Unravelling Antimicrobial Resistance Phenotypes and Carriage of Extended-Spectrum <i>β</i>-Lactamase Genes in <i>Escherichia coli</i> Isolated from Dairy Farms in Kiambu County, Kenya — Oak Academic Publishing
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Unravelling Antimicrobial Resistance Phenotypes and Carriage of Extended-Spectrum <i>β</i>-Lactamase Genes in <i>Escherichia coli</i> Isolated from Dairy Farms in Kiambu County, Kenya
Department of Biochemistry, Biotechnology & Microbiology, Kenyatta University, Nairobi, Kenya
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Centre for Microbiology Research, Kenya Medical Research Institute, Nairobi, Kenya
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Department of Biochemistry, Biotechnology & Microbiology, Kenyatta University, Nairobi, Kenya
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Centre for Microbiology Research, Kenya Medical Research Institute, Nairobi, Kenya
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Centre for Microbiology Research, Kenya Medical Research Institute, Nairobi, Kenya
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Centre for Microbiology Research, Kenya Medical Research Institute, Nairobi, Kenya
,
Centre for Microbiology Research, Kenya Medical Research Institute, Nairobi, Kenya
1 Department of Biochemistry, Biotechnology & Microbiology, Kenyatta University, Nairobi, Kenya
2 Centre for Microbiology Research, Kenya Medical Research Institute, Nairobi, Kenya
3 Department of Biochemistry, Biotechnology & Microbiology, Kenyatta University, Nairobi, Kenya
4 Centre for Microbiology Research, Kenya Medical Research Institute, Nairobi, Kenya
5 Centre for Microbiology Research, Kenya Medical Research Institute, Nairobi, Kenya
6 Centre for Microbiology Research, Kenya Medical Research Institute, Nairobi, Kenya
7 Centre for Microbiology Research, Kenya Medical Research Institute, Nairobi, Kenya
The use of antibiotics for prophylaxis and growth enhancement in livestock farming is on the increase globally. This practice has led to the emergence and spread of antimicrobial-resistant bacteria in livestock. Only limited research has been done to establish the role of cattle farming in antimicrobial resistance. The current study sought to establish the carriage of multi-drug resistance and extended-spectrum beta-lactamase genes in Escherichia coli from farmers, their cattle, and cattle slurry within Kiambu County. A total of 286 (81%) E. coli isolates were recovered from 352 samples analysed. Antibiotic resistance profiles showed 114 (40%) isolates were resistant to ≥3 antimicrobial classes and were considered multidrug-resistant. Among multidrug-resistant (MDR) E. coli strains, 40 (14%) were resistant to 3 different antimicrobial classes, while 71 (25%) were resistant to between 4 and 7 antibiotic classes. Extended-spectrum β -lactamase resistance was found in 18 isolates: human (n = 14), cattle (n = 2), and environmental (n = 2). Both the bla CTX-M and bla TEM genes were detected in 10 and 15 strains, respectively. Sequence analysis showed that the isolates carried the bla TEM-116 (n = 7), bla TEM-1 (n = 5), and bla CTX-M-15 (n = 8) genes. Genotyping MDR isolates using (GTG) 5 PCR demonstrated that the isolates were not clonal. This data shows antimicrobial resistance profiles and different types of resistance genes in the E. coli population on dairy farms. As a result, more effective, targeted public health policies and measures need to be put in place to control and prevent the emergence and spread of resistant bacteria.
O’neill, J. (2015) Antimicrobials in Agriculture and the Environment: Reducing Unnecessary Use and Waste. The Review on Antimicrobial Resistance, London.
Davies, S.C., Fowler, T., Watson, J., Livermore, D.M. and Walker, D. (2013) Annual Report of the Chief Medical Officer: Infection and the Rise of Antimicrobial Resistance. The Lancet, 381, 1606-1609. https://doi.org/10.1016/S0140-6736(13)60604-2
Kariuki, S. and Winters, C. (2010) GARP Activities in Kenya. The Center for Disease Dynamics, Economics & Policy/Global Antibiotic Resistance Partnership, Washington DC.
