Tropical Animal Health and Production

, Volume 50, Issue 6, pp 1327–1341 | Cite as

Virulent gene profile and antibiotic susceptibility pattern of Shiga toxin-producing Escherichia coli (STEC) from cattle and camels in Maiduguri, North-Eastern Nigeria

  • Musa Sakuma Adamu
  • Iniobong Chukwuebuka Ikenna UgochukwuEmail author
  • Sunday Idoko Idoko
  • Yakubu Adamu Kwabugge
  • Nafisatu Sa’ad Abubakar
  • James Ameh Ameh
Regular Articles


Prevalence and distribution of Shiga toxin-producing Escherichia coli (STEC) serogroups from the faecal samples of cattle and camels slaughter in Maiduguri abattoir and their antibiotic resistance profile of the isolates were determined. The highest prevalence (24%) was recorded in the month of September and more STEC isolates came from cattle than the camels. There was significant (P < 0.05) seasonal trend in the prevalence of STEC among cattle and camel with more cases recorded during the wet season. Although, the study did not demonstrate significant influence of sex from the various sources. The serogroups recorded in this study were O157, O26, O91, O103 and O111. There was no significant difference (P < 0.05) between the detection rates of serogroups. The serogroup O26 was significantly (P < 0.05) the most observed serogroup in both camels and cattle. None of the STEC isolates tested positive for the O45 serogroup. PCR assays shows that 50 (63.3%) of the 86 STEC isolates carried the stx2 gene, 34 (43%) possessed the stx1 gene, and 14 (16.3%) carried both stx1 and stx2 genes. Other genes detected include eae and ehlyA. The antimicrobial resistance among the STEC O157 and non-O157 isolates from cattle and camels in Maiduguri abattoir were very high and the STEC isolates were resistant to at least one or more of the antimicrobial agents tested. There was also multidrug resistance with the most frequent occurring patterns been ampicillin/nalidixic acid and tetracycline/trimethoprim. However, all the 79 isolates were sensitive to chloramphenicol, ceftazidime and ceftriaxone; therefore, these drugs could be drugs of choice in the treatment of STEC infections.


Shiga toxin-producing Escherichia coli Virulent gene Antibiotic resistance Cattle Camels 



The authors are grateful for the technical help rendered by the staff of Department of Veterinary Microbiology and Parasitology, University of Maiduguri, Maiduguri, Borno State.

Author contributions

J.A Ameh conceived the idea, M.S. Adamu and Y.A. Kwabugge carried out the research, C.I.I. Ugochukwu wrote the manuscript while S.I. Idoko, C.I.I. Ugochukwu and N.S. Abubakar did the statistical analysis. All authors read and approved the manuscript for submission.

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflict of interest.

Ethical considerations

The ethics governing the use and conduct of experiments on animals were strictly observed, and the experimental protocol was approved by the University of Maiduguri Senate committee on Medical Research ethics. Proper permit and consent were obtained from the Maiduguri abattoir management, before the faecal samples of the cattle and camels slaughtered in this abattoir were used for this experiment.


