doi: 10.14202/IJOH.2019.31-37
Share this article on [Facebook] [LinkedIn]
Article history: Received: 11-09-2018, Accepted: 06-03-2019, Published online: 28-03-2019
Corresponding author: H. F. Massawe
E-mail: heriele@yahoo.com
Citation: Massawe HF, Mdegela RH, Kurwijila LR. Antibiotic resistance of Staphylococcus aureus isolates from milk produced by smallholder dairy farmers in Mbeya Region, Tanzania. Int J One Health 2019;5:31-37.Aim: The study determined and evaluated the prevalence and antibiotic resistance of Staphylococcus aureus isolated from milk collected along the milk value chain from farm herds, milk collection center, and milk shops in Mbeya rural and Mbozi districts, Tanzania.
Materials and Methods: A total of 150 milk samples were collected; 96 from farmers' herds, 18 from milk collection centers, and 36 from milk shops. The samples were cultured in Mannitol salt agar for pathogen isolation and biochemical tests performed for confirmation of S. aureus. Kirby-Bauer disk diffusion method was employed for antibiotic resistance testing.
Results: One hundred and forty samples yielded Staphylococcus species; these were from farmer's herd (92), milk collection center (18), and milk shops (30), respectively. Biochemical tests showed that 21 (15%) were positive for S. aureus. The corresponding prevalence rates from the value chain nodes were 14.1%, 16.7%, and 16.7%, respectively. Resistance to penicillin was frequently observed (57.1%) and vancomycin was effective to all S. aureus isolates tested. Resistance along the sampling points showed a significant positive correlation (r=0.82, p<0.0001; r=0.65, p<0.003; and r=0.61, p<0.01) between farmers, milk collection points, and milk shops, respectively. More than half (57.1%) of the isolates exhibited resistance to three or more of the antibiotics used in this study. S. aureus isolates were shown to have a multiple antimicrobial resistance patterns, particularly with respect to penicillin, ampicillin, erythromycin, and tetracycline.
Conclusion: The level of staphylococcal isolates and the antibiotic resistance of S. aureus found in this study is an indication of subclinical mastitis, poor hygiene, and inappropriate use of antibiotics; therefore, education of farmers on subclinical mastitis control and proper use of antibiotics would be of benefits in these areas.
Keywords: milk contamination, milk products, multiple antibiotic resistant.
1. Spanu V, Spanu C, Virdis S, Cossu F, Scarano C, De Santis EP, et al. Virulence factors and genetic variability of Staphylococcus aureus strains isolated from raw sheep's milk cheese. Int J Food Microbiol 2012;153:53-7. [Crossref] [PubMed]
2. De Oliveira LP, Soares e Barros LS, Silva VC, Cirqueira MG. Study of Staphylococcus aureus in raw and pasteurized milk consumed in the Reconcavo area of the State of Bahia, Brazil. J Food Process Technol 2011;2:128. [Crossref]
3. Mdegela RH, Kusiluka LJ, Kapaga AM, Karimuribo ED, Turuka FM, Bundala A, et al. Prevalence and determinants of mastitis and milk-borne zoonoses in smallholder dairy farming sector in Kibaha and Morogoro districts in Eastern Tanzania. J Vet Med B Infect Dis Vet Public Health 2004;51:123-8. [Crossref] [PubMed]
4. Le Loir Y, Baron F, Gautier M. Staphylococcus aureus and food poisoning. Genet Mol Res 2003;2:63-76. [PubMed]
5. Abo-Shama UH. Prevalence and antimicrobial susceptibility of Staphylococcus aureus isolated from cattle, buffalo, sheep and goat`s raw milk in Sohag Governorate, Egypt. Assiut Vet Med J 2014;141:63-72.
6. Waters AE, Contente-Cuomo T, Buchhagen J, Liu CM, Watson L, Pearce K, et al. Multidrug-resistant Staphylococcus aureus in US meat and poultry. Clin Infect Dis 2011;52:1227-30. [Crossref] [PubMed] [PMC]
7. Marshall BM, Levy SB. Food animals and antimicrobials: Impacts on human health. Clin Microbiol Rev 2011;24:718-33. [Crossref] [PubMed] [PMC]
8. Shryock TR, Richwine A. The interface between veterinary and human antibiotic use. Ann N Y Acad Sci 2010;1213:92-105. [Crossref] [PubMed]
9. Abera M, Demiel B, Aragaw K, Regassa F, Regassa A. Isolation and identification of Staphylococcus aureus from bovine mastitis milk and their drug resistance pattern in Adama town, Ethiopia. J Vet Med Anim Health 2010;3:29-34.
10. Thaker HC, Brahmbhatt MN, Nayak JB. Isolation and identification of Staphylococcus aureus from milk and milk products and their drug resistance patterns in Anand, Gujarat. Vet World 2013;1:10-3. [Crossref]
11. Massawe HF, Makingi GI, Shija DS, Mdegela RH, Kurwijila LR. Prevalence of the staphylococcal enterotoxins genes in raw and milk products along the value chain in Mbeya and Mbozi Districts, Tanzania. J Nat Sci Res 2017;18:47-58.
12. Clinical and Laboratory Standards Institute (CLSI) Performance Standards for Antimicrobial Susceptibility Testing; 25th Informational Supplement. CLSI Document M100-S25, Clinical and Laboratory Standards Institute, Wayne, PA; 2015.