Sarmah, A.K., Meyer, M.T. and Boxall, A.B.A. (2006) A Global Perspective on the Use, Sales, Exposure Pathways, Occurrence, Fate and Effects of Veterinary Antibiotics (VAs) in the Environment. Chemosphere, 65, 725-759. https://doi.org/10.1016/j.chemosphere.2006.03.026
Menz, J., Olsson, O. and Kümmerer, K. (2019) Antibiotic Residues in Livestock Manure: Does the EU Risk Assessment Sufficiently Protect against Microbial Toxicity and Selection of Resistant Bacteria in the Environment? Journal of Hazardous Materials, 379, Article ID: 120807. https://doi.org/10.1016/j.jhazmat.2019.120807
United States Centers for Disease Control (2013) Antibiotic Resistance Threats in the United States, 2013.
Hendriksen, R.S., Mevius, D.J., Schroeter, A., Teale, C., Jouy, E., Butaye, P., et al. (2008) Occurrence of Antimicrobial Resistance among Bacterial Pathogens and Indicator Bacteria in Pigs in Different European Countries from Year 2002-2004: The ARBAO-II Study. Acta Veterinaria Scandinavica, 50, Article No. 19. https://doi.org/10.1186/1751-0147-50-19
Van den Bogaard, A.E.J.M. (2000) Antimicrobial Resistance in Pig Faecal Samples from the Netherlands (Five Abattoirs) and Sweden. Journal of Antimicrobial Chemotherapy, 45, 663-671. https://doi.org/10.1093/jac/45.5.663
Armoni, A., Barbón, J.L. and Petkou, A.C. (2002) Rotating Strings in Confining AdS/CFT Backgrounds. Journal of High Energy Physics, 2002, Article No. 69. https://doi.org/10.1088/1126-6708/2002/10/069
Pfeifer, Y., Cullik, A. and Witte, W. (2010) Resistance to Cephalosporins and Carbapenems in Gram-Negative Bacterial Pathogens. International Journal of Medical Microbiology, 300, 371-379. https://doi.org/10.1016/j.ijmm.2010.04.005
Bush, K. and Jacoby, G.A. (2010) Updated Functional Classification of β-Lactamases. Antimicrobial Agents and Chemotherapy, 54, 969-976. https://doi.org/10.1128/AAC.01009-09
-Lactamase (ESBL)
TEM 116
CTX-M-15
Kenya
Literak, I., Dolejska, M., Radimersky, T., Klimes, J., Friedman, M., Aarestrup, F.M., et al. (2010) Antimicrobial-Resistant Faecal Escherichia coli in Wild Mammals in Central Europe: Multiresistant Escherichia coli Producing Extended-Spectrum Beta-Lactamases in Wild Boars. Journal of Applied Microbiology, 108, 1702-1711. https://doi.org/10.1111/j.1365-2672.2009.04572.x
Hassell, J.M., Ward, M.J., Muloi, D., Bettridge, J.M., Robinson, T.P., Kariuki, S., et al. (2019) Clinically Relevant Antimicrobial Resistance at the Wildlife-Livestock-Human Interface in Nairobi: An Epidemiological Study. The Lancet Planetary Health, 3, e259-e269. https://doi.org/10.1016/S2542-5196(19)30083-X
Magiorakos, A.P., Srinivasan, A., Carey, R.B., Carmeli, Y., Falagas, M.E., Giske, C.G., et al. (2012) Multidrug-Resistant, Extensively Drug-Resistant and Pandrug-Resistant Bacteria: An International Expert Proposal for Interim Standard Definitions for Acquired Resistance. Clinical Microbiology and Infection, 18, 268-281. https://doi.org/10.1111/j.1469-0691.2011.03570.x
