Display options
Share it on

Heliyon. 2020 Mar 31;6(3):e03606. doi: 10.1016/j.heliyon.2020.e03606. eCollection 2020 Mar.

Distribution and antimicrobial resistance profile of coagulase-negative staphylococci from cattle, equipment, and personnel on dairy farm and abattoir settings.

Heliyon

Fikru Gizaw, Tolera Kekeba, Fikadu Teshome, Matewos Kebede, Tekeste Abreham, Halefom Hayishe, Hika Waktole, Takele Beyene Tufa, Bedaso Mammo Edao, Dinka Ayana, Fufa Abunna, Ashenafi Feyisa Beyi, Reta Duguma Abdi

Affiliations

  1. Samara University, College of Veterinary Medicine and Agriculture, P. O. Box 3015, Samara, Afar, Ethiopia.
  2. Addis Ababa University, College of Veterinary Medicine and Agriculture, P.O. Box 34, Bishoftu, Oromia, Ethiopia.
  3. Department of Biomedical Sciences, College of Veterinary Medicine, Long Island University, Greenvale, New York, 11548, USA.

PMID: 32258466 PMCID: PMC7114745 DOI: 10.1016/j.heliyon.2020.e03606

Abstract

BACKGROUND: Safe food is central to social wellbeing. Coagulase-negative staphylococci (CNS) are a threat to food safety because they may harbor multiple enterotoxins and antimicrobial resistance (AMR) genes. CNS bacteria are an emerging nosocomial pathogen in public health. CNS also cause bovine mastitis with a significant economic loss in the dairy industry and may introduce toxins to the food supply chain resulting in foodborne illnesses. However, information on CNS and their AMR status are scarce in food animal production and processing lines in Ethiopia.

METHODOLOGY: This cross-sectional study evaluated the prevalence and AMR patterns of CNS in dairy farms and abattoirs using samples (n = 1001) from udder milk, beef carcass, personnel, and different abattoir and dairy equipment across five locations of central Oromia. The CNS isolates were identified via standard microbiological protocols and evaluated using disc diffusion test against 14 antimicrobials belonging to nine different broad classes. Uni-and-multivariable logistic regressions were used to analyze the association between potential risk factors (location, sample source, and sample type) and positivity to CNS.

RESULTS: The overall prevalence of CNS in the five different geographic locations studied was 9.6% (range: 6.7-12.4%) and varied between abattoirs (11.3%) and dairy farms (8.0%). CNS were prevalent on the carcass, milk, equipment, personnel hands, and nasal samples. Of all CNS isolates, 7.1, 10.7, 7.1, 12.5, 17.9, 10.7, 12.5, 7.1, 1.8, 5.4, 1.8, and 5.4% exhibited AMR simultaneously to single, double, 3, 4, 5, 6, 7, 7, 8, 9, 10, 11, and 13 antimicrobials, respectively. Overall, the isolates displayed 51 different AMR phenotypic patterns in which 50% of the isolates exhibited quadruple-resistance simultaneously based on the nine broad antimicrobial classes tested using 14 representative antimicrobials. The prevalence of multidrug-resistant (MDR) CNS (i.e. ≥ 3 classes of antimicrobials) was significantly (p = 0.037) different between locations with 100, 57.1, 50, 86.7, and 76.9% in Addis Ababa, Adama, Assela, Bishoftu, and Holeta, respectively. However, the prevalence of MDR CNS was not significantly (p = 0.20) different between dairy farms (87.5%) and abattoirs (71.9%). We evaluated the effect of acquiring cefoxitin-resistance of the isolates on the efficacy (i.e. inhibition zone) of the rest antimicrobials using General Linear Model after adjusting geographical locations as a random effect. Isolates with cefoxitin-resistance significantly displayed resistance to eight antimicrobials of 14 tested including amoxicillin, penicillin, cloxacillin, chloramphenicol, nalidixic acid, nitrofurantoin, and tetracycline (p = 0.000), and erythromycin (p = 0.02). On the other hand, cefoxitin-resistant isolates were susceptible to gentamicin, ciprofloxacin, kanamycin, streptomycin, and sulphamethoxazone trimethoprim (p = 0.000). Thus, antimicrobials such as gentamicin and ciprofloxacin may be an alternative therapy to treat cefoxitin-resistant CNS, as 96.4% of CNS isolates were susceptible to these antimicrobials. Overall, 94.1 and 54.5% of the CNS isolates among cefoxitin-resistant and cefoxitin-susceptible, respectively, harbored resistance to 3 or more classes of antimicrobials i.e. MDR.

