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
Affiliations
- Samara University, College of Veterinary Medicine and Agriculture, P. O. Box 3015, Samara, Afar, Ethiopia.
- Addis Ababa University, College of Veterinary Medicine and Agriculture, P.O. Box 34, Bishoftu, Oromia, Ethiopia.
- 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
- Food Microbiol. 2015 Apr;46:222-226 - PubMed
- Clin Microbiol Rev. 2002 Jul;15(3):430-8 - PubMed
- Antimicrob Resist Infect Control. 2016 Jan 29;5:2 - PubMed
- APMIS. 2010 Jan;118(1):1-36 - PubMed
- J Clin Microbiol. 2011 Aug;49(8):2798-803 - PubMed
- Front Microbiol. 2016 Nov 22;7:1846 - PubMed
- Vet Microbiol. 2009 Feb 16;134(1-2):3-8 - PubMed
- N Engl J Med. 1987 Apr 9;316(15):927-31 - PubMed
- Res Vet Sci. 2016 Apr;105:192-4 - PubMed
- Biomed Res Int. 2015;2015:483548 - PubMed
- J Antimicrob Chemother. 2013 Feb;68(2):300-7 - PubMed
- J Infect Dis. 2010 Jul 15;202(2):270-81 - PubMed
- J Glob Infect Dis. 2010 Sep;2(3):275-83 - PubMed
- PLoS One. 2015 Dec 09;10(12):e0138385 - PubMed
- J Food Prot. 2014 Jun;77(6):993-8 - PubMed
- Ecohealth. 2012 Jun;9(2):139-49 - PubMed
- Microb Drug Resist. 2016 Mar;22(2):147-54 - PubMed
- J Med Microbiol. 2016 Dec;65(12):1405-1413 - PubMed
- Eur J Clin Microbiol Infect Dis. 1996 Apr;15(4):281-5 - PubMed
- Anim Nutr. 2018 Sep;4(3):250-255 - PubMed
- Vet Rec. 2008 Dec 20-27;163(25):740-3 - PubMed
- J Antimicrob Chemother. 2010 Mar;65(3):490-5 - PubMed
- Antimicrob Resist Infect Control. 2017 Aug 23;6:85 - PubMed
- Vet Microbiol. 2009 Feb 16;134(1-2):65-72 - PubMed
- J Clin Microbiol. 2009 Jan;47(1):217-9 - PubMed
- Korean J Food Sci Anim Resour. 2014;34(1):7-13 - PubMed
- J Appl Microbiol. 2012 Nov;113(5):1027-36 - PubMed
- J Lab Physicians. 2017 Jan-Mar;9(1):65-66 - PubMed
- Int J Food Microbiol. 2016 Dec 5;238:113-120 - PubMed
- Springerplus. 2014 Jun 24;3:310 - PubMed
- J Dairy Sci. 2014 Feb;97(2):829-37 - PubMed
- BMC Vet Res. 2011 Jan 27;7:6 - PubMed
- Int J Food Microbiol. 2008 Oct 31;127(3):246-51 - PubMed
- Int J Antimicrob Agents. 2018 Dec;52(6):930-935 - PubMed
- Food Microbiol. 2013 May;34(1):106-11 - PubMed
- Food Microbiol. 2014 Sep;42:56-60 - PubMed
- Int J Food Microbiol. 2010 Feb 28;137(2-3):221-9 - PubMed
- Microbiol Immunol. 2007;51(4):381-90 - PubMed
- Syst Appl Microbiol. 2006 Sep;29(6):480-6 - PubMed
- J Antimicrob Chemother. 1990 Oct;26(4):573-83 - PubMed
- J Clin Microbiol. 2005 Aug;43(8):3818-23 - PubMed
- Clin Microbiol Infect. 2003 Dec;9(12):1179-86 - PubMed
- J Med Microbiol. 2011 Nov;60(Pt 11):1661-1668 - PubMed
- Crit Care. 2004 Feb;8(1):R42-7 - PubMed
- Front Microbiol. 2016 Feb 29;7:222 - PubMed
- J Clin Microbiol. 1975 Jan;1(1):82-8 - PubMed
- Clin Infect Dis. 2014 May;58(9):1287-96 - PubMed
- Foodborne Pathog Dis. 2013 Sep;10(9):771-6 - PubMed
- BMC Pharmacol Toxicol. 2014 May 19;15:26 - PubMed
- Nat Commun. 2017 Nov 22;8(1):1689 - PubMed
- Appl Environ Microbiol. 1982 Oct;44(4):992-3 - PubMed
- BMC Public Health. 2017 Jan 5;17(1):14 - PubMed
- Ci Ji Yi Xue Za Zhi. 2016 Apr-Jun;28(2):49-53 - PubMed
- J Clin Invest. 2014 Jul;124(7):2836-40 - PubMed
- Bioessays. 2013 Jan;35(1):4-11 - PubMed
- J Dairy Sci. 2011 May;94(5):2329-40 - PubMed
- J Cataract Refract Surg. 2011 Oct;37(10):1908-9 - PubMed
- BMC Res Notes. 2015 Sep 28;8:482 - PubMed
- J Dairy Res. 2008 Nov;75(4):422-9 - PubMed
- Clin Microbiol Rev. 2014 Oct;27(4):870-926 - PubMed
- Meat Sci. 2013 Mar;93(3):387-96 - PubMed
- Ethiop J Health Sci. 2016 May;26(3):259-76 - PubMed
- Lancet. 2006 Sep 2;368(9538):874-85 - PubMed
- Vet J. 2008 Oct;178(1):119-25 - PubMed
- J Antimicrob Chemother. 2005 Apr;55(4):506-10 - PubMed
- J Clin Microbiol. 2010 Apr;48(4):1428-31 - PubMed
- Appl Environ Microbiol. 1987 Aug;53(8):1893-7 - PubMed
- Antimicrob Agents Chemother. 2009 Jan;53(1):146-9 - PubMed
- Foodborne Pathog Dis. 2018 Jul;15(7):449-458 - PubMed
- Front Microbiol. 2013 May 15;4:123 - PubMed
- Mem Inst Oswaldo Cruz. 2004 Dec;99(8):855-60 - PubMed
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