Prevalence and risk factors for multi-drug resistant Escherichia coli among poultry workers in the Federal Capital Territory, Abuja, Nigeria

English version

Autoři: Mabel Kamweli Aworh ^aff001; Jacob Kwaga ^aff003; Emmanuel Okolocha ^aff003; Nwando Mba ^aff004; Siddhartha Thakur ^aff005
Působiště autorů: Department of Veterinary and Pest Control Services, Federal Ministry of Agriculture and Rural Development, Abuja, Nigeria ^aff001; Nigeria Field Epidemiology and Laboratory Training Programme, Abuja, Nigeria ^aff002; Department of Veterinary Public Health and Preventive Medicine, Ahmadu Bello University, Zaria, Nigeria ^aff003; National Reference Laboratory, Nigeria Center for Disease Control, Abuja, Nigeria ^aff004; Department of Population Health and Pathobiology, College of Veterinary Medicine, North Carolina State University, Raleigh, North Carolina, United States of America ^aff005
Vyšlo v časopise: PLoS ONE 14(11)
Kategorie: Research Article
prolekare.web.journal.doi_sk: https://doi.org/10.1371/journal.pone.0225379

Souhrn

Background

Antimicrobial resistance has emerged as a global health threat. Antimicrobial resistant Escherichia coli infections are associated with high morbidity and expenditure when compared with infections caused by susceptible strains. In Nigeria, antimicrobial drugs are readily available over-the-counter with potential for indiscriminate use by poultry farmers and eventual development of drug resistance. The objective of this study was to investigate prevalence and risk factors for multi-drug resistant E. coli among poultry workers (PW) in Abuja, Nigeria.

Materials and methods

A cross-sectional study was conducted among 122 randomly selected apparently healthy poultry workers (poultry-farmers/ sellers) in Municipal and Kuje Area Councils from December 2018 to April 2019. Data was collected on socio-demographics and exposure factors using a structured interviewer-administered questionnaire. E. coli was isolated and identified from stool samples of poultry workers. Antibiotic susceptibility testing was done using Kirby-Bauer disk diffusion method. Multidrug resistance (MDR) was defined as resistance to three or more classes of antimicrobials. Data was analyzed by computing proportions, prevalence odds-ratios (POR) and logistic regression at 5% significance level.

Results

Among PW, there were 121 males (99.2%). Mean age of the male workers was 30.6 ± 9.7years, 54.6% (n = 66) married, 57.9% (n = 70) had secondary education and 62.0% (n = 75) were farm-workers. Prevalence of E. coli was 39.7% (n = 48), highest among farm-workers (POR = 2.7, 95% Confidence Interval [CI] = 1.3–5.7; p = 0.01) compared to poultry-sellers. Of the 48 E. coli isolates, 16.7% (n = 8) were extended spectrum beta lactamase (ESBL) producers and 79.2% (n = 38) were MDR. We detected resistance against Tetracycline: (83.3%, n = 40), Sulfamethoxazole-Trimethoprim: (79.2%, n = 38), Ampicillin: (77.1%, n = 37), Streptomycin: (72.9%, n = 35), Nalidixic acid: (50%, n = 24), Gentamicin: (41.7%, n = 20), Chloramphenicol: (31.3%, n = 15), Cephalothin: (27.1%, n = 13), Nitrofurantoin: (10.4%, n = 5) and Imipenem: (6.3%, n = 3). Absence of lavatory (POR = 2.7, 95% CI = 1.1–6.7); existence of farm/market for >10years (POR = 2.5, 95% CI = 1.1–5.4) and PW’s history of diarrhea in last three months (POR = 2.8, CI = 1.2–6.3) were associated with MDR. Controlling for age, absence of lavatory (adjusted OR [aOR] = 4.31, 95% CI = 1.6–11.9); PW’s history of diarrhea in last three months (aOR = 3.3,95%CI = 1.3–8.5) and work exposure >10years (aOR = 0.3, 95%CI = 0.1–0.9) remained independent risk factors for MDR.