13. SAS Statistical Users Guide, Statistical Analysis System. 9th ed. Cary, NC, USA: SAS Institute Inc.; 2004. p. 1028.
14. Ayano AA, Hiriko F, Simyalew AM, Yohannes A. Prevalence of subclinical mastitis in lactating cows in selected commercial dairy farms of Holeta district. J Vet Med Anim Health 2013;3:67-72.
15. Kumar R, Prasad A. Detection of E. coli and Staphylococcus in milk and milk products in and around Pantnagar. Vet World 2010;11:495-6.
16. Fagundes H, Barchesi L, Filho AN, Ferreira LM, Oliveira CA. Occurrence of Staphylococcus aureus in raw milk produced in dairy farms in Sao Paulo state, Brazil. Braz J Microbiol 2010;2:376-80. [Crossref]
17. Bendahou A, Lebbadi M, Ennanei L, Essadqui FZ, Abid M. Characterization of Staphylococcus species isolated from raw milk and milk products (lben and jben) in North Morocco. J Infect Dev Ctries 2008;2:218-25. [PubMed]
18. Sarkar P, Mohanta D, Debnath C. Staphylococcus aureus in dairy animals and farm workers in a closed herd in Karnal, North India: Assessment of prevalence rate and COA variations. Int J Innov Res Sci Eng Technol 2014;4:10962-72.
19. Ateba CN, Mbewe M, Moneoang MS, Bezuidenhout C.C. Antibiotic resistance Staphylococcus aureus isolated from milk in Mafikeng Area, North West province, South Africa. S Afr J Sci 2010;11-12:243-8.
20. Tarekgne E, Skeie S, Rudi K, Skjerdal T, Narvhus JA. Staphylococcus aureus and other Staphylococcus species in milk and milk products from Tigray region, Northern Ethiopia. Afr J Food Sci 2015;12:567.
21. De Buyser ML, Dufour B, Maire M, Lafarge V. Implication of milk and milk products in food-borne diseases in France and in different industrialized countries. Int J Food Microbiol 2001;1-2:1-17. [Crossref]
22. Desissa F, Makita K, Teklu A, Grace D. Contamination of informally marketed bovine milk with Staphylococcus aureus in urban and Peri-urban areas of Debre-Zeit, Ethiopia. Afr J Dairy Farm Milk Prod 2013;1:8-11.
23. Omore A, Stall SJ, Osafo EL, Kurwijila L, Barton D, Mdoe N, et al. Market Mechanisms, Efficiency, Processing and Public Health Risks in Peri-Urban Dairy Product Markets: Synthesis of Findings from Ghana and Tanzania. Final Technical Report for LPP Project R7321; 2004. p. 138.
24. Hamidi A, Sylejmani D. Antimicrobial susceptibility of staphylococci isolated from clinical mastitis in dairy cows in Kosovo. Bulg J Agric Sci 2016;5:836-9.
25. Al-Thani R, Al-Ali F. Incidences and antimicrobial susceptibility profile of Staphylococcus species isolated from animals in different Qatari farms. Afr J Microbiol Res 2012;48:7454-8.
26. Gandhale D, Kolhe R, Nalband SD, Jagtap U, Dhandore C, Bhave S, et al. Molecular types and antimicrobial resistance profile of Staphylococcus aureus isolated from dairy cows and farm environments. Turk J Vet Anim Sci 2017;41:713-24. [Crossref]
27. Mohanta A, Mazumder PB. Detection of staphylococci in raw milk and milk products and evaluation of their antibiotic sensitivity: A report from Southern Assam, India. J Environ Sci Toxic Food Technol 2015;3:17-22.
28. Kenar B, Bagcigil AF, Kuyucuoglu Y, Kahraman BB, Konak S. Antimicrobial susceptibility profiles and coagulase gene polymorphism of Staphylococcus aureus isolated from bovine subclinical mastitis. Kafkas Univ Vet Fak Derg 2017;4:535-40.
29. De Oliveira A, Watts J, Salmon S, Aarestrup FM. Antimicrobial susceptibility of Staphylococcus aureus isolated from bovine mastitis in Europe and the United States. J Dairy Sci 2000;4:855-62. [Crossref]
30. dos Santo LL, Viana C, Farinha G, Otutumi KL, Gerbasi AV. Antimicrobial susceptibility of strains of Staphylococcus aureus and Staphylococcus coagulase-negative isolated from cows' milk with mastitis in the west of Parana, Brazil Enciclopedia Biosfera. Centro Cientifico Conhecer - Goiania 2013;17:214-23.
31. Mekuria A, Asrat D, Woldeamanuel Y, Tefera G. Identification and antimicrobial susceptibility of Staphylococcus aureus isolated from milk samples of dairy cows and nasal swabs of farm workers in selected dairy farms around Addis Ababa, Ethiopia. Afr J Microbiol Res 2013;27:3501-3510.
32. Firaol T, Yitagele T, Nateneal T, Endrias Z. Isolation, identifications and antimicrobial susceptibility pattern of coagulase positive Staphylococcus from subclinical mastitis dairy cattle in and around Haramaya University. Ethiop Vet J 2015;2:41-53.