8%) was noticed from burger samples (P<0.01). Enterotoxigenic E. coli was widespread in local raw ground meat and fish surface swabs (P<0.001), EAEC (P<0.01), and EHEC (P<0.001) were only in beef carcasses swabs, STEC was more prevalent in both imported and local raw burger (P<0.01), while the isolates of aEPEC were from imported chicken carcasses (P>0.05). Conclusion: High DEC contamination rate that was observed is attributed to the poor hygienic practices during food processing. Therefore, a superior hygienic application is required.

Keywords


Abbasi, P; Kargar, M; Doosti, A; Mardaneh, J; Ghorbani-Dalini, S and Dehyadegari, MA (2016). Molecular detection of diffusely adherent Escherichia coli strains associated with diarrhea in Shiraz, Iran. Arch. Pediatr. Infect. Dis., 5: e37629.
Amézquita-Montes, Z; Tamborski, M; Kopsombut, UG; Zhang, C; Arzuza, OS and Gómez-Duarte, OG (2015). Genetic relatedness among Escherichia coli pathotypes isolated from food products for human consumption in Cartagena, Colombia. Foodborne Pathog. Dis., 12: 454-461.
Arif, SK and Salih, LIF (2010). Identification of different categories of diarrheagenic Escherichia coli in stool samples by using multiplex PCR technique. Asi. J. Medic. Sci., 2: 237-243.
Bako, E; Kagambèga, A; Traore, KA; Bagre, TS; Ibrahim, HB; Bouda, SC; Bonkoungou, IJO; Kaboré, S; Zongo, C; Traore, AS and Barro, N (2017). Characterization of diarrheagenic Escherichia coli isolated in organic waste products (cattle fecal matter, manure and slurry) from cattle’s markets in Ouagadougou, Burkina Faso. Int. J. Environ. Res. Public. Health. 14: 1-12.
Benevides-Matos, N; Pieri, FA; Penatti, M and Orlandi, PP (2015). Adherence and virulence genes of Escherichia coli from children diarrhoea in the Brazilian Amazon. Braz. J. Microbiol., 46: 131-137.
Caine, L; Nwodo, UU; Okoh, AI; Ndip, RN and Green, E (2014). Occurrence of virulence genes associated with diarrheagenic Escherichia coli isolated from raw cow’s milk from two commercial dairy farms in the eastern Cape Province, South Africa. Int. J. Environ. Resear. Publ. Heal. 11: 11950-11963.
Campos, LC; Vieira, MA; Trabulsi, LR; da Silva, LA; Monteiro-Neto, V and Gomes, TA (1999). Diffusely adhering Escherichia coli (DAEC) strains of fecal origin rarely express F1845 adhesin. Microbiol. Immunol., 43: 167-170.
Canizalez-Roman, A; Gonzalez-Nuñez, E; Vidal, JE; Flores-Villaseñor, H and León-Sicairos, N (2013). Prevalence and antibiotic resistance profiles of diarrheagenic Escherichia coli strains isolated from food items in northwestern Mexico. Int. J. Food Microbiol., 164: 36-45.
Costa, CF; Monteiro Neto, V; Santos, BR; Costa, BR; Azevedo, A; Serra, JL; Mendes, HB; Nascimento, AR; Mendes, MB and Kuppinger, O (2014). Enterobacteria identification and detection of diarrheagenic Escherichia coli in a port complex. Braz. J. Microbiol., 45: 945-952.
Croxen, MA; Law, RJ; Scholz, R; Keeney, KM; Wlodarska, M and Finlay, BB (2013). Recent advances in understanding enteric pathogenic Escherichia coli. Clin. Microbiol. Rev., 26: 822-880.
Estrada-Garcia, T; Lopez-Saucedo, C; Thompson-Bonilla, R; Abonce, M; Lopez-Hernandez, D; Santos, JI and Long, KZ (2009). Association of diarrheagenic Escherichia coli pathotypes with infection and diarrhea among mexican children and association of atypical enteropathogenic E. coli with acute diarrhea. J. Clin. Microbiol., 47: 93-98.
Farooq, S; Hussain, I; Mir, MA; Bhat, MA and Wani, SA (2009). Isolation of atypical enteropathogenic Escherichia coli and Shiga toxin 1 and 2 producing Escherichia coli from avian species in India. Lett. Appl. Microbiol., 48: 692-697.
Fujioka, M; Otomo, Y and Ahsan, CR (2013). A novel single-step multiplex polymerase chain reaction assay for the detection of diarrheagenic Escherichia coli. J. Microbiol. Method., 92: 289-292.
Galal, HM; Hakim, AS and Sohad, MD (2013). Phenotypic and virulence genes screening of Escherichia coli strains isolated from different sources in delta Egypt. Lif. Sci. J., 10: 352-361.
Gomes, TA; Elias, WP; Scaletsky, IC; Guth, BE; Rodrigues, JF; Piazza, RM; Ferreira, LC and Martinez, MB (2016). Diarrheagenic Escherichia coli. Brazillian J. Microbiol., 47: 3-30.
