Evaluation of the frequency of Escherichia coli pathogroups in Brassica oleracea cultivars
,
Abstract
Background and Objectives: Pathogenic diseases resulting from microbial contamination of food have been widely distributed in many parts of the world. Among these, Escherichia coli is one of the most important foodborne pathogenic bacteria. Diarrhea is one of the major causes of children’s death in developing countries, with approximately 2 million deaths annually. The current study aimed to determine the frequency of diarrheagenic E. coli pathotypes such as Enteropathogenic E. coli (EPEC), Enterotoxigenic E. coli (ETEC), Enteroaggregative E. coli (EAEC), and Shiga toxin-producing E. coli (STEC) in Brassica oleracea cultivars in order to provide information on the assessment of diarrheagenic E. coli pathogenesis risk.
Materials and Methods: 100 samples of vegetables were collected in Tehran, including cabbage, cauliflower, broccoli and Brussels sprouts. After homogenizing samples, enrichment was done in the EC broth medium. Five colonies of pure culture were used for DNA extraction. Pathotypes were identified by PCR using virulence genes.
Results: The results showed that the prevalence of diarrheagenic E. coli strains was 7%. The EPEC prevalence was 3%, All EPEC isolates were atypical. The ETEC frequency was 3%, And the EAEC prevalence was 1%.
Conclusion: These findings indicated that Brassica oleracea cultivars could be consideredas a source of contamination with diarrhea-causing E. coli strains.
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10. 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.
11. Svenungsson B, Lagergren A, Ekwall E, Evengård B, Hedlund KO, Kärnell A, et al. Enteropathogens in adult patients with diarrhea and healthy control subjects: a 1-year prospective study in a Swedish clinic for infectious diseases. Clin Infect Dis 2000; 30:770-778.
12. El-Jakee J, Moussa EI, Mohamed KF, Mohamed G. Using molecular techniques for characterization of Escherichia coli isolated from water sources in Egypt. Global Veterinaria 2009; 3: 354-362.
13. Sobur MA, Sabuj AAM, Sarker R, Rahman AMMT, Kabir SML, Rahman MT. Antibiotic-resistant Escherichia coli and Salmonella spp. associated with dairy cattle and farm environment having public health significance. Vet World 2019; 12: 984-993.
14. Herman KM. Hall AJ, Gould LH. Outbreaks attributed to fresh leafy vegetables, United States, 1973-2012. Epidemiol Infect 2015; 143: 3011-3021.
15. González J, Cadona JS, Sanz M, Bustamante AV, Sanso AM. Molecular characterization of diarrheagenic Escherichia coli isolated from vegetables in Argentina. Int J Food Microbiol 2017; 261: 57-61.
16. Waturangi DE, Hudiono F, Aliwarga E. Prevalence of pathogenic Escherichia coli from salad vegetable and fruits sold in Jakarta. BMC Res Notes 2019; 12: 247.
17. Skočková A, Karpíšková R, Koláčková I, Cupáková Š. Characteristics of Escherichia coli from raw vegetables at a retail market in the Czech Republic. Int J Food Microbiol 2013; 167: 196-201.
18. Dias RC, dos Santos BC, dos Santos LF, Vieira MA, Yamatogi RS, Mondelli AL, et al. Diarrheagenic Escherichia coli pathotypes investigation revealed atypical enteropathogenic E. coli as putative emerging diarrheal agents in children living in Botucatu, São Paulo State, Brazil. APMIS 2016; 124: 299-308.
19. Contreras CA, Ochoa TJ, Lacher DW, DebRoy C, Navarro A, Talledo M, et al. Allelic variability of critical virulence genes (eae, bfpA and perA) in typical and atypical enteropathogenic Escherichia coli in Peruvian children. J Med Microbiol 2010; 59: 25-31.
20. Yatsuyanagi J, Saito S, Miyajima Y, Amano KI, Enomoto K. Characterization of atypical enteropathogenic Escherichia coli strains harboring the astA gene that were associated with a waterborne outbreak of diarrhea in Japan. J clin Microbiol 2003; 41: 2033-2039.
21. Nguyen RN, Taylor LS, Tauschek M, Robins-Browne RM. Atypical enteropathogenic Escherichia coli infection and prolonged diarrhea in children. Emerg Infect Dis 2006; 12: 597-603.