Conclusion

Prevalence of resistant E. coli was highest among farm-workers and associated with older farms/markets, occupational exposure of over 10 years and poor hygienic measures. The management of Municipal and Kuje Area Councils were recommended to provide lavatories for public use in farm-settlements/markets. The importance of hand-hygiene and responsible use of antimicrobials in poultry production was emphasized.

Klíčová slova:

Antimicrobials – Antibiotics – Livestock – Social systems – Antimicrobial resistance – Antibiotic resistance – Nigeria – Poultry

Zdroje

1. Kariuki S, Dougan G. Antibacterial resistance in sub-Saharan Africa: an underestimated emergency. Ann N Y Acad Sci. 2014;1323: 43–55. doi: 10.1111/nyas.12380 24628272

2. Nikaido H. Multidrug Resistance in Bacteria. Annu Rev Biochem. 2009;78: 119–146. doi: 10.1146/annurev.biochem.78.082907.145923 19231985

3. Szmolka A, Nagy B. Multidrug resistant commensal Escherichia coli in animals and its impact for public health. Front Microbiol. 2013;4: 258. doi: 10.3389/fmicb.2013.00258 24027562

4. Fair RJ, Tor Y. Antibiotics and bacterial resistance in the 21st century. Perspect Medicin Chem. 2014; 25–64. doi: 10.4137/PMC.S14459 25232278

5. Akintunde OK, Adeoti AI, Okoruwa VO, Omonona BT, Abu AO. Effect of Disease Management on Profitability of Poultry Egg Production in Southwest Nigeria. Asian J Poult Sci. 2015;9: 1–18. doi: 10.3923/ajpsaj.2015.1.18

6. Manyi-Loh C, Mamphweli S, Meyer E, Okoh A. Antibiotic Use in Agriculture and Its Consequential Resistance in Environmental Sources: Potential Public Health Implications. Molecules. 2018;23. doi: 10.3390/molecules23040795 29601469

7. Agyare C, Etsiapa Boamah V, Ngofi Zumbi C, Boateng Osei F. Antibiotic Use in Poultry Production and Its Effects on Bacterial Resistance. Antimicrobial Resistance—A Global Threat. IntechOpen; 2019. doi: 10.5772/intechopen.79371

8. Chishimba K, Hang’ombe BM, Muzandu K, Mshana SE, Matee MI, Nakajima C, et al. Detection of Extended-Spectrum Beta-Lactamase-Producing Escherichia coli in Market-Ready Chickens in Zambia. Int J Microbiol. 2016;2016: 1–5. doi: 10.1155/2016/5275724 27190518

9. Li B, Webster TJ. Bacteria antibiotic resistance: New challenges and opportunities for implant-associated orthopedic infections. J Orthop Res. 2018;36: 22–32. doi: 10.1002/jor.23656 28722231

10. Prestinaci F, Pezzotti P, Pantosti A. Antimicrobial resistance: A global multifaceted phenomenon. Pathogens and Global Health. Maney Publishing; 2015. pp. 309–318. doi: 10.1179/2047773215Y.0000000030 26343252

11. Michael CA, Dominey-Howes D, Labbate M. The antimicrobial resistance crisis: Causes, consequences, and management. Frontiers in Public Health. Frontiers Media S. A; 2014. doi: 10.3389/fpubh.2014.00145 25279369

12. Jasovský D, Littmann J, Zorzet A, Cars O. Antimicrobial resistance-a threat to the world’s sustainable development. Ups J Med Sci. 2016;121: 159–64. doi: 10.1080/03009734.2016.1195900 27416324

13. Miles TD, McLaughlin W, Brown PD. Antimicrobial resistance of Escherichia coli isolates from broiler chickens and humans. BMC Vet Res. 2006;2: 7. doi: 10.1186/1746-6148-2-7 16460561

14. Oloso NO, Fagbo S, Garbati M, Olonitola SO, Awosanya EJ, Aworh MK, et al. Antimicrobial resistance in food animals and the environment in Nigeria: A review. Int J Environ Res Public Health. 2018;15. doi: 10.3390/ijerph15061284 29914203

15. Ibrahim A, Junaidu A, Garba M. Multiple antibiotic residues in meat from slaughtered cattle in Nigeria. Internet J Vet Med. 2012;8: 6–10.