  1. Adamu, M.S., Ugochukwu, I.C.I., Idoko, S.I., Kwabugge, Y.A., Abubakar, N.S. and Ameh, J.A., 2017. Virulent gene profile and antimicrobial susceptibility pattern of Shiga toxin-producing Escherichia coli (STEC) from humans in Maiduguri, Borno State, North-Eastern Nigeria. Comparative Clinical Pathology. doi:
  2. Aibinu, I.E., Peters, R.F., Amisu, K.O. and Adesida S.A., 2007. Multidrug Resistance in E. coli O157 Strains and Public Health Implication Journal of Animal Science, 3(3), 22–33.Google Scholar
  3. Akter, M.M., Majumder, S., Nazir, K. H. M. N. H. N. and M. Rahman, M. 2016. Prevalence and molecular detection of shiga toxin producing Escherichia coli from diarrheic cattle. Journal of Bangladesh Agricultural University, 14(1), 63–68.CrossRefGoogle Scholar
  4. Amézquita-López, B. A., Quiñones, B., Lee, B. G. and Chaidez, C., 2014. Virulence profiling of Shiga toxin-producing Escherichia coli recovered from domestic farm animals in North-western Mexico, Frontiers in Cellular and Infection Microbiology, 4, 7.doi: Scholar
  5. Askari, M., Zahraei Salehi, T., Rabbani Khorasgani, M., Tadjbakhsh, H., Nikbakht Brujeni, G. and Nadalian, M. G., 2010. Virulence gene profiles and intimin subtypes of Shiga toxin-producing Escherichia coli isolated from healthy and diarrhoeic calves, Veterinary Record, 167, 858–861.CrossRefGoogle Scholar
  6. Beco, L., Guaguère, E., Méndez, C.L., Noli, C., Nuttall, T. and Vroom, M. 2013. Suggested guidelines for using systemic antimicrobials in bacterial skin infections: part 2— antimicrobial choice, treatment regimens and compliance. Veterinary Record, 172, 156–160.CrossRefPubMedGoogle Scholar
  7. Beutin, L., Geier, D., Zimmermann, S., Aleksic, S., Gillespie, H.A., Whittam,T.S., 1997. Epidemiological relatedness and clonal types of natural populations of Escherichia coli strains producing Shiga toxins in separate populations of cattle and sheep, Applied Environmental Microbiology 63, 2175–2180.Google Scholar
  8. Beutin, L., Miko, A., Krause, G., Pries, K., Haby, S., Steege, K., and Albrecht, N., 2007. Identification of human-pathogenic strains of Shiga toxin-producing Escherichia coli from food by a combination of serotyping and molecular typing of shiga toxin genes, Applied Environmental Microbiology, 73, 4769–4775.CrossRefPubMedGoogle Scholar
  9. Blanco, M., Blanco, J.E., Blanco, J., Mora, A., Prado, C., Alonso, M.P., Mourino, M., Madrid, C., Balsalobre, C. and Juarez, A., 1997. “Distribution and characterization of faecal verotoxin producing Escherichia coli (VTEC) isolated from healthy cattle”, Veterinary Microbiology, 54, 309–319.CrossRefPubMedGoogle Scholar
  10. Blanco, J., Blanco, M., Blanco, J.E., Mora, A., González, E.A., Bernárdez, M.I., Alonso, M.P., Coira, A., Rodriguez, A., Rey, J., Alonso, J.M. and Usera, M.A., 2003. Verotoxin-Producing Escherichia coli in Spain: Prevalence, serotypes, and virulence genes of O157:H7 and Non-O157 VTEC in ruminants, raw beef products, and humans, Experimental Biology and Medicine (Maywood), 228(4), 345–351.CrossRefGoogle Scholar
  11. Bonanno, L., Loukiadis, E., Mariani-Kurkdjian, P., Oswald, E., Garnier, L., Michel, V. and Auvray, F., 2015. Diversity of Shiga toxin-producing Escherichia coli (STEC) O26:H11 strains examined via stx subtypes and insertion sites of Stx and EspK bacteriophages, Applied Environmental Microbiology, 81, 3712–3721.CrossRefPubMedGoogle Scholar
