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Abstract
Extended spectrum beta-lactamase (ESBL) producing Escherichia coli (E. coli) is resistant to many antibiotics, including cephalosporins and penicillin. The emergence of ESBL-E. coli poses a threat to the entire animal and human community, not just individuals with direct exposure to ruminants but also to the environment. The study evaluated the isolation rate and antimicrobial susceptibility profile of ESBL-producing E. coli from 128 ruminants in the University of Maiduguri campus. E. coli was isolated from 32 (25%) of the rectal swabs collected from cattle, goats, and sheep. ESBL-producing E. coli was more common in young animals 8(30.8%) than in adult animals 12 (11.8%). More than 80% of the isolates were resistant to all of the beta-lactam antibiotics used in the study. The study suggests that the high prevalence of ESBL-producing E. coli in ruminants may be associated with the unregulated use of beta-lactam antibiotics in veterinary practice and animal husbandry. We recommend public health awareness about the dangers of antimicrobial resistance. Also, continued monitoring of BL-E. coli prevalence in both animals and humans is crucial to track trends and guide interventions. Promoting the judicious use of antibiotics in both human and veterinary medicine is essential to reduce selective pressure for resistance development. Improved hygiene practices at farms, slaughterhouses, and food processing facilities can minimize contamination and human exposure.
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References
- Adesokan, H. K., Akanbi, I. M., Akanbi, I. O., and Obaweda, R. A. (2015). Pattern of antimicrobial usage in livestock animals in south-western Nigeria: The need for alternative plans. Onderstepoort Journal of Veterinary Research, 82(1), 1-6. Epub 2015/05/29. PubMed PMID: 26016985; PubMed Central PMCID: PMCPMC6238793. https://doi.org/10.4102/ojvr.v82i1.816.
- Akindele, A. A., Adewuyi, I. K., Adefioye, O. A., Adedokun, S. A., and Olaolu, A. O (2010) Secondary and a tertiary healthcare facility in Nigeria. American, Eurasian Journal of Scientific Research 5 (4), 230-233, 2010
- Aworh, M. K., Ekeng. E., Nilsson, P., Egyir, B., Owusu-Nyantakyi, C., and Hendriksen, R. S (2022) Extended-Spectrum ß-Lactamase-Producing Escherichia coli Among Humans, Beef Cattle, and Abattoir Environments in Nigeria. Frontiers Cell, Infection and Microbiology. 12:869314. doi: 10.3389/fcimb.2022.869314. PMID: 35463650; PMCID: PMC9021871.
- Balami, E. Y., Abdulrahman, H. I., Gashua, M. M., Galadima, H. B., and Gulani, I. A. (2018). Occurrence of Multi Drug Resistant Commensal Escherichia coli in Apparently Healthy Lambs and Kids from Maiduguri, Northeastern Nigeria. Asian Journal of Research in Animal and Veterinary Sciences, 1-10.
- Bortolaia, L. G., Bisgaard, M., Larsen, J. and Bojesen, A. M. (2010). Escherichia coli producing CTX-M-1, -2, and -9 group β-lactamases in organic chicken egg production. Antimicrobial Agents and Chemotherapy. 54(8): 3527–3528.
- Bottenfield, G. W., Burch, D. J., Hedrick, J. A., Schaten, R., Rowinski, C. A., and Davies, J. T. (1998). Safety and tolerability of a new formulation (90 mg/kg/day divided every 12 h) of amoxicillin/clavulanate (Augmentin®) in the empiric treatment of pediatric acute otitis media caused by drug-resistant Streptococcus pneumoniae. The Pediatric infectious disease journal, 17(10), 963-968.
- Chander, A., and Shrestha, C. D. (2013) Prevalence of extended spectrum beta lactamase producing Escherichia coli and Klebsiella pneumoniae urinary isolates in a tertiary care hospital in Kathmandu, Nepal. BMC Research Notes, 6:487–92.