16. Igwe J, Olayinka B, Ehnimidu J, Onaolapo J. Virulent Characteristics of Multidrug Resistant E. coli from Zaria, Nigeria. Clin Microbiol Open Access. 2016;5. doi: 10.4172/2327-5073.1000268

17. NATIONAL BUREAU OF STATISTICS. [cited 21 Oct 2019]. https://www.nigerianstat.gov.ng/

18. Anzaku SA, Umoh JU, Abdu PA, Kabir J, Bala A. Serological Survey of Newcastle Disease in Free Ranging Local Chickens in the Federal Capital Territory, Abuja, Nigeria. New J Sci. 2017;2017: 1–5. doi: 10.1155/2017/9646138

19. Shakya S, Patyal A, Eknath Gade N. Occurrence and characteristics of extended-spectrum β-lactamases producing Escherichia coli in foods of animal origin and human clinical samples in Chhattisgarh, India. 2016 [cited 4 Jul 2019]. doi: 10.14202/vetworld.2016.996-1000

20. Hudzicki J. Kirby-Bauer Disk Diffusion Susceptibility Test Protocol. 2009.

21. Sandhu R, Dahiya S, Sayal P. Evaluation of multiple antibiotic resistance (MAR) index and Doxycycline susceptibility of Acinetobacter species among inpatients. Indian J Microbiol Res. 2016;3: 299.

22. Carter MW, Oakton KJ, Warner M, Livermore DM. Detection of extended-spectrum beta-lactamases in klebsiellae with the Oxoid combination disk method. J Clin Microbiol. 2000;38: 4228–32. Available: http://www.ncbi.nlm.nih.gov/pubmed/11060096 11060096

23. Zhuge X, Ji Y, Tang F, Sun Y, Jiang M, Hu W. Population Structure and Antimicrobial Resistance Traits of Avian-origin. 2017; 0–2 31059196

24. Cho S-H, Lim Y-S, Kang Y-H. Comparison of Antimicrobial Resistance in Escherichia coli Strains Isolated From Healthy Poultry and Swine Farm Workers Using Antibiotics in Korea. Osong Public Heal Res Perspect. 2012;3: 151–155. doi: 10.1016/j.phrp.2012.07.002 24159507

25. van den Bogaard AE. Antibiotic resistance of faecal Escherichia coli in poultry, poultry farmers and poultry slaughterers. J Antimicrob Chemother. 2001;47: 763–771. doi: 10.1093/jac/47.6.763 11389108

26. Thenmozhi S, Rajeswari P, Suresh Kumar BT, Saipriyanga V, Kalpana M. Multi-Drug Resistant Patterns of Biofilm Forming Aeromonas Hydrophila from Urine Samples | International Journal Of Pharmaceutical Sciences And Research. In: Int. J. Pharm Sci Res. 5(7): [Internet]. 2014 [cited 5 Jul 2019] pp. 2908–2918. Available: http://ijpsr.com/bft-article/multi-drug-resistant-patterns-of-biofilm-forming-aeromonas-hydrophila-from-urine-samples/?view=fulltext

27. Campbell JI, Nhung NT, Nhung HN, Van Minh P, Wagenaar JA. Prevalence and risk factors for carriage of antimicrobial-resistant Escherichia coli on household and small-scale chicken farms in the Mekong Delta of Vietnam. 2015; 2144–2152. doi: 10.1093/jac/dkv053 25755000

28. Saleem R., Ejaz H., Zafar A., Y S. Phenotypic characterization of extended-spectrum-beta—lactamase producing E. coli from healthy individuals, patients, sewage sludge, cattle, chickens and raw meat. 2017;33.

