Prevalence and Antibacterial Susceptibility Pattern of Escherichia Coli in Fermented Cow Milk Collected from Selected Markets in Maiduguri, Borno State.

Escherichia coli is an enteric food borne pathogen associated with life-threatening disease conditions. The enterobacteria are frequently found in the cattle gastrointestinal tract with a high potential of contaminated animal products such as milk, meat, and cheese. A cross-sectional study was conducted to investigate the presence of Escherichia coli. in fermented milk products sold within Maiduguri, Borno State. Thirty (30) samples were collected from different sources Bacteriological isolation and biochemical characterization yielded Escherichia coli and the prevalence of E. coli was 3.33 % (2/60). Antibacterial susceptibility test was carried out and the bacteria were sensitive to ciprofloxacin (17 mm) and gentamycin (21 mm), while the remaining antibiotics were non sensitive, i.e. cephalexin, cefoxitin and suphamethoxazole-trimethoprim. Based on EUCAST the isolates were resistant to all the antibiotics except gentamycin. The result revealed the presence of Escherichia coli in the fermented cow milk samples. The finding indicates possible faecal contamination of the milk product with serious public health consequences. This necessitates the need to screen other milk products in the area. Health authorities in the state need to enlighten dairy product farmers on the zoonotic potential of Escherichia coli.

Escherichia coli, Fermented milk, Antimicrobial susceptibility, Foodborne pathogens, Public health

1. Bat. C. A. (2014). Escherichia Coli: Escherichia coli. In Encyclopedia of Food Microbiology: Second Edition (pp. 688-694). https://doi.org/10.1016/B978-0-12-384730-0.00100-2 [Google Scholar] [Crossref]

2. Bentley R. and Meganathan R, (1982). Biosynthesis of vitamin K (menaquinone) in bacteria. Microbiological Reviews. 46 (3):241-280. [Google Scholar] [Crossref]

3. Bharathi, M. Jayahar, Ramakrishnan, R., Vasu, S., Meenakshi, R., & Palaniappan, R. (2002). In vitro efficacy of antibacterials against bacterial pathogens from corneal ulcers. Indian Journal of Ophthalmology, 50(2), 109-114. [Google Scholar] [Crossref]

4. Brenner DJ. Krieg NR, and Staley JT, (2005). The Gammaproteobacteria. Bergey's Manual of Systematic Bacteriology. 2B (2nd ed.). New York: Springer. 1108.14. [Google Scholar] [Crossref]

5. Brooks, G. F., Carroll, K. C., Butel, J. S., Morse, S. A., & Mietzner, T. A. (2022). Jawetz, Melnick & Adelberg’s medical microbiology (29th ed.). McGraw-Hill Education. [Google Scholar] [Crossref]

6. Brumfitt W and Hamilton-Miller JM (1993). Reassessment of the rationale for the combinations of sulphonamides with diaminopyrimidines. London. Journal of Chemotherapy. 5 (6): 465-469. [Google Scholar] [Crossref]

7. Cappuccino, J. G., & Sherman, N. (2018). Microbiology: A laboratory manual (11th ed.). Pearson Education. [Google Scholar] [Crossref]

8. Centers for Disease Control and Prevention (CDC). (2024). E. coli (Escherichia coli) infection. U.S. Department of Health and Human Services. https://www.cdc.gov/ecoli/index.html [Google Scholar] [Crossref]

9. Cheesbrough, M. (2010). District laboratory practice in tropical countries (2nd ed.). Cambridge University Press. [Google Scholar] [Crossref]

10. Cheesebrough M, (2005). District Laboratory Practice in Tropical countries, part 2. Cambridge University Press. 178-187 [Google Scholar] [Crossref]

11. Collee, J. G., Fraser, A. G., Marmion, B. P., & Simmons, A. (1996). Mackie and McCartney practical medical microbiology (14th ed.). Churchill Livingstone. [Google Scholar] [Crossref]

12. Comelis P, (2000). Expressing genes in different Escherichia coli compartments. in Belgium. [Google Scholar] [Crossref]

