Investigating the presence and antibiotic susceptibilities of Escherichia coli O157 and Listeria monocytogenes in ruminant feces and feed in Balıkesir province

Abstract

The aim of this study is to determine the presence, virulence factors, and antibiotic susceptibilities of E. coli O157 and L. monocytogenes in ruminant feces and feed. This study was carried out for the first time in Balıkesir province. Feces, pellet feed, and silage samples were analyzed simultaneously for E. coli O157 and L. monocytogenes using feces of one gram and feed of twenty-five grams according to ISO 16654:2001/Amd 1:2017 and ISO 11290-1, respectively. 38 (38%) E. coli O157 strains were isolated and identified from a total of 100 ruminant feces. A total of 3 (3%) E. coli O157:H7 strains were detected by PCR from one hundred ruminant fecal samples. In the study, resistance to antibiotics increased, especially in E. coli O157 isolates. In this study, enterohaemolysin was the predominant virulence factor among the E. coli isolates, and it was thought that it was important for pathogenesis. The Sxt1 gene was higher than the Stx2 gene. A total of 24 L. monocytogenes strains were isolated from a total of 100 ruminant fecal samples and 50 silage samples. Three of these strains were isolated from silage samples taken from the farms, where L. monocytogenes was isolated from sheep feces. As a result, poor quality silage could be an important source of infection for listeriosis in Balıkesir province. Epidemiologically, poor quality silage was thought to be one of the sources of listeriosis. It was thought that ruminant feces played an important role as a reservoir in the spread and transmission of E. coli O157. The antibiotic resistance status of E. coli O157 and L. monocytogenes isolates should be monitored with epidemiological studies.

Keywords

• E.coli O157
• FECES
• listeria monocytogenes
• Silage
• virulence factors

References

1. Abay S, Aydın F (2005): Isolation and identification of Listeria spp. from faeces samples of healty cattle. J Health Sci, 14, 191-197.
2. Ahlstrom CA, Manuel CS, Den Bakker HC, et al (2018): Molecular ecology of Listeria spp., Salmonella, Escherichia coli O157:H7 and non-O157 Shiga toxin-producing E. coli in pristine natural environments in Northern Colorado. J Appl Microbiol, 124, 511–521.
3. Aksoy A, Sezer Ç, Vatansever L, et al (2018): Presence and antibiotic resistance of Listeria monocytogenes in raw milk and dairy products. Kafkas Üniv Vet Fak Derg, 24, 415-421.
4. Alan S, Altındiş M, Yaman H (2016): An investigation of Escherıchia coli O157: H7 and stx1/stx2 gene in faeces from cattle/diarrheic patients and some foods. Nobel Med, 12, 17-23.
5. Aydın F, İça T, Yontar A (2010): Investigation with conventional and molecular method of Escherichia coli O157:H7 in dairy cattle in Kayseri region. J Health Sci, 19, 159-166.
6. Aydin R, Gökmen M, Kara R, et al (2019): The prevalence and molecular characterization of Listeria monocytogenes in corn silage, feces and bulk tank milk samples in dairy cattle farms in Balikesir, Türkiye. Isr J Vet Med, 74, 184–189.
7. Bangieva DR, Rusev VN (2017): Prevalence of Listeria monocytogenes in raw cow milk – a review. Bulg J Vet Med, 20, 430–436.
8. Birdal E, Ak S (2018): Prevalence of E. coli O157:H7 in dairy cattle and the farm environment in the Marmara region of Türkiye. JAES, 3, 85-90.