Hussein, HSS and Sakuma, T (2005). Invited review: prevalence of Shiga toxin-producing Escherichia coli in dairy cattle and their products. J. Dairy Sci., 88: 450-465.
Kagambèga, A; Barro, N; Traoré, AS; Siitonen, A and Haukka, K (2012a). Characterization of Salmonella enterica and detection of the virulence genes specific to diarrheagenic Escherichia coli from poultry carcasses in Ouagadougou, Burkina Faso. Foodborne Pathog. Dis., 9: 589-593.
Kagambèga, A; Martikainen, O; Lienemann, T; Siitonen, A; Traoré, AS; Barro, N and Haukka, K (2012b). Diarrheagenic Escherichia coli detected by 16-plex PCR in raw meat and beef intestines sold at local markets in Ouagadougou, Burkina Faso. Int. J. Food Microbiol., 153: 154-158.
Kambire, O; Ama, AA; Yao, KM and Koffi-Nevry, R (2017). Prevalence of virulence genes associated with diarrheagenic pathotypes of Escherichia coli isolates from water, sediment, fish, and crab in Aby lagoon, Côte d’ivoire. Int. J. Microbiol., 2017: 9532170.
Kaper, JB; Nataro, JP and Mobley, HLT (2004). Pathogenic Escherichia coli. Nat. Rev. Microbiol., 2: 123-140.
Koo, HJ; Kwak, HS; Yoon, SH and Woo, GJ (2012). Phylogenetic group distribution and prevalence of virulence genes in Escherichia coli isolates from food samples in South Korea. Wor. J. Microbiol. Biotechnol., 28: 1813-1816.
Laury, A; Echeverry, A and Brashears, M (2009). Fate of Escherichia coli O157:H7 in meat. In: Toldra, F (Ed.), Safety of meat and processed meat. (1st Edn.), Chapter 2, Lubbock, TX, USA, Springer. PP: 31-53.
Lee, GY; Jang, HI; Hwang, IG and Rhee, MS (2009). Prevalence and classification of pathogenic Escherichia coli isolated from fresh beef, poultry, and pork in Korea. Int. J. Food Microbiol., 134: 196-200.
Mohammed, MAM (2012). Molecular characterization of diarrheagenic Escherichia coli isolated from meat products sold at Mansoura city, Egypt. Food Cont., 25: 159-164.
Moreno, ACR; Filho, AF; Gomes Tdo, AT; Ramos, STS; Montemor, LPG; Tavares, VC and Martinez, MB (2010). Etiology of childhood diarrhea in the northeast of Brazil: significant emergent diarrheal pathogens. Diag. Microbiol. Infect. Dis., 66: 50-57.
Nessa, K; Ahmed, D; Islam, J; Kabir, FL and Hossain, MA (2007). Usefulness of a multiplex PCR for detection of diarrheagenic Escherichia coli in a diagnostic microbiology laboratory setting. Bang. J. Med. Microbiol., 1: 38-42.
Nunes Mdo, R; Magalhães, PP; Macêdo Ada, S; Franco, RT; Penna, FJ and Mendes, EN (2012). Attaching and effacing Escherichia coli and Shiga toxin-producing E. coli in children with acute diarrhoea and controls in Teresina/PI, Brazil. Trans. Roy. Soc. Trop. Medic. Hyg.,
106: 43-47.
Ramirez-Martinez, ML; Olmos-Ortiz, LM; Barajas-Mendiola, MA; Giono Cerezo, S; Avila, EE and Cuellar-Mata, P (2015). A PCR procedure for the detection of Giardia intestinalis cysts and Escherichia coli in lettuce. Lett. Appl. Microbiol., 60: 517-523.
Rúgeles, LC; Bai, J; Martínez, AJ; Vanegas, MC and Gómez-Duarte, OG (2010). Molecular characterization of diarrheagenic Escherichia coli strains from stools samples and food products in Colombia. Int. J. Food Microbiol., 138: 282-286.
Shirke, SS; Sukham, MD; Nashad, M; Pradeep, HD and Rahman, MR (2018). An overview of adoption of hygienic practices by fish marketing personnel in selected fish markets of Port Blair city, Andaman and Nicobar Islands. Indian J. Econom. Develop., 6: 1-6.
Stein, RA and Katz, DE (2017). Escherichia coli, cattle and the propagation of disease. FEMS Microbiol. Lett., 364: 1-11.
Vidal, M; Kruger, E; Durán, C; Lagos, R; Levine, M; Prado, V; Toro, C and Vidal, R (2005). Single multiplex PCR assay to identify simultaneously the six categories of diarrheagenic Escherichia coli associated with enteric infections. J. Clin. Microbiol., 43: 5362-5365.
Wang, L; Nakamura, H; Kage-Nakadai, E; Hara-Kudo, Y and Nishikawa, Y (2017). Prevalence, antimicrobial resistance and multiple-locus variable-number tandem-repeat analysis profiles of diarrheagenic Escherichia coli isolated from different retail foods. Int. J. Food Microbiol., 16: 44-52.