13. Croxen, M. A., Law, R. J., Scholz, R., Keeney, K. M., Wlodarska, M., & Finlay, B. B. (2013). Recent advances in understanding enteric pathogenic Escherichia coli. Clinical Microbiology Reviews, 26(4), 822–880. https://doi.org/10.1128/CMR.00022-13 [Google Scholar] [Crossref]

14. Davies, J., & Davies, D. (2010). Origins and evolution of antibiotic resistance. Microbiology and Molecular Biology Reviews, 74(3), 417–433. https://doi.org/10.1128/MMBR.00016-10 [Google Scholar] [Crossref]

15. Dean, P., Maresca, M., & Kenny, B. (2005). EPEC’s interactions with host cells: Revealing the strategies of a top bacterial pathogen. Trends in Microbiology, 13(8), 456–463. https://doi.org/10.1016/j.tim.2005.07.008 [Google Scholar] [Crossref]

16. Donnenberg, M. S. (2015). Escherichia coli: Pathotypes and principles of pathogenesis (2nd ed.). Academic Press. [Google Scholar] [Crossref]

17. Fasce, V., Chieffi, D., Fanelli, F., logrieco, A. F., Cho, G.-S., Kabisch, J., Bohnlein, C., & Franz, С. М. А. Р. (2020). Microbial quality and safety of milk and milk products in the 21 century. Comprehensive reviews in food science and food safety, 19(4), 2013-2049. [Google Scholar] [Crossref]

18. Feng P, Weagant S, and Grant M. (2002). Enumeration of Escherichia coli and the Coliform Bacteria. Bacteriological Analytical Manual (8th Ed). FDA/Centrefor Food Safety & Applied Nutrition. Retrieved 2007: 01-25.12. [Google Scholar] [Crossref]

19. Forbes, B. A., Sahm, D. F., & Weissfeld, A. S. (2022). Bailey & Scott’s diagnostic microbiology (15th ed.). Elsevier. [Google Scholar] [Crossref]

20. Forbes, B. A., Sahm, D. F., & Weissfeld, A. S. (2022). Bailey & Scott’s diagnostic microbiology (15th ed.). Elsevier. [Google Scholar] [Crossref]

21. Forbes, B. A., Sahm, D. F., & Weissfeld, A. S. (2022). Bailey & Scott’s diagnostic microbiology (15th ed.). Elsevier. [Google Scholar] [Crossref]

22. Fotadar U, Zaveloff and Terracio 1., (2005), Growth of Escherichia coli at elevated temperatures. Journal of Basic Microbiology. 45(5) 403-404, [Google Scholar] [Crossref]

23. Frank, C., Werber, D., Cramer, J. P., Askar, M., Faber, M., Heiden, M. A., Bernard, H., Fruth, A., Prager, R., Spode, A., Wadl, M., Zoufaly, A., Jordan, S., Kemper, M. J., Follin, P., Müller, L., King, L. A., Rosner, B., Buchholz, U., Stark, K., & Krause, G. (2011). Epidemic profile of Shiga-toxin–producing Escherichia coli O104:H4 outbreak in Germany. New England Journal of Medicine, 365(19), 1771–1780. https://doi.org/10.1056/NEJMoa1106483 [Google Scholar] [Crossref]

24. Frohlicher, G. Krause. C. Zweifel. 1. Beutin, and R. Stephan, (2008) "Characterization of attaching and effacing Escherichia coli(AEEC) isolated from pigs and sheep." BMC Microbiology, vol.8, article 144, [Google Scholar] [Crossref]

25. Frost, L. S., Leplae, R., Summers, A. O., & Toussaint, A. (2005). Mobile genetic elements: The agents of open source evolution. Nature Reviews Microbiology, 3(9), 722–732. https://doi.org/10.1038/nrmicro1235 [Google Scholar] [Crossref]