  12. Bosilevac, J.M., Mustafa, A., Gassem, M.A., Al Sheddy, I.A., Almaiman, S.A., Al-Mohizea, I.S., 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 (1), 89–96.CrossRefPubMedGoogle Scholar
  13. Burnens, A.P., Frey, A., Lior, H. and Nicolet, J., 1995. Prevalence and clinical significance of vero-cytotoxin-producing Escherichia coli (VTEC) isolated from cattle in herds with and without calf diarrhoea, Journal of Veterinary Medicine B, 42, 311–318.CrossRefPubMedGoogle Scholar
  14. Caprioli, A., Morabito, S., Brugere, H. and Oswald, E., 2005. Enterohaemorrhagic Escherichia coli: emerging issues on virulence and modes of transmission. Veterinary Research, 36, 289–311.CrossRefPubMedGoogle Scholar
  15. CDC, 2018. Escherichia coli. CDC National Center for Emerging and Zoonotic Infectious Diseases. Accessed on 20 February 2018
  16. Cheesbrough, M., 2000. District laboratory practice in tropical countries (Part 2), Low Price Ed, (Cambridge University Press, UK).Google Scholar
  17. China, B., Pirson, V., Maini, J., 1998. Prevalence and molecular typing of attaching and effacing Escherichia coli among calf population in Belgium, Veterinary Microbiology, 63, 249–259.CrossRefPubMedGoogle Scholar
  18. Clinical Laboratory Standard Institute (CLSI)., 2006. Performance standards of antimicrobial disc and dilution susceptibility tests for bacteria isolated from animal, approved standard. 3rd edition. 28, 8.Google Scholar
  19. Daini, O.A., Adesemowo, A., 2008. Antimicrobial Susceptibility Patterns and R-Plasmids of Clinical strains of Escherichia coli, Australian Journal of Basic and Applied Sciences, 2, 397–400.Google Scholar
  20. Das, S. C., Khan, A., Panja, P., Datta, S., Sikdar, A., Yamasaki, S., Takeda, Y., Bhattacharya, S. K., Ramamurthy, T. and Nair, G. B., 2005. Dairy farm investigation on Shiga toxin-producing Escherichia coli (STEC) in Kolkata, India with emphasis on molecular characterization. Epidemiology and Infection, 133(4), 617–626.CrossRefPubMedPubMedCentralGoogle Scholar
  21. Dastmalchi, S.H., Ayremlou, N., 2012. Characterization of Shiga toxin-producing Escherichia coli (STEC) in faeces of healthy and diarrheic calves in Urmia region, Iran. Iran Journal of Microbiology, 4 (2), 63–69Google Scholar
  22. EFSA. The community summary report on food-borne outbreaks in the European Union in 2007. The EFSA Journal, 2009. Accessed 11 Nov 2015.
  23. Elder, R. O., Keen, J. E., Siragusa, G. R., Barkocy-Gallagher, G. A., Koohmaraie, M. and Laegreid, W. W. (2000). Correlation of enterohemorrhagic Escherichia coli O157 prevalence in faeces, hides, and carcasses of beef cattle during processing. Proceedings of the National Academy of Sciences of the United States of America, 97(7), 2999–3003.CrossRefPubMedPubMedCentralGoogle Scholar
  24. 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.CrossRefPubMedGoogle Scholar
  25. FAO 1990. Conducting small scale nutrition survey: a field manual. Nutrition in Agriculture Series No 5: FAO Rome, Food and Agriculture Organization of the United Nations Rome, Italy.Google Scholar
  26. Frank, C., Kapfhammer, S., Werber, D., 2008. Cattle density and Shiga toxin-producing Escherichia coli infection in Germany: increased risk for most but not all serogroup, Vector Borne Zoonotic Diseases, 8(5), 635–643.CrossRefPubMedGoogle Scholar
  27. Geue, L., Segura-Alvarez, M., Conraths, F.J., Kuczius, T., Bockemuhl, J., Karch, H., Gallien, P., 2002. A long-term study on the prevalence of shiga toxin-producing Escherichia coli (STEC) on four German cattle farms, Epidemiology and Infection, 129, 173–185.CrossRefPubMedPubMedCentralGoogle Scholar