- Chandran, A., and Mazumder, A. (2014). Occurrence of diarrheagenic virulence genes and genetic diversity in Escherichia coli isolates from fecal material of various avian hosts in British Columbia, Canada. Applied and environmental microbiology, 80(6), 1933-1940.
- Cheesbrough, M. (2005) District laboratory practice in tropical countries. Part 2, Second Edition, Cambridge University Press; 2
- Chukwu, E. E., Oladele, D. A., and Anwuru, L. A. (2021) Antimicrobial resistance awareness and antibiotic prescribing behaviour among health workers in Nigeria: a national survey. BMC infectious Disease, 21:22. Available: https://doi.org/10.1186/s12879- 020-05689-x
- Clark, C., Bozdogan, B., Peric, M. et al. (2002). In vitro selection of resistance in Haemophilus influenzae by amoxicillin/clavulanate, cefpodoxime, cefprozil, azithromycin and clarithromycin. Antimicrobial Agents and Chemotherapy 46, 2956–62.
- Cleaveland, S., Laurenson, M. K. and Taylor, L. H. (2001). –Diseases of humans and their domestic mammals: pathogen characteristics, host range and the risk of emergency. Philosophical Transaction of the royal Society, London., B, biological Sciences, 356 (1411), 991-999
- CLSI. Clinical and Laboratory Standards Institute. Performance standards for antimicrobial susceptibility testing. 26th informational supplement; M100-S22. Wayne, PA; 2016
- Coura, F. M., Lage, A. P., and Heinemann, M. B. (2014). Escherichia coli pathotypes associated with diarrhea in calves: an update. Pesquisa Veterinária Brasileira, 34, 811-818.
- Daszak, P., Cunningham, A.A. and Hyatt, A.D. (2000). – Emerging infectious diseases of wildlife: threats to biodiversity and human health. Science, 287 (5452), 443-449.
- Dhingra, S., Rahman, N. A., Peile, E., Rahman, M., Sartelli, M., Hassali, M. A., Islam, T., Islam, S., and Haque, M. (2020) Microbial Resistance Movements: An Overview of Global Public Health Threats Posed by Antimicrobial Resistance, and How Best to Counter (Frontiers in Public Health Public Health Education and Promotion) Fronters, Public Health 2020. Available: https://doi.org/10.3389/fpubh.202 0.535668
- Dipeolu, M. A. (2010) Healthy meat for wealth. 29th Inaugural Lecture, Federal University of Agriculture, Abeokuta, Nigeria.
- Egbule, O. S., and Yusuf, I. (2019). Multiple Antibiotic Resistances in Escherichia coli Isolated from Cattle and Poultry Faeces in Abraka, South-South Nigeria. Pertanika Journal of Tropical Agricultural Science, 42(2).
- Egbule, O. S., and Iweriebor B. C. (2021). Beta-Lactamase-Producing Escherichia Coli Isolates Recovered from Pig Handlers in Retail Shops and Abattoirs in Selected Localities in Southern Nigeria: Implications for Public Health. Antibiotics 10 (9), 1–10. doi: 10.3390/antibiotics10010009.
- Ejeh, F. E., Lawan, F. A., Abdulsalam, H., Mamman, P. H., and Kwanashie, C. N. (2017). Multiple antimicrobial resistance of Escherichia coli and Salmonella species isolated from broilers and local chickens retailed along the roadside in Zaria, Nigeria. Sokoto Journal of Veterinary Sciences, 15(3), 45-53.
- Ejikeugwu, C., Morteza, S., Nwakaeze, E., Eze, P., Chinedu, O., Carissa, D., Edeh, C., Esimone, C., Iroha, I., and Adikwu, M (2019) Characterization of metallo-β-lactamases-encoding genes blaIMP-1 and blaVIM-1 amongst Klebsiella pneumoniae from abattoir samples of Ebonyi state, southeastern Nigeria. Gene Reports, 16, https://doi.org/10.1016/j.genrep.2019.100428. (https://www.sciencedirect.com/science/article/pii/S2452014419300706)
- Fashae, K., Engelmann, I., Monecke, S. et al. (2021) Molecular characterisation of extended-spectrum ß-lactamase producing Escherichia coli in wild birds and cattle, Ibadan, Nigeria. BMC Veterinary Research, 17, 33. https://doi.org/10.1186/s12917-020-02734-4
- Guss, S. B (1977) Management and diseases of dairy goats. Dairy Goat Journal, 138–139.
- Igbinosa, E. O., Beshiru, A., Igbinosa, I. H., Cho G-S, and Franz C. M. A. P (2023) Multidrug-resistant extended spectrum β-lactamase (ESBL)-producing Escherichia coli from farm produce and agricultural environments in Edo State, Nigeria. PLoS ONE 18(3): e0282835. https://doi.org/10.1371/journal.pone.0282835
- Matthews, L., Cameron, C., Sheahan, A., Kolver, E., and Roche, J. (2012) Associations among dairy cow body condition and welfare-associated behavioral traits. Journal of Dairy Science. 95, 2595–2601.
- Miller, V. M. (2014). Why are sex and gender important to basic physiology and translational and individualized medicine?. American Journal of Physiology-Heart and Circulatory Physiology, 306: H781–H788
- Mueller, L., Cimen, C., Poirel, L., Descombes, M. C., and Nordmann, P. (2016) Prevalence of fosfomycin resistance among ESBL-producing Escherichia coli isolates in the community, Switzerland. European Journal of Clinical Microbiology and Infectious Diseases. 38, 945–949
- Mukherjee, M., Basu, S., Mukherjee, S. K., and Majumder, M. (2013) Multidrug-resistance and extended spectrum beta-lactamase production in uropathogenic E. coli which were isolated from hospitalized patients in Kolkata, Indian Journal of Clinical Diagnostic Research; 7:449–53. 6.
- Ogefere, H.O., Osikobia, J.G., and Omoregie, R. (2016) Prevalence of AMPC B-lactemose among Gram-negative bacteria recovered from clinical specimens in Benin city; Nigeria: Tropical Journal of Pharmaceutical Research 15(9):1947-1953. DOI: 10.4314/tjpr.v15i9.20
- Ogunleye, A. O., Okunlade, A. O., Jeminlehin, F. O., and Ajuwape, A. T. P. (2013). Antibiotic resistance in Escherichia coli isolated from healthy cattle at a major cattle market in Ibadan, Oyo State, Southwestern, Nigeria. African Journal of Microbiology Research, 7(37), 4572-4575.
- Olaitan, J. O., Shittu, O. B., and Akinliba, A. A. (2011). Antibiotic resistance of enteric bacteria isolated from duck droppings. Journal of Applied Biosciences, 45, 3008-3018.
- Onuoha, C., Stephenson-Clarke, S., Thoms-Rodriguez, C. A., and Brown, P. (2023). Mixed-species biofilms and resistance to heavy metals and disinfectants: implications for UPEC and UTIS. International Journal of Infectious Diseases, 130, S29.
- Rahimi, E., Kazemeini, H. R., Salajegheh, M (2012) Escherichia coli O157:H7/NM prevalence in raw beef, camel, sheep, goat, and water buffalo meat in Fars and Khuzestan provinces, Iran. Veterinary Research Forum; 3:13-17
- Raimondi, S., Righini, L., Candeliere, F., Musmeci, E., Bonvicini, F., Gentilomi, G., Erjavec, M.S., Amaretti, A., and Rossi, M. (2019) Antibiotic resistance, virulence factors, phenotyping, and genotyping of E. coli isolated from the feces of healthy subjects. Microorganisms, 7, 251.
- Raji, M. A. (2014) General overview of Escherichia coli infections in animals in Nigeria. Epidemiology; 4:153. DOI: 10.4172/2161-1165.1000153
- Raji, M., Ojemeh. O., and Rotimi, O (2015) Sequence analysis of genes mediating extended-spectrum beta lactamase production in isolates of enterobacteriaceae in Lagos Teaching Hospital. BioMed Central Infectious Diseases; 15:259.
- Rawat, D., and Nair, D (2010) Extended-spectrum β-lactamases in Gram Negative Bacteria. Journal of Global Infectious Diseases. 2010 Sep;2(3):263-74. doi: 10.4103/0974-777X.68531. PMID: 20927289; PMCID: PMC2946684.
- Rottier, W. C., Ammerlaan, H. S. M. and Bonten, M. J. M. (2012). Effects of confounders and intermediates on the association of bacteraemia caused by extendedspectrum β-lactamase producing Enterobacteriacea e and patient outcome: a meta-analysis, Journal of Antimicrobial Chemotherapy, 67(6): 1311–1320.
- Rural Electrification Agency (2021); Livelihood Restoration Plan (LRP) for University of Maiduguri (UNIMAID) and Teaching Hospital, Maiduguri, Borno State.
- Shaikh, S., Fatima, J., Shakil, S., Rizvi, S. M. D., and Kamal, M. A. (2015). Antibiotic resistance and extended spectrum beta-lactamases: Types, epidemiology and treatment. Saudi journal of biological sciences, 22(1), 90-101.
- Schmiedel, J., Falgenhauer, L., Domann, E., Bauerfeind, R., Prenger-Berninghoff, E., Imirzalioglu, C., and Chakraborty, T. (2014). Multi resistant extended-spectrum β-lactamase- producing Enterobacteriaceae from humans, companion animals and horses in central Hesse, Germany. BMC microbiology, 14(1), 1-13.
- Schrijver, R., Stijntjes, M., Rodríguez-Baño, J., Tacconelli, E., Babu Rajendran, N., and Voss, A. (2018) Review of antimicrobial resistance surveillance programmes in livestock and meat in EU with focus on humans. Clinical Microbiology and Infection, 24, 577–590
- World Health Organization WHO antimicrobial resistance; 2020 Home/Newsroom/Fact. sheets/Detail. Available:https:www.who int Accessed 26/07/2021.
References
Adesokan, H. K., Akanbi, I. M., Akanbi, I. O., and Obaweda, R. A. (2015). Pattern of antimicrobial usage in livestock animals in south-western Nigeria: The need for alternative plans. Onderstepoort Journal of Veterinary Research, 82(1), 1-6. Epub 2015/05/29. PubMed PMID: 26016985; PubMed Central PMCID: PMCPMC6238793. https://doi.org/10.4102/ojvr.v82i1.816.
Akindele, A. A., Adewuyi, I. K., Adefioye, O. A., Adedokun, S. A., and Olaolu, A. O (2010) Secondary and a tertiary healthcare facility in Nigeria. American, Eurasian Journal of Scientific Research 5 (4), 230-233, 2010
Aworh, M. K., Ekeng. E., Nilsson, P., Egyir, B., Owusu-Nyantakyi, C., and Hendriksen, R. S (2022) Extended-Spectrum ß-Lactamase-Producing Escherichia coli Among Humans, Beef Cattle, and Abattoir Environments in Nigeria. Frontiers Cell, Infection and Microbiology. 12:869314. doi: 10.3389/fcimb.2022.869314. PMID: 35463650; PMCID: PMC9021871.
Balami, E. Y., Abdulrahman, H. I., Gashua, M. M., Galadima, H. B., and Gulani, I. A. (2018). Occurrence of Multi Drug Resistant Commensal Escherichia coli in Apparently Healthy Lambs and Kids from Maiduguri, Northeastern Nigeria. Asian Journal of Research in Animal and Veterinary Sciences, 1-10.
Bortolaia, L. G., Bisgaard, M., Larsen, J. and Bojesen, A. M. (2010). Escherichia coli producing CTX-M-1, -2, and -9 group β-lactamases in organic chicken egg production. