Prevalence of Antibiotic Resistance among Mycobacterium Tuberculosis Complex Species from Camel Milk in Isiolo County, Kenya
Keywords:
Antibiotic resistance, Mycobacterium tuberculosis complex, camel, multi-drug resistanceAbstract
The rising levels of antibiotic resistance among bacterial pathogens is a major global concern of human and animal health. This has been attributed to unauthorized use of therapeutic drugs in livestock, a situation which is worse in pastoral system, which may result in residual antibiotic residues and antibiotic resistance in animal based-food such as milk, meat, eggs and fish. In Kenya, however, there is no formal surveillance system for drug resistance among livestock and human bacterial isolates. Therefore, there is limited data on prevalence of multi-drug resistant zoonotic diseases due to consumption of animal based foods. The aim of this study was to determine presence of Mycobacterium tuberculosis complex (MTBC) species and multi-antibiotic resistant MTBC species in camel milk in Isiolo County, Kenya. Raw camel milk was aseptically collected from 308 positive, negative and inconclusive bovine reactor
, and positive avian reactor camels randomly selected from 15 camel herds in 3 major camel producing milk clusters in Isiolo County, Kenya. DNA was extracted directly from raw camel milk samples. A first single step Polymerase Chain Reaction (PCR) using primer set MTB-F 5'-CGGGTATGCTGTTAGGCGACG-3' and MTB-R 5'CCACCACAAGACATGCATG-3' was done to determine presence of MTBC species in camel milk samples. A second single step PCR using primer set RF1 5’-GGTCGCCGCGATCAAGGAGT-3’ and RF2 5’TGCACGTCGCGGACCTCCA-3’, targeting the rpoB gene, a marker of multi-drug resistant TB, was done to determine presence of multi-drug resistant MTBC species. The prevalence of MTBC species and multi-drug resistant MTBC species in raw camel milk was 3.1% and 1.55%, respectively. The presence of MTBC species and multi-drug resistant MTBC species in raw camel milk should be major public health concern to veterinary and human health medical services; especially among pastoralists who are traditionally accustomed to consuming raw camel milk.
References
FAO/WHO. Residues of some veterinary drugs in animals and foods. Sixty-second report of the Joint FAO/WHO 41/16. Food and Agriculture Organization and World Health Organization, Rome, pp 109, 2004.
Global Antibiotic Resistance Partnership-Kenya Working Group. Situation analysis and recommendations: Antibiotic use and resistance in Kenya. Washington, DC and New Delhi: Center for Disease Dynamics, Economics & Policy. 2011.
UN. High-level meeting on antimicrobial resistance convened by the President of the General Assembly. Resolutions No. 70/183 and 70/29, Report No. 7A/INF/71/4. 71st session of United Nations General Assembly, United Nations Headquarters, New York, 19 to 26 September, 2016.
WHO. Integrated surveillance of antimicrobial resistance in foodborne bacteria: Application of a One Health approach. World Health Organization. ISBN 978-92-4-151241-1, 2017.
Robinson, T.P., Bu, D.P., Carrique-Mas, J., Fevre, E.M., Gilbert, M., Grace, D., Hay, S.I., Jiwakanon, J., Kakkar, M., Kariuki, S., Laxminarayan, R., Lubroth, J., Magnusson, U., Thi Ngoc, P., Van Boeckel, T.P., Woolhouse, M.E.J. Opinion paper: Antibiotic resistance: mitigation opportunities in livestock sector development. Animal, 11(1), pp 1–3, 2017.
Catery, B., Laevens, H., Deverisa, L.A., Opsomer, G., De Kruif, A. Antimicrobial resistance in milk and meat; perceptions and realities. Journal of Veterinary Medicine, 87, pp 1222-1228, 2003.
Ben-Madhi, M.H., Ouslimani, S. Mise en évidence de résidus d’antibiotiques dans le lait de vache produit dans l’algérois. European Journal of Science Research, 36 (3), pp 357-362, 2009.
Samandoulougou, S., Ilboudo, A.J., Bagre, T.S., Tapsoba, F.W., Savadogo, A., Scippo, M., Traore, A.S. Screening of antibiotic residues in beef consumed in Ouagadougou, Burkina Faso. African Journal of Food Science, 9(6), pp 367-371, 2015.
MRA (Ministère des ressources animales). Annuaire statistiques du secteur de l’élevage. Ouagadougou, Burkina Faso. pp 151, 2011.
Lamuka, P.O., Njeruh, F.M., Gitao, G.C. Abey, K.A. Camel health management and pastoralists’ knowledge and information on zoonoses and food safety risks in Isiolo County, Kenya. Pastoralism: Research, Policy and Practice, 7, pp 20-30, DOI 10.1186/s13570-017-0095-z. 2017.
Robinson, T.P., Wertheim, H.F.L., Kakkar, M., Kariuki, S., Bu, D., Price, L.B. Animal production and antimicrobial resistance in the clinic. The Lancet, 387, e1–e3, 2016a.
UNAIDS. Joint United Nations programme on HIV/AIDS (UNAIDS). JUNP on H. Global report: UNAIDS report on the global AIDS epidemic. UNAIDS/JC2502/1/E. UNAIDS, 20. Geneva, Switzerland, 2013.