9. Blanco JM, Blanco JE, Blanco A, et al (2001): Verocytotoxigenic Escherichia coli. In: Epidemiology of verocytotoxigenic Escherichia coli (vtec) in ruminants. (Duffy G, Garvey P, McDowell DA, Eds.), Food&Nutrition Press Inc., Trumbull, CT, USA, pp. 113-148.
10. BSAC (2013): Methods for antimicrobial susceptibility testing. Version 12 May 2013.
11. Caprioli A, Morabito S, Brugere H, et al (2005): Enterohaemorrhagic Escherichia coli: emerging issues on virulence and modes of transmission. Vet Res, 36, 289-311.
12. CLSI (2012): Performance standards for antimicrobial susceptibility testing; twenty second informational supplement M100-S22 (Vol. 32, No. 3). Wayne, PA, USA.
13. CLSI (2014): Performance standards for antimicrobial susceptibility testing; twenty forth informational supplement M100-S24. (Vol. 34, No. 1). Wayne, PA, USA.
14. CLSI (2021): Performance standards for antimicrobial susceptibility testing M100-ED31. 31st Ed. Wayne, PA, USA.
15. Czuprynski CJ (2005): Listeria monocytogenes: silage, sandwiches and science. Anim Health Res Rev, 6, 211-217.
16. Çiçek E (2008): Ege bölgesindeki sığırların süt ve dışkı örneklerinden Escherichia coli O157:H7 izolasyonu ve verotoksinlerinin belirlenmesi. Adnan Menderes Üniversitesi Sağlık Bilimleri Enstitüsü. Yüksek Lisans Tezi. Available at http://adudspace.adu.edu.tr:8080/ jspui/bitstream/11607/1368/3/Erdem%c3%87%c4%b0%c3%87EK-tez.pdf (Accessed September 29, 2021).
17. Datlı S, Onmaz Ertaş N (2018): Bir büyükbaş hayvan kesimhanesinde Escherichia coli O157:H7 varlığının ıms-pzr teknikleri ile araştırılması. Eurasian J Vet Sci, 34, 49-55.
18. Deka D, Roychoudhury P, Motina E, et al (2020): Detection of antimicrobial drug resistance in Listeria monocytogenes of cattle origin. Int J Chem Stud, 8, 2825–2829.
19. EFSA, ECDC (2021): The European Union One Health 2020 Zoonoses Report. EFSA J, 19, 324.
20. Ertaş N, Yıldırım Y, Karadal F, et al (2013): Hayvansal gıdalarda Escherichia coli O157:H7’nin önemi. Erciyes Üniv Vet Fak Derg, 10, 45-52.
21. Esteban JI, Oporto B, Aduriz G, et al (2009): Fecal shedding and strain diversity of Listeria monocytogenes in healthy ruminants and swine in Northern Spain. BMC Vet Res, 5, 1–10.
22. EUCAST (2021): Breakpoint tables for interpretation of MICs and zone diameters. Version 11.0. Available at https://www.eucast.org/fileadmin/src/media/PDFs/EUCAST_files/Breakpoint_tables/v_11.0_Breakpoint_Tables.pdf (Accessed September 29, 2021).
23. Ferdous M, Zhou K, Mellmann A, et al (2015): Is shiga toxin-negative Escherichia coli O157:H7 enteropathogenic or enterohemorrhagic Escherichia coli? comprehensive molecular analysis using whole-genome sequencing. J Clin Microbiol, 53, 3530-3538.
24. Garcia-Garcera M, Hafner L, Burucoa C, et al (2021): Listeria monocytogenes fecal carriage is common and driven by microbiota. BioRxiv, 2021.01.13.426560. Available at https://www.biorxiv.org/content/10.1101/ 2021.01.13.426560v1%0Ahttps://www.biorxiv.org/content/10.1101/2021.01.13.426560v1.abstract (Accessed September 29, 2021)
25. Gutema, FD, Rasschaert G, Agga GE, et al (2021): Occurrence, molecular characteristics, and antimicrobial resistance of Escherichia coli O157 in cattle, beef, and humans in Bishoftu Town, Central Ethiopia. Foodborne Pathog Dis, 18, 1–7.
26. Gülhan T (2003): Sağlıklı görünen hayvanların dışkılarından izole edilen Escherichia coli suşlarının biyokimyasal, enterotoksijenik ve verotoksijenik özelliklerinin belirlenmesi. YYÜ Vet Fak Derg, 14, 102-109.
27. Hurtado A, Ocejo M, Oporto B (2017): Salmonella spp. and Listeria monocytogenes shedding in domestic ruminants and characterization of potentially pathogenic strains. Vet Microbiol, 210, 71–76.
28. Igbinosa IH, Chiadika C (2021): Prevalence, characteristics and antibiogram profile of Escherichia coli O157:H7 isolated from raw and fermented (nono) milk in Benin City, Nigeria. Afr J Clin Exper Microbiol, 22, 223–233.
29. Iida T, Kanzaki M, Nakama A, et al (1998): Detection of Listeria monocytogenes in humans, animals and foods. J Vet Med Sci, 60, 1341-1343.
30. ISO (2017): 11290-1 Microbiology of the food chain — Horizontal method for the detection and enumeration of Listeria monocytogenes and of Listeria spp. — Part 1: Detection method.
31. ISO (2017): 16654 Microbiology of food and animal feeding stuffs — Horizontal method for the detection of Escherichia coli O157.
