Survey on antimicrobial usage in local dairy cows in North-central Nigeria: Drivers for misuse and public health threats

English version

Autoři: Nma Bida Alhaji ^aff001; Mohammed Baba Aliyu ^aff001; Ibrahim Ghali-Mohammed ^aff002; Ismail Ayoade Odetokun ^aff002
Působiště autorů: Department of Public Health and Epidemiology, Niger State Ministry of Livestock and Fisheries, Minna, Nigeria ^aff001; Department of Veterinary Public Health and Preventive Medicine, University of Ilorin, Ilorin, Nigeria ^aff002
Vyšlo v časopise: PLoS ONE 14(12)
Kategorie: Research Article
prolekare.web.journal.doi_sk: https://doi.org/10.1371/journal.pone.0224949

Souhrn

Background

Antimicrobials are used as a measure to maintain good health and productivity of lactating cows. This study assessed pastoralists’ knowledge and practices regarding AMU in lactating cows; and risk pathways for AMR dissemination from cow milk to humans.

Methods

Interview questionnaire-based cross-sectional study was conducted in Fulani pastoral communities. Frequencies and proportions were used for descriptive statistics. Chi-square test and multivariable logistic regressions were used for analytic statistics at 95% confidence level.

Results

All recruited 384 pastoral households participated. About 11% of participants indicated antimicrobials misuse as when given at under-dose, while 58.9% had no knowledge of what antimicrobial misuse entailed. Most participants (51.6%) were unaware about effects of improper AMU. Most respondents (61.7%) reported self-prescription of antimicrobials used on cows. Also, 67.4% of respondents reported arbitrary applications of antimicrobials used in cows, while 15% used antimicrobials to increase milk yield. Frequently used antimicrobials were: tetracycline (98.7%), penicillin (96.6%), streptomycin (95.8%) and sulfonamides (95.3%). Consumption of raw milk and milk products (p = 0.010); contacts with contaminated udder (p = 0.002); and aerosols of discarded contaminated milk P = 0.001) were perceived risk pathways for spread of antimicrobial resistance from cow milk. Improper AMU (p<0.001), non-enforcement of regulating laws (p<0.001), weak financial status (p<0.001), and low education and expertise (p<0.001) influenced antimicrobials misuse in lactating cows.

Conclusions

This study highlighted low levels of knowledge, risk perceptions and practices regarding AMU and AMR among survey pastoralists. This calls for education of the vulnerable populations on promotion of prudent AMU in lactating cows through ‘One Health’ approach, to assure food safety, food security, and public and environmental health.

Klíčová slova:

Public and occupational health – Antimicrobials – Milk – Livestock – Antimicrobial resistance – Nigeria – Mastitis – Bovine mastitis

Zdroje

1. Sharma C, Rokana N, Chandra M, Singh BP, Gulhane RD, Gill JPS, et al. Antimicrobial Resistance: Its Surveillance, Impact, and Alternative Management Strategies in Dairy Animals. Front Vet Sci. 2018; 4:237. doi: 10.3389/fvets.2017.00237 29359135

2. FAO. World Livestock 2011: Livestock in food security. Food and Agriculture Organization of the United Nations, Rome, Italy; 2011. Available: http://www.fao.org/3/i2373e/i2373e.pdf Accessed 18 October 2019.

3. Hemme T, Otte J. Status and Prospects for Smallholder Milk Production: A Global Perspective. In: Pro-Poor Livestock Policy Initiative, editor. A Living from Livestock. Food and Agriculture Organization of the United Nations, Rome, Italy; 2010. pp. 1–12. Available: http://www.fao.org/docrep/012/i1522e/i1522e00.pdf. Accessed 18 October 2019.

4. Annatte I. Nigeria- Milk production Fact Sheet. In: IFCN Dairy Report 2009, International Farm Comparison Network, Dairy Research Center, Kiel, Germany 2010; Vol. 3.63 (129).

5. Gussmann MK, Steeneveld W, Kirkeby CT, Hogeveen H, Farre M, Halasa T. Economic and epidemiological impact of different intervention strategies for subclinical and clinical mastitis. 2019; Prev Vet Med. 166:78–85. doi: 10.1016/j.prevetmed.2019.03.001 30935508

6. Stevens M, Piepers S, De Vliegher S. The effect of mastitis management input and implementation of mastitis management on udder health, milk quality, and antimicrobial consumption in dairy herds. J Dairy Sci. 2019; 102(3):2401–2415. doi: 10.3168/jds.2018-15237 30692005

7. Van Boeckel TP, Brower C, Gilbert M, Grenfella BT, Levina SA, Robinson TP, et al. Global trends in antimicrobial use in food animals. Proc Natl Acad Sci USA (PNAS). 2015; 12(18):5649–5654. http://dx.doi.org/10.1073/pnas.1503141112

8. WHO. Antimicrobial resistance. World Health Organization Fact Sheet, No. 194, 2016. Available: http://www.who.int/mediacentre/factsheets/fs194/en. Accessed 22 November 2018.