26. Gaastra, W., & Svennerholm, A. M. (1996). Colonization factors of human enterotoxigenic Escherichia coli (ETEC). Trends in Microbiology, 4(11), 444–452. https://doi.org/10.1016/0966-842X(96)10068-7 [Google Scholar] [Crossref]

27. Garau J (2008). Other antimicrobials of interest in the era of extended-spectrum beta-lactamases: fosfomycin, nitrofurantoin, and tigecycline. Journal Clinical of Microbiology and infection. 14 (1), 198-202. [Google Scholar] [Crossref]

28. Grozdanov L., Raasch C, Schulze J, Sonnenborn U, Gottschalk G. Hacker J and Dobrindt U (2004). Analysis of the genome structure of the non-pathogenic probiotic Escherichia coli strain Nissle 1917. Journal of Bacteriology. 186 (16): pp5432-5441. [Google Scholar] [Crossref]

29. Gupta K. Hooton TM, Naber KG, Wullt B, Colgan R, Miller LG, Moran GJ, Nicolle LE, Raz R. Schaeffer AJ and Soper D E (2011). International Clinical Practice Guidelines for the Treatment of Acute Uncomplicated Cystitis and Pyelonephritis in Women: A 2010 Update by the Infectious Diseases Society of America and the European Society for Microbiology and Infectious Diseases. Clinical Infectious Diseases 52 (5): e103-e120. [Google Scholar] [Crossref]

30. H. Karch, P. 1. Tarr, and M. Bielaszewska, "Enterohaemorrhagic Escherichia coli in human medicine," International Journal of Medical Microbiology, vol. 295, no. 6-7, pp. 405-418,2005. [Google Scholar] [Crossref]

31. Harrington, S. M., Dudley, E. G., & Nataro, J. P. (2006). Pathogenesis of enteroaggregative Escherichia coli infection. FEMS Microbiology Letters, 254(1), 12–18. https://doi.org/10.1111/j.1574-6968.2005.00005.x [Google Scholar] [Crossref]

32. Haug, A., Christophersen, O. A., Høstmark, A. T., & Harstad, O. M. (2007). Milk and health. Tidsskrift for Den Norske Laegeforening. 127(19),2542-2545. https://doi.org/10.1056/nejmra1903547 [Google Scholar] [Crossref]

33. Holko, T. Borisova, Z. Holkova, and V. Kmet, (2006) "Virulence markers of Escherichia coli strains isolated from traditional cheeses made from unpasteurized sheep milk in Slovakia, "Food Control, vol. 17, no. 5, pp. 393-396.. [Google Scholar] [Crossref]

34. Hudault S, Guignot J,and Servin AL. (2001). Escherichia coli strains colonizing the gastrointestinal tract protect germ-free mice against Salmonella typhimurium infection Pp. 49 (1) 47-55. [Google Scholar] [Crossref]

35. Jayaraman, Sathishkumar, Manoharan M, Ilanchezian S, Sekher R, and Sathyamurthy, (2012). Plasmid analysis and prevalence of Multidrugresistant Staphylococcus aureus reservoirs in Chennai city, India. Journal Clinical Microbiology and infection. 14(7):143-151. [Google Scholar] [Crossref]

36. Johnson, J. R., & Russo, T. A. (2005). Molecular epidemiology of extraintestinal pathogenic (uropathogenic) Escherichia coli. International Journal of Medical Microbiology, 295(6-7), 383–404. https://doi.org/10.1016/j.ijmm.2005.07.005 [Google Scholar] [Crossref]

37. Joseph F. Sullivan Center. (2020). Dairy products and nutrition overview. Clemson University. Retrieved from https://www.clemson.edu/health/sullivan-center/ [Google Scholar] [Crossref]

38. Joseph F. Sullivan Center. (2020). Dairy products and their nutritional importance. Clemson University. https://www.clemson.edu/centers-institutes/sullivan-center [Google Scholar] [Crossref]

39. Kaper, J. B., Nataro, J. P., & Mobley, H. L. T. (2004). Pathogenic Escherichia coli. Nature Reviews Microbiology, 2(2), 123–140. https://doi.org/10.1038/nrmicro818 [Google Scholar] [Crossref]