  28. Gyles, C. L., 2007. Shiga toxin-producing Escherichia coli: an overview, Journal of Animal Science, 85, E45–E62.CrossRefPubMedGoogle Scholar
  29. Gyles, C.L. and Fairbrother, J.M., 2004. Escherichia coli. In: Gyles, C.L., Prescott, J.F., Songer, J.G. and C. O. Thoen (eds), Pathogenesis of Bacterial Infections in Animals, 3rd edn, Blackwell publishing, New Jersey, USA, pp 193–223.Google Scholar
  30. Hassan, J., Parvej, M.S., Rahman, M.B., Khan, M.S.R., Rahman, M.T., Kamal, T. and Nazir, K.H.M.N.H., 2014. Prevalence and characterization of Escherichia coli from rectal swab of apparently healthy cattle in Mymensingh, Bangladesh. Microbes Health, 3, 12–14.CrossRefGoogle Scholar
  31. Hussein, H.S., 2007. Prevalence and pathogenicity of Shiga toxin-producing Escherichia coli in beef cattle and their products, Journal of Animal Science, 85, E63-E72.CrossRefPubMedGoogle Scholar
  32. Islam, M. A., Heuvelink, A.E., Talukder, K.A., Zwietering, M.H. and de Boer E., 2006a. Evaluation of immunomagnetic separation and PCR for the detection of Escherichia coli O157 in animal faeces and meats, Journal of Food Protection, 66:2865–2869.CrossRefGoogle Scholar
  33. Islam, M. A., Heuvelink, A.E., Talukder, K.A. and de Boer E., 2006b. Immunoconcentration of Shiga toxin-producing Escherichia coli O157 from animal faeces and raw meats by using Dynabeads anti-E. coli O157 and the VIDAS system, International Journal of Food Microbiology, 109, 151–156.CrossRefGoogle Scholar
  34. Islam M. A., Mondol, A.S., de Boer, E., Beumer, R.R., Zwietering, M.H., Talukder, K.A and Heuvelink, A.E., 2008. Prevalence and genetic characteristics of Shiga toxin-producing E. coli isolates from slaughtered animal in Bangladesh. Journal of Applied and Environmental Microbiology, 74(17), 5414–5421.CrossRefPubMedGoogle Scholar
  35. Islam, K., Ahad, A., Barua, M., Islam, A., Chakma, S., Dorji, C., Uddin, M.A., Islam, S. and Ahasan, A.S.M.L. 2016. Isolation and epidemiology of multidrug resistant Escherichia coli from goats in Cox’s Bazar, Bangladesh. Journal of Advanced Veterinary and Animal Research, 3, 166–172.CrossRefGoogle Scholar
  36. Kabir, J., Umoh, U.J. and Umoh, V.J., 2002, A survey of veterinary drug use among animal health workers and livestock owners and its implication in the occurrence and control of drug residues. Sahel Journal Veterinary Science, 1, 40–47.Google Scholar
  37. Karmali M. A., Gannon, V. and Sargeant, J. M., 2010. Verocytotoxin- producing Escherichia coli (VTEC), Veterinary Microbiology, 140, 360–370.CrossRefPubMedGoogle Scholar
  38. Krüger, A., Lucchesi, P.M.A. and Parma, A.E., 2011. “Verotoxins in bovine and meat verotoxin-producing Escherichia coli isolates: type, number of variants, and relationship to cytotoxicity”, Applied and Environmental Microbiology, 77(1), 73–79.CrossRefPubMedGoogle Scholar
  39. Kudva, I.T., Hatfield, P.G. and Hovde, C.J. 1997. Characterization of Escherichia coli O157:H7 and other Shiga toxin- producing E. coli serotypes isolated from sheep. Journal of Clinical Microbiology, 35, 892–899.PubMedPubMedCentralGoogle Scholar