OIE. Terrestrial Code. Chapter 11.5 Bovine tuberculosis (2015). Available from: http://www.oie.int/index.php?id=169&L=0&htmfile=chapitre_bovine_tuberculosis.htm. Accessed December, 2016.
WHO. Factsheet No. 104: Tuberculosis (2015). Reviewed March 2015. Available from: http://www.who.int/mediacentre/factsheets/fs104/en/, 2015. Accessed December, 2016.
AVMA. One health: A new professional imperative. One health initiative task force, Final report. Schaumburg, IL: American Veterinary Medical Association, 2008.
Kaneene, J., Miller, R.A., Kaplan, B., Steele, J.H., Thoen, C.O. Preventing and controlling zoonotic tuberculosis: a one health approach. Veterinary Italian. 50, pp 7–22, 2014.
Robinson, T.P., Bu, D.P., Carrique-Mas, J., Fevre, E.M., Gilbert, M., Grace, D., Hay, S.I., Jiwakanon, J., Kakkar, M., Kariuki, S., Laxminarayan, R., Lubroth, J., Magnusson, U., Thi Ngoc, P., Van Boeckel, T.P., Woolhouse, M.E.J. Antibiotic resistance is the quintessential One Health issue. Trans Royal Society of Tropical Medicine and Hygiene, 110, pp 377–380, 2016b.
Omulo, S., Thumbi,S.M., Njenga, M.K., Call D.R. A review of 40 years of enteric antimicrobial resistance research in Eastern Africa: what can be done better? Antimicrobial Resistance and Infection Control, 4, pp 1-13, 2015.
Garcia-Rodriguez, J.A., Garcia-Sanchez, J.E., Trujillano, I. Lack of effective bactericidal activity of new quinolones against Brucella spp. Antimicrobial Agents Chemotherapy, 35, pp 756–759, 1991.
Ogaro, T.D., Githui, W., Kikuvi, G., Okari, J., Wangui, E., Asiko, V. Anti-tuberculosis drug resistance in Nairobi, Kenya. African Journal of Health Science, 20, pp 21-27, 2012.
Ombura, I.P., Onyango, N., Odera, S., Mutua, F., Nyagol, J. Prevalence of drug resistance Mycobacterium tuberculosis among Patients Seen in Coast Provincial General Hospital, Mombasa, Kenya. PLoS ONE 11(10): e0163994, 2016. https://doi.org/10.1371/journal.pone.0163994.
Ndung’u, P. W., Kariuki, S., Ng’ang’a, Z., Revathi, G. Resistance patterns of Mycobacterium tuberculosis isolates from pulmonary tuberculosis patients in Nairobi. Journal of Infection in Developing Countries, 6(1), pp 33-39, 2012. Available at: http://ecommons.aku.edu/eastafrica_fhs_mc_pathol/23.
Nyamogoba, H.D., Mbuthia, G., Mining, S., Kikuvi, G., Biegon, R., Mpoke, S., Menya, D., Waiyaki, P.G. HIV co-infection with tuberculous and non-tuberculous mycobacteria in western Kenya: challenges in the diagnosis and management. African Health Science, 12, pp 305-311, 2012.
Umubyeyi, A.N., V G, Gasana M, Basinga P, Zawadi JP, Gatabazi J, Pauwels P, Nzabintwali F, Nyiramasarabwe L, Fissette K, Rigouts L, Struelens MJ, Portaels F. Results of a national survey on drug resistance among pulmonary tuberculosis patients in Rwanda. International Journal of Tuberculosis Lung Diseases, 11(2), pp 189-194, 2007
Kibiki, G.S., Mulder, B., Dolmans, W.M., de Beer, J.L., Boeree, M., Sam, N., van Soolingen, D., Sola, C., van der Zanden, A.G. M. Tuberculosis genotypic diversity and drug susceptibility pattern in HIV-infected and non-HIV infected patients in northern Tanzania. BMC Microbiology, 7, pp 51-59, 2007.
Bazira, J., Asiimwe, B.B., Joloba, M.L., Bwanga, F., Matee, M.I. Mycobacterium tuberculosis spoligotypes and drug susceptibility pattern of isolates from tuberculosis patients in South-Western Uganda. BMC Infectious. Diseases, 11, pp 81-90, 2011.
Nyabundi, D., Onkoba, N., Kimathi, R., Nyachieo, A., Juma, G., Peter Kinyanjui, P., Kamau, J. Molecular characterization and antibiotic resistance profiles of Salmonella isolated from fecal matter of domestic animals and animal products in Nairobi. Tropical Diseases, Travel Medicine and Vaccines, 3, 2-7, 2017
Leal-Klevezas, D.S., Martinez-Vazquez, I.O., Lopez-Merino, A., Martinez-Soriano, J.P. Single-step PCR for detection of Brucella Spp. from blood and milk of infected animals. Journal of Clinical Microbiology, 33(12), pp 3087–3090, 1995.