40. Kaper, J. B., Nataro, J. P., & Mobley, H. L. T. (2004). Pathogenic Escherichia coli. Nature Reviews Microbiology, 2(2), 123–140. https://doi.org/10.1038/nrmicro818 [Google Scholar] [Crossref]

41. Lan, R., Alles, M. C., Donohoe, K., Martinez, M. B., & Reeves, P. R. (2004). Molecular evolutionary relationships of enteroinvasive Escherichia coli and Shigella spp. Infection and Immunity, 72(9), 5080–5088. https://doi.org/10.1128/IAI.72.9.5080-5088.2004 [Google Scholar] [Crossref]

42. Leclercq, R., & Courvalin, P. (2002). Resistance to macrolides and related antibiotics in Streptococcus pneumoniae. Antimicrobial Agents and Chemotherapy, 46(9), 2727–2734. https://doi.org/10.1128/AAC.46.9.2727-2734.2002 [Google Scholar] [Crossref]

43. Lederberg, Joshua EL and Tatum (1946). "Gene recombination in E.coli" (PDF). Nature.158 [Google Scholar] [Crossref]

44. Lee M. Bozzo P. Einarson A and Koren G (2008). "Urinary tract infections in pregnancy", [Google Scholar] [Crossref]

45. Leimbach, A., Hacker, J., & Dobrindt, U. (2013). E. coli as an all-rounder: The thin line between commensalism and pathogenicity. Current Topics in Microbiology and Immunology, 358, 3–32. https://doi.org/10.1007/82_2012_303 [Google Scholar] [Crossref]

46. Leimbach, A., Hacker, J., & Dobrindt, U. (2013). E. coli as an all-rounder: The thin line between commensalism and pathogenicity. Current Topics in Microbiology and Immunology, 358, 3–32. https://doi.org/10.1007/82_2012_303 [Google Scholar] [Crossref]

47. Levin, B. R., Baquero, F., & Ankomah, P. (2017). Phylogenetics and population biology of bacterial resistance. In F. Baquero, R. Cantón, & G. Lanza (Eds.), Antibiotic resistance: Origins, evolution, selection and spread (pp. 45–67). Springer. [Google Scholar] [Crossref]

48. Lodinová Zádníková R. Cukrowska B and Tlaskalova-Hogenova H. (2003). "Oral administration of probiotic Escherichia coli after birth reduces frequency of allergies and repeated infections later in life (after 10 and 20 years)". International Archives of Allergy and Immunology. 131 (3): 209-211. [Google Scholar] [Crossref]

49. Madigan MT and Martinko JM (2006). Brock Biology of Microorganisms (11th Ed). SouthernIllinois University. Pearson. Pp. 420-430. [Google Scholar] [Crossref]

50. Madigan, M. T., Bender, K. S., Buckley, D. H., Sattley, W. M., & Stahl, D. A. (2022). Brock biology of microorganisms (16th ed.). Pearson Education. [Google Scholar] [Crossref]

51. Madigan, M. T., Bender, K. S., Buckley, D. H., Sattley, W. M., & Stahl, D. A. (2022). Brock biology of microorganisms (16th ed.). Pearson Education. [Google Scholar] [Crossref]

52. March, S. B., & Ratnam, S. (1986). Sorbitol-MacConkey medium for detection of Escherichia coli O157:H7 associated with hemorrhagic colitis. Journal of Clinical Microbiology, 23(5), 869–872. https://doi.org/10.1128/jcm.23.5.869-872.1986 [Google Scholar] [Crossref]

53. Migula W, EnglerA, PrantIK, Teill,andAbteilungl. (1985). Bacteriaceae (stabchenbacterien) Die Naturlichen Pfanzen familien, pp. 20-3.Kashef N, David GE and Shahbazi S (2010). [Google Scholar] [Crossref]

54. Nataro, J. P., & Kaper, J. B. (1998). Diarrheagenic Escherichia coli. Clinical Microbiology Reviews, 11(1), 142–201. https://doi.org/10.1128/CMR.11.1.142 [Google Scholar] [Crossref]