32. Jacop ME, Foster DM, Rogers AT, et al (2013): Prevalence and relatedness of Escherichia coli O157:H7 strains in the feces and on the hides and carcasses of U.S. meat goats at slaughter. J Appl Environ Microbiol, 79, 4154-4158.
33. Jafari E, Oloomi M, Bouzari S (2021): Characterization of antimicrobial susceptibility, extended-spectrum β-lactamase genes and phylogenetic groups of shigatoxin producing Escherichia coli isolated from patients with diarrhea in Iran. Ann Clin Microbiol Antimicrob, 20, 1–9.
34. Kalender H (2003): Detection of Listeria monocytogenes in faeces from chickens, sheep and cattle in Elaziǧ province. Turkish J Vet Anim Sci, 27, 449–451.
35. Kalender H (2013): Isolation, virulence genes and antimicrobial susceptibilities of shiga toxin-producing Escherichia coli O157 from slaughtered cattle in abattoirs and ground beef sold in Elazığ. Kafkas Univ Vet Fak Derg, 19, 461-467.
36. Kalorey DR, Kurkure NV, Warke SR, et al (2006): Isolation of pathogenic Listeria monocytogenes in faeces of wild animals in captivity. Comp Immun Microbiol Infect Dis, 29, 295–300.
37. Khalifa E, Nossair MA, Ayoub MA, et al (2019): Molecular characterization of diarrheagenic E. coli isolated from newly born calves and humans. AJVS, 60, 55-62.
38. Kuyucuoǧlu Y, Şeker E, Sareyyüpoǧlu B, et al (2011): Detection of enterohemolysin and intimin genes in Escherichia coli O157:H7 strains ısolated from calves and cattle in Afyonkarahisar-Türkiye. Kafkas Univ Vet Fak Derg, 17, 663-666.
39. Kuyucuoǧlu Y, Şeker E, Uǧuz C, et al (2011): Virulence genes of shiga toxin-producing Escherichia coli O157:H7 strains isolated from calves and cattle. Ank Univ Vet Fak Derg, 58, 255–260.
40. Lukasova J, Abraham B, Cupakova S (2004): Occurrence of Escherichia coli O157 in raw material and food in Czech Republic. J Vet Med, B51, 77-81.
41. Matto C, Varela G, Braga V, et al (2018): Detection of Listeria spp. in cattle and environment of pasture-based dairy farms. Pesqui Vet Bras, 38, 1736–1741.
42. McCabe E, Burgees CM, Lawal D, et al (2019): An investigation of shedding and super‐ shedding of shiga toxigenic Escherichia coli O157 and E. coli O26 in cattle presented for slaughter in the Republic of Ireland. Zoonoses Public Health, 66, 83–91.
43. Mersha G, Asrat D, Zewde BM, et al (2010): Occurrence of Escherichia coli O157:H7 in faeces, skin and carcasses from sheep and goats in Ethiopia. Lett App Microbiol, 50, 71-76.
44. Nobili G, Franconieri I, La Bella G, et al (2017): Prevalence of verocytotoxigenic Escherichia coli strains isolated from raw beef in southern Italy. Int J Food Microbiol, 257, 201-205.
45. Oxoid (2013): Manufacturer guidance for zone diameters of antibiotic discs.
46. Oyinloye MA, David OM, Famurewa O (2018): Pathogenic potential of Listeria monocytogenes isolated from cattle faeces in Adoekiti. African J Clin Exp Microbiol, 19, 104.
47. Philips CA (1999): The epidemiology, detection and control of Escherichia coli O157. J Sci Food Agric, 79, 1367- 1381.
48. Sanaa M, Poutrel B, Menard JL, et al (1993): Risk Factors associated with contamination of raw milk by Listerls monocytogenes in dairy farms. J Dairy Sci, 76, 2891-2898.
49. Şeker E, Kuş FS (2019): The prevalence, virulence factors and antibiotic resistance of Escherichia coli O157 in feces of adult ruminants slaughtered in three provinces of Türkiye. Vet Arh, 89, 107-121.
50. Şeker E, Kuyucuoǧlu Y, Sareyyüpoǧlu B, et al (2010): PCR detection of shiga toxins, enterohaemolysin and intimin virulence genes of Escherichia coli O157: H7 strains isolated from faeces of anatolian water buffaloes in Türkiye. Zoonoses Public Health, 57, 33–37.
51. Şeker E, Yardimci H (2008): First isolation of Escherichia coli O157:H7 from fecal and milk specimens from Anatolian water buffaloes (Bubalus bubalus) in Türkiye. J S Afr Vet Assoc, 79, 167–170.
52. Tchatchouang CDK, Fri J, De Santi M, et al (2020): Listeriosis outbreak in South Africa: a comparative analysis with previously reported cases worldwide. Microorganisms, 8.
53. Umar I, Shiaka GP, Aminu AU (2018): Phenotypic detection of Escherichia coli O157:H7 from faeces of slaughtered cattle in dutse abattoir. DUJOPAS, 4, 480-488.
54. Unnerstad H, Romell A, Ericsson H, et al (2000): Listeria monocytogenes in faeces from clinically healthy dairy cows in Sweden. Acta Vet Scand, 41, 167–171.
55. Vivant AL, Gamyn D, Piveteau P (2013): Listeria monocytogenes, a down-to-earth pathogen. Front Cell Infect Microbiol, 3, Article 87.
56. Weis J, Seeliger HPR (1975): Incidence of Listeria monocytogenes in nature. App Microbiol, 30, 29-32.