  40. Kumarasamy, K.K., Toleman, M.A., Walsh, T.R., Bagaria, J., Butt, F., Balakrishnan, R., Chaudhary, U., Doumith, M., Giske, C.K., Irfan, S., Krishnan, P., Kumar, A.V., Maharjan, S., Mushtaq, S., Noorie, T., Paterson, D.L., Pearson, A., Perry, C., Pike, R., Rao, B., Ray, U., Sarma, J.B., Sharma, M., Sheridan, M., Thirunarayan, M.A., Turton, J., Upadhyay, S.,Warner, M., Welfare, W., Livermore, D.M. and Woodford, N., 2010. Emergence of a new antibiotic resistance mechanism in India, Pakistan, and the UK: a molecular, biological, and epidemiological study, Lancet Infectious Disease, 10(9), 597–602.CrossRefGoogle Scholar
  41. Leomil, L., Aidar-Ugrinovich, L., Guth, B.E.C., Irino, K., Vettorato, M.P., Onuma, D.L. and De Castro, A.F.P., 2003. “Frequency of Shiga toxin-producing Escherichia coli (STEC) isolates among diarrheic and non-diarrheic calves in Brazil”, Veterinary Microbiology, 97, 103–109.CrossRefPubMedGoogle Scholar
  42. Llorente, P., Barnech, L., Irino, K., Rumi, M.V. and Bentancor, A., 2014. Characterization of Shiga Toxin-Producing Escherichia coli isolated from ground beef collected in different socioeconomic strata markets in Buenos Aires. BioMed Research International.
  43. Luga, I., Akodu, I., Mhomga, LI., Allam, L., Ajogi, I., Umoh, V.J. and Kwaga, J.K.P., 2007. Antimicrobial Resistance of Shiga toxin Producing Escherichia coli 0157: NM Isolates from Water Fed to Cattle in North-western Nigeria, Asian Journal of Animal and Veterinary Advances, 2, 205–211.CrossRefGoogle Scholar
  44. Melton-Celsa, A. R., 2014. Shiga Toxin (Stx) Classification, Structure, and Function. Microbiology Spectrum, 2(2).
  45. Moore, J. E., McCalmont, M., Xu, J.R., Nation, G., Tinson, A.H. and Cartothers, L., 2002. Prevalence of faecal pathogens in calves of racing camels (Camelus dromedarius) in the United Arab Emirates, Tropical Animal Health and Production, 34(4), 283–287.CrossRefPubMedGoogle Scholar
  46. Moses, A.E., Egwu, G.O. and Ameh, J.A., 2012. Antimicrobial resistant pattern of E. coli O157 Isolated from human, cattle and surface water samples in northeast Nigeria, Journal of Veterinary Advances, 2(5), 209–215.Google Scholar
  47. Ogden, I. D., MacRae, M. and Strachan, N.J.C., 2004. Is prevalence and shedding of E. coli O157 in beef cattle in Scotland seasonal? FEMS Microbiology Letters, 233, 297–300.CrossRefPubMedGoogle Scholar
  48. Ojo, O. E., Oyekunle, M.A., Ogunleye, A.O. and Otesile, E.B., 2009. E. coli 0157:H7 in food animals in part of S/Western Nigeria: Prevalence and in vitro antimicrobial susceptibility, Tropical Veterinarian, 26, 23–30.Google Scholar
  49. Ojo, O.E., Ajuwape, A.T.P., Otesile, E.B., Owoade, A.A., Oyekunle, M.A. and Adetosoye A.I. 2010, Potentially zoonotic shiga toxin-producing Escherichia coli serogroups in the faeces and meat of food-producing animals in Ibadan, Nigeria, International Journal of Food Microbiology, 142 (1–2), 214–221.CrossRefPubMedGoogle Scholar
  50. Okeke, I.N., Lamikanra, A. and Edelman, R., 1999, Socioeconomic and behavioural factors leading to acquired bacterial resistance to antibiotics in developing countries, Emerging Infectious Diseases, 5(1), 18–27.CrossRefPubMedPubMedCentralGoogle Scholar
  51. Olatoye, I. O., 2010. The incidence and antibiotics susceptibility of Escherichia coli O157:H7 from beef in Ibadan Municipal, Nigeria, African Journal of Biotechnology, 9, 1196–1199.CrossRefGoogle Scholar
  52. Orden, J.A., Ruiz-Santa-Quiteria, J.A., Cid, D., García, S., Sanz, R. and de la Fuente R.,1998. Verotoxin producing Escherichia coli (VTEC) and eae-positive non-VTEC in 1-30-days-old diarrhoeic dairy calves. Veterinary Microbiology, 63(2–4), 239–248.CrossRefPubMedGoogle Scholar
