Antibiotic resistance and heavy metal tolerance of livestock-associated Methicillin resistant Staphylococcus aureus in selected livestock settings in Zaria, Nigeria
DOI:
https://doi.org/10.47430/ujmr.2492.023Keywords:
Anti-microbial resistance, livestock, Abattoir, MRSA, heavy metal tolerance, poultry farmAbstract
Study’s Excerpt:
• Most S. aureus isolates had a MAR index ≥0.2 and exhibited beta-lactam resistance.
• S. aureus isolates exhibited varying copper and zinc tolerance irrespective of their source.
• There was a correlation between MAR index and copper tolerance limit of S. aureus isolated from poultry farms.
• The total MRSA from the abattoir and cattle ranch was greater than that from poultry farms.
• However, the MRSA of poultry farm workers was greater than that of abattoir/cattle ranch workers.
Full Abstract:
The inappropriate antibiotic use in animal husbandry raises concerns about possible reservoirs and transmission pathways of methicillin-resistant Staphylococcus aureus (MRSA) in livestock environments. This study assessed the antibiotic resistance and heavy metal tolerance of S. aureus isolated from livestock farm settings; abattoir and cattle ranch, and poultry farms in Zaria, Nigeria. This involved sample and data collection, heavy metal analysis, isolation of S. aureus, antibiogram, and heavy metal tolerance assay. Copper and Zinc concentrations varied in the water and animal wastes (cow dung and poultry litter) samples. Copper concentrations were higher in the cow dung (13.5-16.0 mg/L) compared to poultry litter (7.8-12.2mg/L). Zinc concentrations were higher in poultry litter (77.7-99.9 mg/L) compared to cow dung (44.1-66.4 mg/L). Out of a total of 76 S. aureus isolates, 65.8% (50/76) were MRSA with 77.8% (28/36) and 55% (22/40) from the abattoir and cattle ranch, and poultry farms respectively. S. aureus with MAR index ≥0.2 were greater for the abattoir and cattle ranch (75%) compared with those from the poultry farms (50%) with most isolates exhibiting beta-lactam resistance. MRSA distribution varied with sample type with most isolated from water samples. MRSA isolates from livestock handlers in the poultry farms (27.3%) were greater than those from the abattoir and cattle ranch (7.1%). S. aureus isolates exhibited varying Copper and Zinc tolerance limits irrespective of their source. Proper implementation of biosecurity measures, antimicrobial resistance (AMR) surveillance, and policies are required to decrease the transmission of MRSA and AMR dissemination in livestock settings.
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References
Adekanmbi, A., & Falodun, O. (2015). Heavy metals and antibiotics susceptibility profiles of Staphylococcus aureus isolated from several points receiving daily input from the Bodija abattoir in Ibadan, Oyo State, Nigeria. Advances in Microbiology, 5, 871–880. https://doi.org/10.4236/aim.2015.513091
Agu, A. P., Onah, C. K., Umeokonkwo, C. D., Nnabu, R. C., & Una, A. F. I. (2021). Hygiene practices in abattoir and slaughter slab, determinants and assessment of abattoir and slaughter slab facilities in Abakaliki, Ebonyi State South-East Nigeria. African Health Sciences, 21(4), 1914–1923. https://doi.org/10.4314/ahs.v21i4.50
Akinnusi, F. A., Sodiya, C. I., & Adamu, C. O. (2018). Determinants of farmers' use of farm hygiene practices in preventing and controlling poultry diseases in Lagos State, Nigeria. Journal of Agricultural Extension, 22(2), 13–27. https://doi.org/10.4314/jae.v22i2.2
Amalesh, S., Bera, P., & Khatun, M. (2012). An investigation on heavy metal tolerance and antibiotic resistance properties of bacterial strain Bacillus sp. isolated from municipal waste. Journal of Microbiology and Biotechnology Research Scholars, 2(1), 178–189.