55. Nataro, J. P., & Kaper, J. B. (1998). Diarrheagenic Escherichia coli. Clinical Microbiology Reviews, 11(1), 142–201. https://doi.org/10.1128/CMR.11.1.142 [Google Scholar] [Crossref]

56. Nataro, J. P., Yikang, D., Yingkang, D., & Walker, K. (1995). AggR, a transcriptional activator of enteroaggregative Escherichia coli virulence plasmid genes. Journal of Bacteriology, 177(20), 3499–3503. https://doi.org/10.1128/jb.177.20.3499-3503.1995 [Google Scholar] [Crossref]

57. Nordeng H. Lupattelli A, Romeren M and Koren, G (2013). "Neonatal outcomes after gestational exposure to nitrofurantoin". Obstetrics and gynaecology121 (2 Pt 1): 306-313. [Google Scholar] [Crossref]

58. Paterson DL and Bonomo RA (2005). "Extended-spectrum beta-lactamases: a clinical update". Clinical Microbiology Reviews. 18 (4): 657-686. [Google Scholar] [Crossref]

59. Perfeito L. Fernandes L. Mota C and Gordo I (2007). "Adaptive Mutations in Bacteria: High Rate and Small Effects". Science. 317 (5839): 813-815. [Google Scholar] [Crossref]

60. Prescott LM. John PH and Donald AK (2005), Microbiology 16th Ed. Arizona. McGraw Hill. Pp.485-783. [Google Scholar] [Crossref]

61. Prescott, L. M., Harley, J. P., & Klein, D. A. (2020). Prescott’s microbiology (11th ed.). McGraw-Hill Education. [Google Scholar] [Crossref]

62. Proft, T., & Baker, E. N. (2009). Pili in Gram-negative and Gram-positive bacteria—Structure, assembly, and their role in disease. Cellular and Molecular Life Sciences, 66(4), 613–635. https://doi.org/10.1007/s00018-008-8477-4 [Google Scholar] [Crossref]

63. Qadri, F., Svennerholm, A. M., Faruque, A. S. G., & Sack, R. B. (2005). Enterotoxigenic Escherichia coli in developing countries: Epidemiology, microbiology, clinical features, treatment, and prevention. Clinical Microbiology Reviews, 18(3), 465–483. https://doi.org/10.1128/CMR.18.3.465-483.2005 [Google Scholar] [Crossref]

64. Russell JB, Jarvis GN (2001). "Practical mechanisms for interrupting the oral-faecal lifecycle of Escherichia coli". Journal of Molecular Microbiology and Biotechnology. 3 (2): 265272. [Google Scholar] [Crossref]

65. Russo E. (2003). "The birth of biotechnology". Nature. 421 (6921): 456-457. [Google Scholar] [Crossref]

66. Salyers AA, Gupta A and Wang Y (2004). "Human intestinal bacteria as reservoirs for antibioticresistance genes". Trends Microbiology. 12 (9): 412-416. [Google Scholar] [Crossref]

67. Sansonetti, P. J. (2001). Microbes and microbial toxins: Paradigms for microbial–mucosal interactions I. Shigella interactions with the intestinal epithelium. American Journal of Physiology–Gastrointestinal and Liver Physiology, 280(3), G319–G323. https://doi.org/10.1152/ajpgi.2001.280.3.G319 [Google Scholar] [Crossref]

68. Singleton P. (1999). Bacteria in Biology, Biotechnology, and Medicine (5th ed.), England. Wiley. 444-454. [Google Scholar] [Crossref]

69. Solomakos, A. Govaris, A. S. Angelidis, 2009) et al., "Occurrence, virulence genes and antibiotic resistance of Escherichia coliO157 isolated from raw bovine, caprine and ovine milk in Greece,". Food Microbiology. vol. 26, no. 8, pp. 865-871. [Google Scholar] [Crossref]