CONCLUSION: The overall prevalence of CNS in milk, meat, equipment, and food handlers in central Oromia was 9.6% but varied by location and sample source. Some specific niches such as equipment, hands, and nasal cavities of personnel are significant sites for the source of CNS. Most, but not all, MDR CNS isolates were cefoxitin-resistant. Overall, 78.6% of the CNS tested were MDR and 50% had resistance to four or more broad classes of antimicrobials. CNS in food animals (raw milk and meat), equipment, and food handlers can be the source of MDR to the public. Personnel safety and hygienic food handling practices are needed. In addition, further investigation into the risk factors for the transmission and mechanisms of resistance of the CNS is required for intervention.

© 2020 Published by Elsevier Ltd.

Keywords: Antibiotic resistance; Antimicrobial resistance; Bacteria; CNS; Epidemiology; Food hygiene; Food safety; Livestock; Microbial ecology of foods; Microbiology; Multidrug resistance; Prevalence; Staphylococcus

References

  1. Food Microbiol. 2015 Apr;46:222-226 - PubMed
  2. Clin Microbiol Rev. 2002 Jul;15(3):430-8 - PubMed
  3. Antimicrob Resist Infect Control. 2016 Jan 29;5:2 - PubMed
  4. APMIS. 2010 Jan;118(1):1-36 - PubMed
  5. J Clin Microbiol. 2011 Aug;49(8):2798-803 - PubMed
  6. Front Microbiol. 2016 Nov 22;7:1846 - PubMed
  7. Vet Microbiol. 2009 Feb 16;134(1-2):3-8 - PubMed
  8. N Engl J Med. 1987 Apr 9;316(15):927-31 - PubMed
  9. Res Vet Sci. 2016 Apr;105:192-4 - PubMed
  10. Biomed Res Int. 2015;2015:483548 - PubMed
  11. J Antimicrob Chemother. 2013 Feb;68(2):300-7 - PubMed
  12. J Infect Dis. 2010 Jul 15;202(2):270-81 - PubMed
  13. J Glob Infect Dis. 2010 Sep;2(3):275-83 - PubMed
  14. PLoS One. 2015 Dec 09;10(12):e0138385 - PubMed
  15. J Food Prot. 2014 Jun;77(6):993-8 - PubMed
  16. Ecohealth. 2012 Jun;9(2):139-49 - PubMed
  17. Microb Drug Resist. 2016 Mar;22(2):147-54 - PubMed
  18. J Med Microbiol. 2016 Dec;65(12):1405-1413 - PubMed
  19. Eur J Clin Microbiol Infect Dis. 1996 Apr;15(4):281-5 - PubMed
  20. Anim Nutr. 2018 Sep;4(3):250-255 - PubMed
  21. Vet Rec. 2008 Dec 20-27;163(25):740-3 - PubMed
  22. J Antimicrob Chemother. 2010 Mar;65(3):490-5 - PubMed
  23. Antimicrob Resist Infect Control. 2017 Aug 23;6:85 - PubMed
  24. Vet Microbiol. 2009 Feb 16;134(1-2):65-72 - PubMed
  25. J Clin Microbiol. 2009 Jan;47(1):217-9 - PubMed
  26. Korean J Food Sci Anim Resour. 2014;34(1):7-13 - PubMed