Argudín A, Lauzat B, Kraushaar B, Alba P, Agerso Y, Cavaco L, Butaye P, Porrero, MC, Battisti A, Tenhagen B, Fetsch A, Guerra B. 2016. Heavy metal and disinfectant resistance genes among livestock-associated methicillin-resistant Staphylococcus aureus Vet. Microbiol.191: 88-95. https://doi.org/10.1016/j.vetmic.2016.06.004
Arjyal, C., Kc, J., & Neupane, S. (2020). Prevalence of methicillin-resistant Staphylococcus aureus in shrines. International Journal of Microbiology. https://doi.org/10.1155/2020/9082903
Arumugam, G., Periasamy, H., & Maneesh, P. S. (2017). Overview of bacteriology, clinical diseases, epidemiology, antibiotic resistance, and therapeutic approach. Frontiers in Staphylococcus aureus, 5772–6733.
Beshiru, A., Igbinosa, I. H., Akinnibosun, O., & Others. (2024). Characterization of resistance and virulence factors in livestock-associated methicillin-resistant Staphylococcus aureus. Scientific Reports, 14(1), 13235. https://doi.org/10.1038/s41598-024-63963-3
Bhatta, D. R., Hamal, D., Shrestha, R., Hosuru, S., Baral, N., Singh, R. K., Nayak, N., & Gokhale, S. (2018). Bacterial contamination of frequently touched objects in a tertiary care hospital of Pokhara, Nepal: How safe are our hands? Antimicrobial Resistance and Infection Control, 7(1), 97. https://doi.org/10.1186/s13756-018-0385-2
Biswas, R., Halder, U., Kabiraj, A., Mondal, A., & Bandopadhyay, R. (2021). Overview on the role of heavy metals tolerance on developing antibiotic resistance in both Gram-negative and Gram-positive bacteria. Archives of Microbiology, 203(6), 2761–2770. https://doi.org/10.1007/s00203-021-02275-w
Bounar-Kechih, S., Hamdi, T. M., Aggad, H., Meguenni, N., & Cantekin, Z. (2018). Carriage of methicillin-resistant Staphylococcus aureus in poultry and cattle in Northern Algeria. Veterinary Medicine International, 2018, 4636121. https://doi.org/10.1155/2018/4636121
Cheng, G., Jianan, N., Saeed, A., Junhong, H., Rizwan, U., Boyu, A., Haihong, H., Dai, M., Lingli, H., X. W., & Zonghui, Y. (2019). Selection and dissemination of antimicrobial resistance in agri-food production. Antimicrobial Resistance and Infection Control, 8(158). https://doi.org/10.1186/s13756-019-0593-4
Clinical and Laboratory Standards Institute. (2021). Performance standards for antimicrobial susceptibility testing (31st ed.). CLSI Supplement M100. Wayne, PA: Clinical and Laboratory Standards Institute.
Crespo-Piazuelo, D., & Lawlor, P. G. (2021). Livestock-associated methicillin-resistant Staphylococcus aureus (LA-MRSA) prevalence in humans in close contact with animals and measures to reduce on-farm colonisation. Irish Veterinary Journal, 74(21). https://doi.org/10.1186/s13620-021-00200-7
Dong, Q., Liu, Y., Li, W., Liu, Y., & Ye, X. (2021). Cross-species transmission risk of livestock-associated MRSA: A systematic review and Bayesian meta-analysis of global data. Preventive Veterinary Medicine. https://doi.org/10.1016/j.prevetmed.2021.105429
Dweba, C. C., Zishiri, O. T., & El Zowalaty, M. E. (2018). Methicillin-resistant Staphylococcus aureus: Livestock-associated, antimicrobial, and heavy metal resistance. Infection and Drug Resistance, 11, 2497–2509. https://doi.org/10.2147/IDR.S175967
Dweba, C. C., Zishiri, O. T., & Zowalaty, M. E. (2019). Isolation and molecular identification of virulence, antimicrobial, and heavy metal resistance genes in livestock-associated methicillin-resistant Staphylococcus aureus. Pathogens, 8(2), 79. https://doi.org/10.3390/pathogens8020079
Edet, U. O., Bassey, I. U., & Joseph, A. P. (2023). Heavy metal co-resistance with antibiotics amongst bacteria isolates from an open dumpsite soil. Heliyon, 9(2). https://doi.org/10.1016/j.heliyon.2023.e13457