29. Winokur PL, Vonstein DL, Hoffman LJ, Uhlenhopp EK, Doern GV. Evidence for transfer of CMY-2 AmpC β-lactamase plasmids between Escherichia coli and Salmonella isolates from food animals and humans. Antimicrob Agents Chemother. 2001;45: 2716–2722. doi: 10.1128/AAC.45.10.2716-2722.2001 11557460

30. Guetiya Wadoum RE, Zambou NF, Anyangwe FF, Njimou JR, Coman MM, Verdenelli MC, et al. Abusive use of antibiotics in poultry farming in Cameroon and the public health implications. Br Poult Sci. 2016;57: 483–493. doi: 10.1080/00071668.2016.1180668 27113432

31. Zhang H, Zhai Z, Li Q, Liu L, Guo S, Li Q, et al. Characterization of Extended-Spectrum β-Lactamase–Producing Escherichia coli Isolates from Pigs and Farm Workers. J Food Prot. 2016;79: 1630–1634. doi: 10.4315/0362-028X.JFP-16-093 28221927

32. Founou LL, Founou RC, Essack SY. Antibiotic Resistance in the Food Chain : A Developing. 2016;7: 1–19. doi: 10.3389/fmicb.2016.01881 27933044

33. Eltai NO, Yassine HM, Al Thani AA, Abu Madi MA, Ismail A, Ibrahim E, et al. Prevalence of antibiotic resistant Escherichia coli isolates from fecal samples of food handlers in Qatar. Antimicrob Resist Infect Control. 2018;7: 78. doi: 10.1186/s13756-018-0369-2 29983931

34. Kluytmans J, Overdevest I, Willemsen I, Bergh M, Zwaluw K, Heck M, et al. Extended-Spectrum β -Lactamase–Producing Escherichia coli From Retail Chicken Meat and Humans: Comparison of Strains, Plasmids, Resistance Genes, and Virulence Factors. Clin Infect Dis. 2013;56: 478–87. doi: 10.1093/cid/cis929 23243181

35. Carattoli A. Animal reservoirs for extended spectrum β-lactamase producers. Clin Microbiol Infect. 2008;14: 117–123. doi: 10.1111/j.1469-0691.2007.01851.x 18154535

36. Caudell MA, Mair C, Subbiah M, Matthews L, Quinlan RJ, Quinlan MB, et al. Articles Identification of risk factors associated with carriage of resistant Escherichia coli in three culturally diverse ethnic groups in Tanzania: a biological and socioeconomic analysis. Lancet Planet Heal. 2018;2: e489–e497. doi: 10.1016/S2542-5196(18)30225-0 30396440

37. Singh S, Shukla S, Tandia N, Kumar N, Paliwal R. Pharma science monitor. 2014;5: 184–197.

38. Daniels JB, Call DR, Hancock D, Sischo WM, Baker K, Besser TE. Role of Ceftiofur in Selection and Dissemination of blaCMY-2-Mediated Cephalosporin Resistance in Salmonella enterica and Commensal Escherichia coli Isolates from Cattle. Appl Environ Microbiol. 2009;75: 3648–3655. doi: 10.1128/AEM.02435-08 19376926

39. Amaechi N, Nwankwo I, Olu S. Antibiotic Resistance Inescherichia Coli Isolate From Healthy Food Animals in Ngor Okpala, Imo State, Nigeria. IOSR J Agric Vet Sci. 2015;8: 55–59.

40. Huijbers PMC, Graat EAM, Haenen APJ, van Santen MG, van Essen-Zandbergen A, Mevius DJ, et al. Extended-spectrum and AmpC β-lactamase-producing Escherichia coli in broilers and people living and/or working on broiler farms: prevalence, risk factors and molecular characteristics. J Antimicrob Chemother. 2014;69: 2669–2675. doi: 10.1093/jac/dku178 24879667