9. Littmann J, Viens AM. The ethical significance of antimicrobial resistance. Pub Health Ethics. 2015; 8(3):209–24. https://doi.org/10.1093/phe/phv025

10. Robinson TP, Bu DP, Carrique-Mas J, Fevre EM, Gilbert M, Grace D, et al. Antibiotic resistance is the quintessential One Health issue. Trans R Soc Trop Med Hyg. 2016; 110(7):377–380. doi: 10.1093/trstmh/trw048 27475987

11. Suleiman H. Policy issues in agropastoral development in Nigeria. Proceedings of the National Conference on Pastoralism in Nigeria, Ahmadu Bello University Zaria, Nigeria; 1988.

12. de Leeuw PN, McDermott JJ, Lebbie SHB. Monitoring of livestock health and production in sub-Saharan Africa. Prev Vet Med. 1995; 25:195–212.

13. Hochbaum GM. Public Participation in Medical Screening Programs: A Socio-psychological Study, Public Health Service Publication No. 572, Washington DC; 1958.

14. Dean AG, Sullivan KM, Soe MM. Open Source Epidemiologic Statistics for Public Health (OpenEpi), Version 2.3.1; 2009.

15. Thrusfield M. Veterinary Epidemiology. 3rd ed, Blackwell Science Ltd, a Blackwell Publishing company, 9600 Garsington Road, Oxford OX4 2DQ, UK, 2009; p. 228–238.

16. WMADH. World Medical Association Declaration of Helsinki. Ethical principles for medical research involving human subjects. Bull World Health Organ. 2001; 373–374. 11357217

17. Alhaji NB, Babalobi OO, Isola TO. A quantitative exploration of nomadic pastoralists’ knowledge and practices towards Rift Valley fever in Niger State, North-central Nigeria: The associated sociocultural drivers. One Health, 2018; 6(1):16–22. https://doi.org/10.1016/j.onehlt.2018.09.001

18. Dohoo I, Martin W, Studahl H. Measures of Association. In: McPike SM, editor. Veterinary Epidemiologic Research, 2nd ed., University of Prince Edward Island, Charlottetown, PE, Canada; 2009; 136–148.

19. Aminov R.I, Mackie RI. Evolution and ecology of antibiotic resistance genes, FEMS Microbiol Lett. 2007; 271:147–161. doi: 10.1111/j.1574-6968.2007.00757.x 17490428

20. More SJ, Clegg TA, O’Grady L. Insights into udder health and intramammary antibiotic usage on Irish dairy farms during 2003–2010. Irish Vet J. 2012; 65:7. https://doi.org/10.1186/2046-0481-65-7

21. Asredie T, Engdaw TA. 2015. Antimicrobial Residues in Cow Milk and its Public Health Significance. World J Dairy Food Sci. 2015; 10(2):147–153. https://doi.org/10.5829/idosi.wjdfs.2015.10.2.96244

22. Okoli IC, Nwosu CI, Okoli GC, Okeudo NJ, Ibekwe V. Drug management of anti-microbial resistance in avian bacterial pathogen in Nigeria, Intern J Environ Health Human Dev. 2002; 3(1):39–48.

23. Sirdar MM, Picard J, Bisschop S, Gummow BA. A questionnaire survey of poultry layer farmers in Khartoum State, Sudan, to study their antimicrobial awareness and usage patterns. Onderstepoort J Vet Res. 2012; 79(1):1–8. https://doi.org/10.4102/ojvr.v79i1.361

24. Oluwasile BB, Agbaje M, Ojo OE, Dipeolu MA. Antibiotic usage pattern in selected poultry farms in Ogun state. Sokoto J Vet Sci. 2014; 12(1):45–50. https://doi.org/10.4314/sokjvs.v12i1.7

25. Alhaji NB, Haruna AE, Muhammad B, Lawan MK, Isola TO. Antimicrobials usage assessments in commercial poultry and local birds in North-central Nigeria: Associated pathways and factors for resistance emergence and spread. Prev Vet Med. 2018; 154:139–147. doi: 10.1016/j.prevetmed.2018.04.001 29685438