Fasiku, O. S., Omotosho, O. O., Ajulo, S. O., Adesanwo, E. E., Oni, O. D., Awoyele, A. A., Okunlade, O. A., & Adetunji, V. O. (2024). Occurrence and antibiotic sensitivity patterns of methicillin-resistant and methicillin-sensitive Staphylococcus aureus in pigs in Ibadan, Nigeria. Medical Sciences Forum, 24(1), 8. https://doi.org/10.3390/ECA2023-16398
Fetsch, A., Etter, D., & Johler, S. (2021). Livestock-associated methicillin-resistant Staphylococcus aureus—Current situation and impact from a One Health perspective. Current Clinical Microbiology Reports, 8, 103–113. https://doi.org/10.1007/s40588-021-00170-y
Graveland, H., Duim, B., van Duijkeren, E., Heederik, D., & Wagenaar, J. A. (2011). Livestock-associated methicillin-resistant Staphylococcus aureus in animals and humans. International Journal of Medical Microbiology, 301(8), 634. https://doi.org/10.1016/j.ijmm.2011.09.004
Grenni, P., Corno, G. (2019). Knowledge Gaps and Research Needs in Bacterial Co-Resistance in the Environment. In: Mandal, S., Paul, D. (eds) Bacterial Adaptation to Co-resistance. Springer, Singapore. https://doi.org/10.1007/978-981-13-8503-2_3Agu, A. P., Onah, C. K., Umeokonkwo, C. D., Nnabu, R. C., and Una, A. F. I. (2021). Hygiene practices in abattoir and slaughter slab, determinants and assessment of abattoir and slaughter slab facilities in Abakaliki, Ebonyi State South-East Nigeria. African Health Sciences, 21(4), 1914–1923. https://doi.org/10.4314/ahs.v21i4.50
Icgen, B., & Yilmaz, F. (2014). Co-occurrence of antibiotic and heavy metal resistance in Kızılırmak River isolates. Bulletin of Environmental Contamination and Toxicology, 93, 735–743. https://doi.org/10.1007/s00128-014-1383-6
Jardine, J., Mavumengwana, V., & Ubomba-Jaswa, E. (2019). Antibiotic resistance and heavy metal tolerance in cultured bacteria from hot springs as indicators of environmental intrinsic resistance and tolerance levels. Environmental Pollution, 249, 696–702. https://doi.org/10.1016/j.envpol.2019.03.059
Jayaweera, J. A. A. S., & Kumbukgolla, W. W. (2017). Antibiotic resistance patterns of methicillin-resistant Staphylococcus aureus (MRSA) isolated from livestock and associated farmers in Anuradhapura, Sri Lanka. Germs, 7(3), 132–139. https://doi.org/10.18683/germs.2017.1118
Kasela, M., Ossowski, M., Dzikoń, E., Ignatiuk, K., Wlazło, Ł., & Malm, A. (2023). The epidemiology of animal-associated methicillin-resistant Staphylococcus aureus. Antibiotics, 12(6), 1079. https://doi.org/10.3390/antibiotics12061079
Korish, M. A., & Attia, Y. A. (2020). Evaluation of heavy metal content in feed, litter, meat, meat products, liver, and table eggs of chickens. Animals, 10(4), 727. https://doi.org/10.3390/ani10040727
Kwaghe, A. V., Vakuru, C. T., Ndahi, M. D., Abubakar, A., Iwar, V. N., & Eze, E. (2016). Proper hygiene and effective management of livestock as a panacea for agricultural development and increase in Nigeria's gross domestic product (GDP): A review. CABI Reviews, 1–27. https://doi.org/10.1079/PAVSNNR201611024
Lim, K. T., Hanifah, Y. A., Mohd Yusof, M. Y., Ito, T., & Thong, K. L. (2013). Comparison of methicillin-resistant Staphylococcus aureus strains isolated in 2003 and 2008 with an emergence of multidrug-resistant ST22: SCCmec IV clone in a tertiary hospital, Malaysia. Journal of Microbiology, Immunology, and Infection, 46(4), 224–233. https://doi.org/10.1016/j.jmii.2013.02.001
Mamfe, L. M., Akwuobu, C. A., & Ngbede, E. O. (2021). Phenotypic detection, antimicrobial susceptibility, and virulence profile of staphylococci in the pig production setting, Makurdi, Nigeria. Access Microbiology, 3, 000293. https://doi.org/10.1099/acmi.0.000293