22. Zhang S, Wu Q, Zhang J, Lai Z, Zhu X. Prevalence, genetic diversity, and antibiotic resistance of enterotoxigenic Escherichia coli in retail ready-to-eat foods in China. Food Control 2016; 68: 236-243.
23. Gómez-Aldapa CA, Rangel-Vargas E, Bautista-De León H, Castro-Rosas J. Presence of non-O157 Shiga toxin-producing Escherichia coli, enterotoxigenic E. coli, enteropathogenic E. coli and Salmonella in fresh beetroot (Beta vulgaris L.) juice from public markets in Mexico. J Sci Food Agric 2014; 94: 2705-2711.
24. Lee GY, Jang HI, Hwang IG, Rhee MS. Prevalence and classification of pathogenic Escherichia coli isolated from fresh beef, poultry, and pork in Korea. Int J Food Microbiol 2009; 134: 196-200.
25. Dell'Orco F, Gusmara C, Loiacono M, Gugliotta T, Albonico F, Mortarino M, et al. Evaluation of virulence factors profiles and antimicrobials resistance of Escherichia coli isolated from bulk tank milk and raw milk filters. Res Vet Sci 2019; 123: 77-83.
26. Mirhoseini A, Amani J, Nazarian S. Review on pathogenicity mechanism of enterotoxigenic Escherichia coli and vaccines against it. Microb Pathog 2018; 117: 162-169.
27. Kaur P, Chakraborti A, Asea A. Enteroaggregative Escherichia coli: an emerging enteric food borne pathogen. Interdiscip Perspect Infect Dis 2010; 2010: 254159.
28. de Quadros Rodrigues R, Loiko MR, de Paula CMD, Hessel CT, Jacxsens L, Uyttendaele M, et al. Microbiological contamination linked to implementation of good agricultural practices in the production of organic lettuce in Southern Brazil. Food Control 2014; 42: 152-164.
29. Mukherjee A, Speh D, Dyck E, Diez-Gonzalez F. Preharvest evaluation of coliforms, Escherichia coli, Salmonella, and Escherichia coli O157: H7 in organic and conventional produce grown by Minnesota farmers. J Food Prot 2004; 67: 894-900.
30. Mazaheri S, Salmanzadeh Ahrabi S, Aslani MM. Shiga toxin-producing Escherichia coli isolated from lettuce samples in Tehran, Iran. Jundishapur J Microbiol 2014; 7(11): e12346.
31. Kochakkhani H, Dehghan P, Mousavi MH, Sarmadi B. Occurrence, molecular detection and antibiotic resistance profile of Escherichia coli O157: H7 isolated from ready-to-eat vegetable salads in Iran. Pharml Sci 2016; 22: 195-202.
32. 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(5): e62288.
33. Özpınar H, Turan B, Tekiner İH, Tezmen G, Gökçe İ, Akıneden Ö. Evaluation of pathogenic Escherichia coli occurrence in vegetable samples from district bazaars in Istanbul using real‐time PCR. Lett Appl Microbiol 2013; 57: 362-367.
34. Mohammadi P, Abiri R. Isolation of Enteropathogenic Escherichia coli (EPEC) from raw milk in Kermanshah by polymerase chain reaction (PCR). Jundishapur J Microbiol 2013; 6(4): e5439.
35. Philipsborn R, Ahmed SM, Brosi BJ, Levy K. Climatic drivers of diarrheagenic Escherichia coli incidence: a systematic review and meta-analysis. J Infect Dis 2016; 214: 6-15.
36. Gonzales L, Joffre E, Rivera R, Sjöling Å, Svennerholm AM, Iñiguez V. Prevalence, seasonality and severity of disease caused by pathogenic Escherichia coli in children with diarrhoea in Bolivia. J Med Microbiol 2013; 62: 1697-1706.
37. Mohammadzadeh M, Goudarzi H, Dabiri H, Fallah F. Characterization of enteropathogenic Escherichia coli associated with diarrhea among Iranian infants. Arch Pediat Infect Dis 2016; 5(1): e36920.
2. Kaper JB, Nataro JP, Mobley HL. Pathogenic Escherichia coli. Nat Rev Microbiol 2004; 2: 123-140.
3. Canizalez-Roman A, Gonzalez-Nuñez E, Vidal JE, Flores-Villaseñor H, León-Sicairos N. Prevalence and antibiotic resistance profiles of diarrheagenic Escherichia coli strains isolated from food items in northwestern Mexico. Int J Food Microbiol 2013; 164: 36-45.