Dierikx, C., van der Goot, J., Fabri, T., van Essen-Zandbergen, A., Smith, H. and Mevius, D. (2013) Extended-Spectrum-β-Lactamase- and AmpC-β-Lactamase-Producing Escherichia coli in Dutch Broilers and Broiler Farmers. Journal of Antimicrobial Chemotherapy, 68, 60-67. https://doi.org/10.1093/jac/dks349
Mohapatra, B.R., Broersma, K. and Mazumder, A. (2007) Comparison of Five Rep-PCR Genomic Fingerprinting Methods for Differentiation of Fecal Escherichia coli from Humans, Poultry and Wild Birds. FEMS Microbiology Letters, 277, 98-106. https://doi.org/10.1111/j.1574-6968.2007.00948.x
Manske, M. (2006) GENtle, a Free Multi-Purpose Molecular Biology Tool. Doctoral Dissertation, Verlag Nicht Ermittelbar, Bern, 1-89. https://doi.org/10.1007/978-3-8349-9336-6_5
Altschul, S.F., Madden, T.L., Schäffer, A.A., Zhang, J., Zhang, Z., Miller, W., et al. (1997) Gapped BLAST and PSI-BLAST: A New Generation of Protein Database Search Programs. Nucleic Acids Research, 25, 3389-3402. https://doi.org/10.1093/nar/25.17.3389
Bevan, E.R., Powell, M.J., Toleman, M.A., Thomas, C.M., Piddock, L.J.V. and Hawkey, P.M. (2021) Molecular Characterization of Plasmids Encoding blaCTX-M from Faecal Escherichia coli in Travellers Returning to the UK from South Asia. Journal of Hospital Infection, 114, 134-143. https://doi.org/10.1016/j.jhin.2021.03.030
Agoba, E.E., Govinden, U., Peer, A.K.C., Osei Sekyere, J., Essack, S.Y. (2018) ISAba1 Regulated OXA-23 Carbapenem Resistance in Acinetobacter baumannii Strains in Durban, South Africa. Microbial Drug Resistance, 24, 1289-1295. https://doi.org/10.1089/mdr.2017.0172
Aslam, B., Wang, W., Arshad, M.I., Khurshid, M., Muzammil, S., Rasool, M.H., et al. (2018) Antibiotic Resistance: A Rundown of a Global Crisis. Infection and Drug Resistance, 11, 1645-1658. https://doi.org/10.2147/IDR.S173867
Lhermie, G., Gröhn, Y.T. and Raboisson, D. (2017) Addressing Antimicrobial Resistance: An Overview of Priority Actions to Prevent Suboptimal Antimicrobial Use in Food-Animal Production. Frontiers in Microbiology, 7, Article No. 2114. https://doi.org/10.3389/fmicb.2016.02114
Shrivastava, S.R., Shrivastava, P.S. and Ramasamy, J. (2018) World Health Organization Releases Global Priority List of Antibiotic-Resistant Bacteria to Guide Research, Discovery, and Development of New Antibiotics. Journal of Medical Society, 32, 76-77. https://doi.org/10.4103/jms.jms_25_17
Sharma, M., Millner, P.D., Hashem, F., Vinyard, B.T., East, C.L., Handy, E.T., et al. (2018) Survival of Escherichia coli in Manure-Amended Soils Is Affected by Spatiotemporal, Agricultural, and Weather Factors in the Mid-Atlantic United States. Applied and Environmental Microbiology, 85, e02392-18. https://doi.org/10.1128/AEM.02392-18
Durán-Lara, E.F., Valderrama, A. and Marican, A. (2020) Natural Organic Compounds for Application in Organic Farming. Agriculture, 10, Article 41. https://doi.org/10.3390/agriculture10020041
Strawn, L.K. and Truitt, L. (2019) Food Safety Modernization Act Produce Safety Rule Add-On Module General Rules: Soil Amendments. Virginia Cooperative Extension, 1-18.