Ilhan, Z., Solmaz, H., Aksakal, A., Gulhan, T., Ekin, I.H., Boynukara, B. Detection of Brucella melitensis DNA in the milk of sheep after abortion by PCR assay. Arch Medicine Veterinary, 40, pp 141-146, 2008.
Gonza’ lez-y-Merchand, J.A., Colston, M.J., Cox, RA. The rRNA operon of Mycobacterium smegmatis and Mycoba.cterium tuberculosis: comparison of promoter elements and of neighbouring upstream genes. Microbiology, 142, pp 667–67, 1996.
Kirschner, P., Springer, B., Vogel, U., Meier, A., Wrede, A., Kiekenbeck, M., Bange, F., Bottger, E.C. Genotypic identification of Mycobacteria by nucleic acid sequence determination: Report of a 2-year experience in a clinical laboratory. Journal of Clinical Microbiology, 31, pp 2882–2889, 1993.
De Beenhouwer, H., Lhiang, Z., Jannes, G., Mijs, W., Machtelinckx, L., Hartha, R., Traore, H., Portaels, F. Rapid detection of rifampicin resistance in sputum and biopsy specimens from tuberculosis patients by PCR and line probe assay. Tubercle Lung Diseases, 76, pp 425-430, 1995.
Sechi, L.A., Zanetti, S., Sanguinetti, M., Molicotti, P., Romano, L., Leori, G., Delogu, G., Boccia, S., La Sorda, M., Fadda, G. Molecular basis of rifampin and isoniazid resistance in Mycobacterium bovis strains isolated in Sardinia, Italy. Antimicrobial Agents. Chemotherapy, 45, pp 1645–1647, 2001.
Somoskovi, A., Parsons, L.M., Salfinger, M. The molecular basis of resistance to isoniazid, rifampin, and pyrazinamide in Mycobacterium tuberculosis. Respiratory Research, 2, pp 164–168, 2001.
Hermans, P.W.M., van Soolingen, D., Dale, J.W., Schuitema, A.R.J., McAdam, R.A., Catty, D., van Embden, J.D.A. Insertion element IS 986 from Mycobacterium tuberculosis: a useful tool for diagnosis and epidemiology of tuberculosis. Journal of Clinical Microbiology, 28, pp 2051–2058, 1990.
Yam, W.C., Tam, C.M., Leung, C.C., Tong, H.L., Chan, K.H., Leung, E.T.Y., Wong, K.C., Yew, W.W., Seto, W.H., Yuen, K.Y., Ho, P.L. Direct detection of rifampin-resistant Mycobacterium tuberculosis in respiratory specimens by PCR-DNA sequencing. Journal of Clinical Microbiology, 42(10), pp 4438–4443, 2004.
Kohanski, M.A., DePristo, M.A, Collins, J.J., Sublethal antibiotic treatment leads to multi-drug resistance via radical-induced mutagenesis. Molecular cell, 37(3), pp 311-320, 2010
Disassa, N., Sibhat, B., Mengistu, S., Muktar, Y., Belina, D. Prevalence and antimicrobial susceptibility pattern of E. coli O157:H7 isolate d from traditionally marketed raw cow milk in and around Asosa Town, Western Ethiopia. Veterinary Medicine International Article ID 7581531, 7 pages. 2017, https://doi.org/10.1155/2017/7581531.
O’Neill J 2016. Tackling drug-resistant infections globally: final report and recommendations. The review on antimicrobial resistance. Retrieved on 31 July 2017 from https://amr-review.org/sites/default/files/160518_Final paper, with cover.pdf.
Kariuki, S., Revathi G., Kariuki N., Kiiru, J., Mwituria, J., Muyodi, J., Githinji, J.W., Kagendo, D., Munyalo, A., Hart, C.A. Invasive multi-drug resistant non typhoidal Salmonella infections in Africa: zoonotic or anthroponotic transmission? Journal of Medical Microbiology, 55, pp 585-591, 2006.
Kariuki S, Revathi G, Gakuya F, Yamo V, Muyodi J, Hart CA. Lack of clonal relationship between non-typhi Salmonella strain types from humans and those isolated from animals living in close contact. FEMS Immunology Medical Microbiology, 33, pp 165-171, 2002.
Kariuki, S., Revathi, G., Muyodi, J., Mwituria, J., Munyalo, A., Kagendo, D., Murungi, L., Hart, C.A. Increasing prevalence of multidrug-resistant non-typhoidal salmonellae, Kenya, 1994–2003. International Journal of Antimicrobial Agents, 25, pp 39–45. 2005.
Omoshaba, E.O., Olufemi, F.O., Ojo, O.E., Sonibare, A.O., Agbaje, M. Multidrug-resistant Salmonellae isolated in Japanese quails reared in Abeokuta, Nigeria. Tropical Animal Health and Production, https://doi.org/10.1007/s11250-017-1347-z, pp 1-6, 2017.
Kariuki, S., Gilks, C.F., Kimari, J., Muyodi, J., Waiyaki P., Hart, C.A. Plasmid diversity of multi-drug-resistant Escherichia coli isolated from children with diarrhoea in a poultry-farming area in Kenya. Annals of Tropical Medicine & Parasitology, 91(1), 87-94, 1997.
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