  53. Parry, S.M., Salmon, R.L., Willshaw, G.A., Cheasty, T., 1998. Risk factors for and prevention of sporadic infections with vero cytotoxin (shiga toxin) producing Escherichia coli O157, Lancet, 351, 1019–1022.CrossRefPubMedGoogle Scholar
  54. Paton J.C. and Paton, A.W., 1998. Pathogenesis and diagnosis of shiga toxin producing E.coli infections. Clinical Microbiology Review, 11, 450–479.Google Scholar
  55. Persson, S., Olsen, K.E., Scheutz, F., Krogfelt, K.A., Gerner-Smidt, P., 2007. A method for fast and simple detection of major diarrhoeagenic Escherichia coli in the routine diagnostic laboratory. Clinical Microbiology and Infection, 13(5), 516–524.CrossRefPubMedGoogle Scholar
  56. Pierard, D., D. Stevens, L. Moriau, H. Lior, and S. Lawers (1997). Isolation and virulence factors of verocytotoxin-producing Escherichia coli in human stool samples. Clinical Microbiology and Infection, 3, 531–540.CrossRefPubMedGoogle Scholar
  57. Rahimi, E., Momtaz, H. and Nozarpour, N., 2010. Prevalence of Listeria spp., Campylobacter spp., and Escherichia coli O157:H7 isolated from camel carcasses during processing. Bulgaria Journal Veterinary Medicine, 13, 179–185.Google Scholar
  58. Reller, L.B., Weinstein, M., Jorgensen J.H., Ferraro M.J., 2009. Antimicrobial Susceptibility Testing: A Review of General Principles and Contemporary Practices Clinical Infectious Diseases, 49(11), 1749–1755.CrossRefGoogle Scholar
  59. Rhoades, J.R., Duffy, G. and Koutsoumanis, K. 2009. Prevalence and concentration of verocytotoxigenic Escherichia coli, Salmonella enterica and Listeria monocytogenes in the beef production chain: a review, Food Microbiology, 26(4), 357–76CrossRefPubMedGoogle Scholar
  60. Rigobelo, E.C. and de Ávila, F.A., 2012. Shiga toxin - Producing Escherichia coli from beef carcass. Journal of Microbiology Research, 2, 103–107.CrossRefGoogle Scholar
  61. Rigobelo, E.C., Gamez, H.J., Marin, J.M., Macedo, C., Ambrosin, J.A.and Ávila, F.A., 2006. Virulence factors of Escherichia coli isolated from diarrheic calves. Arquivo Brasileiro de Medicina Veterinária e Zootecnia, 58(3), 305–310,CrossRefGoogle Scholar
  62. Sa’Ayinzat, F. E., Shaibu, S. J. and Tekdek, L.B., 2015. The Earliest Occurrence of Escherichia coli in Calves in Zaria, Nigeria, International Journal Current Microbiology and Applied Sciences, 4(6), 218–223.Google Scholar
  63. Savoye, F., Feng, P., Rozand, C., Bouvier, M., Gleizal, A., Thevenot, D., 2011. Comparative evaluation of a phage protein ligand assay with realtime PCR and a reference method for the detection of Escherichia coli O157:H7in raw ground beef and trimmings. Journal of Food Protection, 74(1), 6–12.CrossRefPubMedGoogle Scholar
  64. Sayah, R.S., Kaneene, JB., Johnson, Y. and Miller, R., 2005. Patterns of Antimicrobial Resistance Observed in Escherichia coli Isolates Obtained from Domestic- and Wild-Animal Fecal Samples, Human Septage, and Surface Water, Applied Environmental Microbiology, 71(3), 1394–1404CrossRefPubMedGoogle Scholar
  65. Scheutz, F., Cheasty, T. and Woodward, D., 2004. Designation of O174 and O175 to temporary O groups OX3 and OX7, and six new E. coli O groups that include Verocytotoxin producing E. coli(VTEC): O176, O177, O178, O179, O180 and O181, APMIS, 112(9), 569–584.CrossRefPubMedGoogle Scholar
  66. Scheutz, F., Teel, L.D., Beutin, L., Pierard, D., Buvens, G., Karch, H., Mellmann, A., Caprioli, A., Tozzoli, R., Morabito, S., 2012. Multicenter evaluation of a sequence-based protocol for subtyping Shiga toxins and standardizing Stx nomenclature, Journal of Clinical Microbiology, 50, 2951–2963.CrossRefPubMedPubMedCentralGoogle Scholar