Mittapally, S., Taranum, R., & Parveen, S. (2018). Metal ions as antibacterial agents. Journal of Drug Delivery and Therapeutics, 8, 411–419. https://doi.org/10.22270/jddt.v8i6-s.2063
Mohamed, S. H., Elshahed, M. M. S., Saied, Y. M., Mohamed, M. S. M., & Osman, G. H. (2020). Detection of heavy metal tolerance among different MLSB resistance phenotypes of methicillin-resistant S. aureus (MRSA). Journal of Pure and Applied Microbiology, 14(3), 1905–1916. https://doi.org/10.22207/JPAM.14.3.29
Nwobi, O. C., Anyanwu, M. U., Jaja, I. F., Nwankwo, I. O., Okolo, C. C., Nwobi, C. A., Ezenduka, E. V., & Oguttu, J. W. (2023). Staphylococcus aureus in horses in Nigeria: Occurrence, antimicrobial, methicillin and heavy metal resistance and virulence potentials. Antibiotics, 12(2), 242. https://doi.org/10.3390/antibiotics12020242
Odetokun, I. A., Maurischat, S., Adetunji, V. O., & Fetsch, A. (2022). Methicillin-resistant Staphylococcus aureus from municipal abattoirs in Nigeria: Showing highly similar clones and possible transmission from slaughter animals to humans. Foodborne Pathogens and Disease, 19(1). https://doi.org/10.1089/fpd.2021.0030
Omoshaba, E., Olufemi, O., Solnibare, A., & Adebayo, A. (2020). Methicillin-resistant Staphylococcus aureus (MRSA) isolated from raw milk and nasal swabs of small ruminants in Abeokuta, Nigeria. Tropical Animal Health and Production, 52. https://doi.org/10.1007/s11250-020-02301-x
Oves, M., & Hussain, F. M. (2016). Antibiotics and heavy metal resistance emergence in water borne bacteria. Journal of Investigative Genomics, 3(2), 00045. https://doi.org/10.15406/jig.2016.03.00045
Oves, M., & Hussain, F. M. (2016). Antibiotics and heavy metal resistance emergence in water-borne bacteria. Journal of Investigative Genomics, 3(2), 00045. https://doi.org/10.15406/jig.2016.03.00045
Samutela, M. T., Kwenda, G., Simulundu, E., Nkhoma, P., Higashi, H., Frey, A., Bates, M., and Hang'ombe, B. M. (2021). Pigs as a potential source of emerging livestock associated Staphylococcus aureus in Africa: A systematic review. International Journal of Infectious Diseases, 109, 38–49. https://doi.org/10.1016/j.ijid.2021.06.023
Seiler, C., & Berendonk, T. U. (2012). Heavy metal-driven co-selection of antibiotic resistance in soil and water bodies impacted by agriculture and aquaculture. Frontiers in Microbiology, 3(399), 1–10. https://doi.org/10.3389/fmicb.2012.00399
Tchounwou, P. B., Yedjou, C. G., Patlolla, A. K., & Sutton, D. J. (2012). Heavy metal toxicity and the environment. Molecular, Clinical and Environmental Toxicology, 101, 133–164. https://doi.org/10.1007/978-3-7643-8340-4
Umair, M., Hassan, B., Farzana, R., Ali, Q., Sands, K., Mathias, J., Afegbua, S., Haque, N., Walsh, T. R., & Mohsin, M. (2023). International manufacturing and trade in colistin, its implications in polymyxin resistance and One-Health global policies: A microbiological, economic and anthropological study. The Lancet Microbe, LANMIC556. https://doi.org/10.1016/S2666-5247(22)00387-1
Wang, Y., Zhang, P., Wu, J., et al. (2023). Transmission of livestock-associated methicillin-resistant Staphylococcus aureus between animals, environment, and humans in the farm. Environmental Science and Pollution Research, 30, 86521–86539. https://doi.org/10.1007/s11356-023-28532-7
Zhang, F., Li, Y., Yang, M., & Li, W. (2012). Content of heavy metals in animal feeds and manures from farms of different scales in Northeast China. International Journal of Environmental Research and Public Health, 9(8), 2658–2668. https://doi.org/10.3390/ijerph9082658
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