4. Kapusta-Duch J, Kopec A, Piatkowska E, Borczak B, Leszczynska T. The beneficial effects of Brassica vegetables on human health. Rocz Panstw Zakl Hig 2012; 63: 389-395.
5. Abadias M, Usall J, Anguera M, Solsona C, Viñas I. Microbiological quality of fresh, minimally-processed fruit and vegetables, and sprouts from retail establishments. Int J Food Microbiol 2008; 123: 121-129.
6. Ekici G, Dümen E (2019). Escherichia coli and food safety. In: The universe of Escherichia coli. Ed, MS Erjavec. IntechOpen publishing, 1st ed. London, UK, pp 85-100.
7. Alegbeleye OO, Singleton I, Sant'Ana AS. Sources and contamination routes of microbial pathogens to fresh produce during field cultivation: a review. Food Microbiol 2018; 73: 177-208.
8. Feng P, Weagant SD, Jinneman K. BAM: diarrheagenic Escherichia coli. Silver Spring, MD: United States Food and Drug Administration 2011.
9. Kim HJ, Koo M, Jeong AR, Baek SY, Cho JI, Lee SH, et al. Occurrence of pathogenic Escherichia coli in commercially available fresh vegetable products in Korea. J Korean Soc Appl Biol Chem 2014; 57: 367-70.
10. 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.
11. Svenungsson B, Lagergren A, Ekwall E, Evengård B, Hedlund KO, Kärnell A, et al. Enteropathogens in adult patients with diarrhea and healthy control subjects: a 1-year prospective study in a Swedish clinic for infectious diseases. Clin Infect Dis 2000; 30:770-778.
12. El-Jakee J, Moussa EI, Mohamed KF, Mohamed G. Using molecular techniques for characterization of Escherichia coli isolated from water sources in Egypt. Global Veterinaria 2009; 3: 354-362.
13. Sobur MA, Sabuj AAM, Sarker R, Rahman AMMT, Kabir SML, Rahman MT. Antibiotic-resistant Escherichia coli and Salmonella spp. associated with dairy cattle and farm environment having public health significance. Vet World 2019; 12: 984-993.
14. Herman KM. Hall AJ, Gould LH. Outbreaks attributed to fresh leafy vegetables, United States, 1973-2012. Epidemiol Infect 2015; 143: 3011-3021.
15. González J, Cadona JS, Sanz M, Bustamante AV, Sanso AM. Molecular characterization of diarrheagenic Escherichia coli isolated from vegetables in Argentina. Int J Food Microbiol 2017; 261: 57-61.
16. Waturangi DE, Hudiono F, Aliwarga E. Prevalence of pathogenic Escherichia coli from salad vegetable and fruits sold in Jakarta. BMC Res Notes 2019; 12: 247.
17. Skočková A, Karpíšková R, Koláčková I, Cupáková Š. Characteristics of Escherichia coli from raw vegetables at a retail market in the Czech Republic. Int J Food Microbiol 2013; 167: 196-201.
18. Dias RC, dos Santos BC, dos Santos LF, Vieira MA, Yamatogi RS, Mondelli AL, et al. Diarrheagenic Escherichia coli pathotypes investigation revealed atypical enteropathogenic E. coli as putative emerging diarrheal agents in children living in Botucatu, São Paulo State, Brazil. APMIS 2016; 124: 299-308.
19. Contreras CA, Ochoa TJ, Lacher DW, DebRoy C, Navarro A, Talledo M, et al. Allelic variability of critical virulence genes (eae, bfpA and perA) in typical and atypical enteropathogenic Escherichia coli in Peruvian children. J Med Microbiol 2010; 59: 25-31.
20. Yatsuyanagi J, Saito S, Miyajima Y, Amano KI, Enomoto K. Characterization of atypical enteropathogenic Escherichia coli strains harboring the astA gene that were associated with a waterborne outbreak of diarrhea in Japan. J clin Microbiol 2003; 41: 2033-2039.
21. Nguyen RN, Taylor LS, Tauschek M, Robins-Browne RM. Atypical enteropathogenic Escherichia coli infection and prolonged diarrhea in children. Emerg Infect Dis 2006; 12: 597-603.
22. Zhang S, Wu Q, Zhang J, Lai Z, Zhu X. Prevalence, genetic diversity, and antibiotic resistance of enterotoxigenic Escherichia coli in retail ready-to-eat foods in China. Food Control 2016; 68: 236-243.