70. Tarr, P. I., Gordon, C. A., & Chandler, W. L. (2005). Shiga-toxin-producing Escherichia coli and hemolytic uremic syndrome. The Lancet, 365(9464), 1073–1086. https://doi.org/10.1016/S0140-6736(05)71144-2 [Google Scholar] [Crossref]

71. Tarr, P. I., Gordon, C. A., & Chandler, W. L. (2005). Shiga-toxin–producing Escherichia coli and haemolytic uraemic syndrome. The Lancet, 365(9464), 1073–1086. https://doi.org/10.1016/S0140-6736(05)71144-2 [Google Scholar] [Crossref]

72. The Johnson J, Kuskowski M, Menard M, Gajewski A, Xercavins M, and Garau J, (2006). similarity between human and chicken Escherichia coli isolates with ciprofloxacin resistance status. Journal of Infectious Diseases. 194 (1): 7178. [Google Scholar] [Crossref]

73. Todar, K. (2007). Pathogenic Escherichia coli. In Todar’s Online Textbook of Bacteriology. University of Wisconsin–Madison. https://www.textbookofbacteriology.net/e.coli.html [Google Scholar] [Crossref]

74. Todar, K. (2020). Antimicrobial resistance in bacteria. In Todar’s Online Textbook of Bacteriology. University of Wisconsin–Madison. https://www.textbookofbacteriology.net [Google Scholar] [Crossref]

75. Todar, K. (2020). Todar’s online textbook of bacteriology. University of Wisconsin–Madison. https://www.textbookofbacteriology.net [Google Scholar] [Crossref]

76. Tortora G, (2010). Microbiology: An Introduction. San Francisco, CA: Benjamin Cummings.85-87, 161, 165. (2016): 558. [Google Scholar] [Crossref]

77. Tortora, G. J., Funke, B. R., & Case, C. L. (2021). Microbiology: An introduction (14th ed.). Pearson Education. [Google Scholar] [Crossref]

78. Tortora, G. J., Funke, B. R., & Case, C. L. (2021). Microbiology: An introduction (14th ed.). Pearson Education. [Google Scholar] [Crossref]

79. Visioli, F., & Strata, A. (2014). Milk, dairy products, and their functional effects in humans: a narrative review of recent evidence. Advances in Nutrition, 5(2), 131-143. [Google Scholar] [Crossref]

80. Wang Q Ruan X, and Wei D (2010) "Development of a serogroup specific multiplex PCR assay to detect a set of Escherichia coli serogroups based on the identification of their O-antigen gene clusters," Molecular and Cellular Probes, vol. 24, no. 5, pp. 286-290. [Google Scholar] [Crossref]

81. Wariso BA, Ibe SN. Bacteriology of chronic discharging ears in Port Harcourt, Nigeria. West Afr J Med. 2006;25(3):219–222. [Google Scholar] [Crossref]

82. World Health Organization (WHO). (2023). E. coli (Escherichia coli). WHO Fact Sheets. https://www.who.int/news-room/fact-sheets/detail/e-coli [Google Scholar] [Crossref]

83. World Health Organization (WHO). (2023). E. coli (Escherichia coli). WHO Fact Sheets. https://www.who.int/news-room/fact-sheets/detail/e-coli [Google Scholar] [Crossref]

84. World Health Organization (WHO). (2023). E. coli (Escherichia coli). WHO Fact Sheets. https://www.who.int/news-room/fact-sheets/detail/e-coli [Google Scholar] [Crossref]

85. Wormser GP. Keusch GT and Heel RC. (1982). "Co-trimoxazole (trimethoprim-sulfamethoxazole):an updated review of its antibacterial activity and clinical efficacy". Drugs24 (6): 459-518. [Google Scholar] [Crossref]

86. Zhang, Y., Yew, W. W., & Barer, M. R. (2012). Targeting persisters for tuberculosis control. Antimicrobial Agents and Chemotherapy, 56(5), 2223–2230. https://doi.org/10.1128/AAC.06288-11 [Google Scholar] [Crossref]