26. Morgan DJ, Okeke LN, Laxminarayan R, Perencevich EN, Weisenberg S. Nonprescription antimicrobial use worldwide: a systematic review. Lancet Infect. Dis. 2011; 11:692–701. doi: 10.1016/S1473-3099(11)70054-8 21659004

27. Locatelli C, Cremonesi P, Caprioli A, Carfora V, Ianzano A, Barberio A, Morandi S, et al., Occurrence of methicillin-resistant Staphylococcus aureus in dairy cattle herds, related swine farms, and humans in contact with herds. J Dairy Sci. 2017; 100(1):608–619. doi: 10.3168/jds.2016-11797 27865508

28. Martinez JL. Antibiotics and antibiotic resistance genes in natural environments. Science. 2008; 321:365–367. doi: 10.1126/science.1159483 18635792

29. You Y, Silbergeld EK. Learning from agriculture: understanding low-dose antimicrobials as drivers of resistome expansion, Front Microbiol. 2014; 5:284. doi: 10.3389/fmicb.2014.00284 24959164

30. Adesokan HK, Akanbi IO, Akanbi IM, Obaweda RA. Pattern of antimicrobial usage in livestock animals in south-western Nigeria: the need for alternative plans. Onderstepoort J Vet Res. 2015; 82(1):Art #816, 6 pages. http://dx.doi.org/10.4102/ojvr.v82i1.816

31. Alhaji NB, Isola TO. Antimicrobial usage by pastoralists in food animals in North-central Nigeria: The associated socio-cultural drivers for antimicrobials misuse and public health implications. One Health. 2018; 6(1):41–47. https://doi.org/10.1016/j.onehlt.2018.11.001

32. Katakweba AAS, Mtambo MMA, Olsen JE, Muhairwa AP. Awareness of human health risks associated with the use of antibiotics among livestock keepers and factors that contribute to selection of antibiotic resistance bacteria within livestock in Tanzania. Livest Res Rural Dev. 2012; 24:170. Art #.

33. Landers TF, Cohen B, Wittum TE, Larson EL. A review of antibiotic use in food animals: perspective, policy, and potential. Pub Health Rep. 2012; 127(1):4–22. https://doi.org/10.1177/003335491212700103

34. Eagar H, Swan G, Van Vuuren M. A survey of antimicrobial usage in animals in South Africa with specific reference to food animals. J South Afr Vet Assoc. 2012; 83(1):Art #16. 8 pages. http://dx.doi.org/10.4102/jsava.v83i1.16

35. Sahoo KC, Tamhankar AJ, Johansson E, Lundborg CS. Antibiotic use, resistance development and environmental factors: a qualitative study among healthcare professionals in Orissa, India. BMC Pub Health. 2010; 10(629):1–10. http://dx.doi.org/10.1186/1471-2458-10-629

36. Smith GW, Gehring R, Craigmill AL, Webb AI, Riviere JE. Extra-label intramammary use of drugs in dairy cattle. J Am Vet Med Assoc. 2005; 226:1994–1996. 15989181

37. Woolridge M, Evidence for the circulation of antimicrobial-resistant strains and genes in nature and especially between humans and animals, Rev Sci Techn Off Int Epiz. 2012; 31:231–247.

38. Mceachran AD, Blackwell BR, Hanson JD, Wooten KJ, Mayer GD, Cox SB et al. Antibiotics, bacteria, and antibiotic resistance genes: aerial transport from cattle feed yards via particulate matter. Environ Health Perspect. 2015; 123:337–343. doi: 10.1289/ehp.1408555 25633846

39. Lhermie G, Grohn YT, Raboisson D. Addressing antimicrobial resistance: an overview of priority actions to prevent suboptimal antimicrobial use in food animal production. Front Microbiol. 2016; 7:2114. doi: 10.3389/fmicb.2016.02114 28111568

40. Marshall BM, Levy SB. Food animals and antimicrobials: impacts on human health. Clin Microbiol Rev. 2011; 24:718–33. doi: 10.1128/CMR.00002-11 21976606

41. Chang Q, Wang W, Regev-Yochay G, Lipsitch M, Hanage WP. Antibiotics in agriculture and the risk to human health: how worried should we be? Evol Appl. 2015; 8:240–5. doi: 10.1111/eva.12185 25861382

42. McEwen SA. Antibiotic use in animal agriculture: what have we learned and where are we going? Anim Biotechnol. 2006; 17:239–250. doi: 10.1080/10495390600957233 17127534

43. Mtenga A, Emanuel M, Mabula J, Peter R. Consumer and Practitioner Education: Status of Antibiotic Resistance, Alliance for the Prudent Use of Antibiotics (APUA), 136 Harrison Avenue, Boston, 2011.