23. Gómez-Aldapa CA, Rangel-Vargas E, Bautista-De León H, Castro-Rosas J. Presence of non-O157 Shiga toxin-producing Escherichia coli, enterotoxigenic E. coli, enteropathogenic E. coli and Salmonella in fresh beetroot (Beta vulgaris L.) juice from public markets in Mexico. J Sci Food Agric 2014; 94: 2705-2711.
24. Lee GY, Jang HI, Hwang IG, Rhee MS. Prevalence and classification of pathogenic Escherichia coli isolated from fresh beef, poultry, and pork in Korea. Int J Food Microbiol 2009; 134: 196-200.
25. Dell'Orco F, Gusmara C, Loiacono M, Gugliotta T, Albonico F, Mortarino M, et al. Evaluation of virulence factors profiles and antimicrobials resistance of Escherichia coli isolated from bulk tank milk and raw milk filters. Res Vet Sci 2019; 123: 77-83.
26. Mirhoseini A, Amani J, Nazarian S. Review on pathogenicity mechanism of enterotoxigenic Escherichia coli and vaccines against it. Microb Pathog 2018; 117: 162-169.
27. Kaur P, Chakraborti A, Asea A. Enteroaggregative Escherichia coli: an emerging enteric food borne pathogen. Interdiscip Perspect Infect Dis 2010; 2010: 254159.
28. de Quadros Rodrigues R, Loiko MR, de Paula CMD, Hessel CT, Jacxsens L, Uyttendaele M, et al. Microbiological contamination linked to implementation of good agricultural practices in the production of organic lettuce in Southern Brazil. Food Control 2014; 42: 152-164.
29. Mukherjee A, Speh D, Dyck E, Diez-Gonzalez F. Preharvest evaluation of coliforms, Escherichia coli, Salmonella, and Escherichia coli O157: H7 in organic and conventional produce grown by Minnesota farmers. J Food Prot 2004; 67: 894-900.
30. Mazaheri S, Salmanzadeh Ahrabi S, Aslani MM. Shiga toxin-producing Escherichia coli isolated from lettuce samples in Tehran, Iran. Jundishapur J Microbiol 2014; 7(11): e12346.
31. Kochakkhani H, Dehghan P, Mousavi MH, Sarmadi B. Occurrence, molecular detection and antibiotic resistance profile of Escherichia coli O157: H7 isolated from ready-to-eat vegetable salads in Iran. Pharml Sci 2016; 22: 195-202.
32. 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(5): e62288.
33. Özpınar H, Turan B, Tekiner İH, Tezmen G, Gökçe İ, Akıneden Ö. Evaluation of pathogenic Escherichia coli occurrence in vegetable samples from district bazaars in Istanbul using real‐time PCR. Lett Appl Microbiol 2013; 57: 362-367.
34. Mohammadi P, Abiri R. Isolation of Enteropathogenic Escherichia coli (EPEC) from raw milk in Kermanshah by polymerase chain reaction (PCR). Jundishapur J Microbiol 2013; 6(4): e5439.
35. Philipsborn R, Ahmed SM, Brosi BJ, Levy K. Climatic drivers of diarrheagenic Escherichia coli incidence: a systematic review and meta-analysis. J Infect Dis 2016; 214: 6-15.
36. Gonzales L, Joffre E, Rivera R, Sjöling Å, Svennerholm AM, Iñiguez V. Prevalence, seasonality and severity of disease caused by pathogenic Escherichia coli in children with diarrhoea in Bolivia. J Med Microbiol 2013; 62: 1697-1706.
37. Mohammadzadeh M, Goudarzi H, Dabiri H, Fallah F. Characterization of enteropathogenic Escherichia coli associated with diarrhea among Iranian infants. Arch Pediat Infect Dis 2016; 5(1): e36920.
| Files | ||
| Issue | Vol 14 No 1 (2022) | |
| Section | Original Article(s) | |
| DOI | https://doi.org/10.18502/ijm.v14i1.8808 | |
| Keywords | ||
| Diarrheagenic Escherichia coli; Virulent genes; Raw vegetables; Brassica oleracea | ||
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This work is licensed under a Creative Commons Attribution-NonCommercial 4.0 International License. |
How to Cite
1.
Razeh F, Salmanzadeh-Ahrabi S, Zarei R, Attaran B. Evaluation of the frequency of Escherichia coli pathogroups in Brassica oleracea cultivars. Iran J Microbiol. 2022;14(1):84-89.