  67. Schmidt, H., Geitz, C., Tarr, P.I., Frosch, M. and Karch, H., 1999. Non- O157:H7 pathogenic Shiga toxin-producing Escherichia coli: phenotypic and genetic profiling of virulence traits and evidence for clonality, Journal of Infectious Diseases, 179, 115–123.CrossRefPubMedGoogle Scholar
  68. Serna, A.T. and Boedeker, E.C., 2008. Pathogenesis and treatment of Shiga toxin-producing Escherichia coli infections, Current Opinion in Gastroenterology, 2008, 24, 38–47.CrossRefGoogle Scholar
  69. Shahrani, M., Dehkordi F.S., Momtaz, H., 2014. Characterization of Escherichia coli virulence genes, pathotypes and antibiotic resistance properties in diarrheic calves in Iran, Biological Research, 47(28), 1–13.Google Scholar
  70. Shittu, O.B., Nwagboniwe, C.A.K., George, O.O., 2007. Antibiotic Resistance patterns of Escherichia Coli isolates from human, pet, livestock and poultry living in close contact. ASSET Series B, 6 (2), 164–170.Google Scholar
  71. Synge, B.A. and Hopkins, G.F., 1994. Studies of Verotoxigenic Escherichia coli O157 in cattle in Scotland and association with human cases, Elsevier Science (Armstadam), 65–68.Google Scholar
  72. Wells, J. G., Chipman, L.D., Greene, K.D., Sowers, E.G., Green, J.H., Cameron, D.N., Downes, F.P., Martin, M.L., Griffin, P.M., Ostroff, S.M., Potter, M.E., Tauxe, R.V. and Wachsmuth, J.K., 1991. Isolation of Escherichia coli serotype O157:H7 and other Shiga like toxin-producing E. coli from dairy cattle, Journal of Clinical Microbiology, 29, 985–989.PubMedPubMedCentralGoogle Scholar
  73. WHO. World Health Organization. Zoonotic non-O157 Shiga toxin-producing Escherichia coli (STEC). Report of WHO Scientific Working Group Meeting, 1998, World Health Organization (Geneva, Switzerland).Google Scholar
  74. York, M.K., Rodrigues-Wong, P. and Church, D.L., 2010. Faecal culture for aerobic pathogens of gastroenteritis, In: Garcia, L.S. (ed), Clinical Microbiology procedures handbook, 3rd ed, ASM Press, (Washington, DC), 3811–3851.Google Scholar
  75. Zahraei, S.T., Mahzounieh, M., Asadian, F., Khosravi, M., 2006. Virulence genes in Escherichia coli isolates from calves in Shahrekord area, Iran; 16th European Congress of Clinical Microbiology and Infectious Disease (Nice, France).Google Scholar
  76. Zhang, X.Y., Ding, L.J., Fan, M.Z., 2009. Resistance patterns and detection of aac (3)-IV gene in apramycin-resistant Escherichia coli isolated from farm animals and farm workers in Northeastern China, Research in Veterinary Science, 87, 449–454.CrossRefPubMedGoogle Scholar

Copyright information

© Springer Science+Business Media B.V., part of Springer Nature 2018

Authors and Affiliations

  • Musa Sakuma Adamu
    • 1
  • Iniobong Chukwuebuka Ikenna Ugochukwu
    • 2
    Email author
  • Sunday Idoko Idoko
    • 3
  • Yakubu Adamu Kwabugge
    • 4
  • Nafisatu Sa’ad Abubakar
    • 1
  • James Ameh Ameh
    • 5
  1. 1.Department of Animal Health and Production TechnologyFederal PolytechnicMubiNigeria
  2. 2.Department of Veterinary Pathology and MicrobiologyUniversity of NigeriaNsukkaNigeria
  3. 3.Department of Veterinary PathologyUniversity of AbujaAbujaNigeria
  4. 4.Department of Animal Health TechnologyAdamawa College of AgricultureGanyeNigeria
  5. 5.Department of Veterinary MicrobiologyUniversity of AbujaAbujaNigeria

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