  27. J Appl Microbiol. 2012 Nov;113(5):1027-36 - PubMed
  28. J Lab Physicians. 2017 Jan-Mar;9(1):65-66 - PubMed
  29. Int J Food Microbiol. 2016 Dec 5;238:113-120 - PubMed
  30. Springerplus. 2014 Jun 24;3:310 - PubMed
  31. J Dairy Sci. 2014 Feb;97(2):829-37 - PubMed
  32. BMC Vet Res. 2011 Jan 27;7:6 - PubMed
  33. Int J Food Microbiol. 2008 Oct 31;127(3):246-51 - PubMed
  34. Int J Antimicrob Agents. 2018 Dec;52(6):930-935 - PubMed
  35. Food Microbiol. 2013 May;34(1):106-11 - PubMed
  36. Food Microbiol. 2014 Sep;42:56-60 - PubMed
  37. Int J Food Microbiol. 2010 Feb 28;137(2-3):221-9 - PubMed
  38. Microbiol Immunol. 2007;51(4):381-90 - PubMed
  39. Syst Appl Microbiol. 2006 Sep;29(6):480-6 - PubMed
  40. J Antimicrob Chemother. 1990 Oct;26(4):573-83 - PubMed
  41. J Clin Microbiol. 2005 Aug;43(8):3818-23 - PubMed
  42. Clin Microbiol Infect. 2003 Dec;9(12):1179-86 - PubMed
  43. J Med Microbiol. 2011 Nov;60(Pt 11):1661-1668 - PubMed
  44. Crit Care. 2004 Feb;8(1):R42-7 - PubMed
  45. Front Microbiol. 2016 Feb 29;7:222 - PubMed
  46. J Clin Microbiol. 1975 Jan;1(1):82-8 - PubMed
  47. Clin Infect Dis. 2014 May;58(9):1287-96 - PubMed
  48. Foodborne Pathog Dis. 2013 Sep;10(9):771-6 - PubMed
  49. BMC Pharmacol Toxicol. 2014 May 19;15:26 - PubMed
  50. Nat Commun. 2017 Nov 22;8(1):1689 - PubMed
  51. Appl Environ Microbiol. 1982 Oct;44(4):992-3 - PubMed
  52. BMC Public Health. 2017 Jan 5;17(1):14 - PubMed
  53. Ci Ji Yi Xue Za Zhi. 2016 Apr-Jun;28(2):49-53 - PubMed
  54. J Clin Invest. 2014 Jul;124(7):2836-40 - PubMed
  55. Bioessays. 2013 Jan;35(1):4-11 - PubMed
  56. J Dairy Sci. 2011 May;94(5):2329-40 - PubMed
  57. J Cataract Refract Surg. 2011 Oct;37(10):1908-9 - PubMed
  58. BMC Res Notes. 2015 Sep 28;8:482 - PubMed
  59. J Dairy Res. 2008 Nov;75(4):422-9 - PubMed
  60. Clin Microbiol Rev. 2014 Oct;27(4):870-926 - PubMed
  61. Meat Sci. 2013 Mar;93(3):387-96 - PubMed
  62. Ethiop J Health Sci. 2016 May;26(3):259-76 - PubMed
  63. Lancet. 2006 Sep 2;368(9538):874-85 - PubMed
  64. Vet J. 2008 Oct;178(1):119-25 - PubMed
  65. J Antimicrob Chemother. 2005 Apr;55(4):506-10 - PubMed
  66. J Clin Microbiol. 2010 Apr;48(4):1428-31 - PubMed
  67. Appl Environ Microbiol. 1987 Aug;53(8):1893-7 - PubMed
  68. Antimicrob Agents Chemother. 2009 Jan;53(1):146-9 - PubMed
  69. Foodborne Pathog Dis. 2018 Jul;15(7):449-458 - PubMed
  70. Front Microbiol. 2013 May 15;4:123 - PubMed
  71. Mem Inst Oswaldo Cruz. 2004 Dec;99(8):855-60 - PubMed

Publication Types