Wilson, R.T. (2018) Domestic Livestock in African Cities: Production, Problems and Prospects. Open Urban Studies and Demography Journal, 4, 1-14. https://doi.org/10.2174/2352631901804010001
Fairbrother, J.M. and Nadeau, é. (2006) Escherichia coli: On-Farm Contamination of Animals. OIE Revue Scientifique et Technique, 25, 555-569. https://doi.org/10.20506/rst.25.2.1682
Taitt, C.R., Leski, T.A., Erwin, D.P., Odundo, E.A., Kipkemoi, N.C., Ndonye, J.N., et al. (2017) Antimicrobial Resistance of Klebsiella pneumoniae Stool Isolates Circulating in Kenya. PLoS ONE, 12, e0178880. https://doi.org/10.1371/journal.pone.0178880
Muloi, D., Kiiru, J., Ward, M.J., Hassell, J.M., Bettridge, J.M., Robinson, T.P., et al. (2019) Epidemiology of Antimicrobial-Resistant Escherichia coli Carriage in Sympatric Humans and Livestock in a Rapidly Urbanizing City. International Journal of Antimicrobial Agents, 54, 531-537. https://doi.org/10.1016/j.ijantimicag.2019.08.014
Mouiche, M.M.M., Moffo, F., Akoachere, J.F.T.K., Okah-Nnane, N.H., Mapiefou, N.P., Ndze, V.N., et al. (2019) Antimicrobial Resistance from a One Health Perspective in Cameroon: A Systematic Review and Meta-Analysis. BMC Public Health, 19, Article No. 1135. https://doi.org/10.1186/s12889-019-7450-5
Jacoby, G.A. and Sutton, L. (1991) Properties of Plasmids Responsible for Production of Extended-Spectrum β-Lactamases. Antimicrobial Agents and Chemotherapy, 35, 164-169. https://doi.org/10.1128/AAC.35.1.164
Moken, M.C., McMurry, L.M. and Levy, S.B. (1997) Selection of Multiple-Antibiotic-Resistant (Mar) Mutants of Escherichia coli by Using the Disinfectant Pine Oil: Roles of the Mar and acrAB Loci. Antimicrobial Agents and Chemotherapy, 41, 2770-2772. https://doi.org/10.1128/AAC.41.12.2770
Liebana, E., Batchelor, M., Hopkins, K.L., Clifton-Hadley, F.A., Teale, C.J., Foster, A., et al. (2006) Longitudinal Farm Study of Extended-Spectrum Β-lactamase-mediated Resistance. Journal of Clinical Microbiology, 44, 1630-1634. https://doi.org/10.1128/JCM.44.5.1630-1634.2006
Watson, E., Jeckel, S., Snow, L., Stubbs, R., Teale, C., Wearing, H., et al. (2012) Epidemiology of Extended Spectrum Beta-Lactamase E. coli (CTX-M-15) on a Commercial Dairy Farm. Veterinary Microbiology, 154, 339-346. https://doi.org/10.1016/j.vetmic.2011.07.020
Lahlaoui, H., Dahmen, S., Moussa, M.B. and Omrane, B. (2011) First Detection of TEM-116 Extended-Spectrum β-Lactamase in a Providencia stuartii Isolate from a Tunisian Hospital. Indian Journal of Medical Microbiology, 29, 258-261. https://doi.org/10.4103/0255-0857.83909
Gevers, D., Huys, G. and Swings, J. (2001) Applicability of rep-PCR Fingerprinting for Identification of Lactobacillus Species. FEMS Microbiology Letters, 205, 31-36. https://doi.org/10.1111/j.1574-6968.2001.tb10921.x
Hartmann, A., Locatelli, A., Amoureux, L., Depret, G., Jolivet, C., Gueneau, E., et al. (2012) Occurrence of CTX-M Producing Escherichia coli in Soils, Cattle, and Farm Environment in France (Burgundy Region). Frontiers in Microbiology, 3, Article No. 83. https://doi.org/10.3389/fmicb.2012.00083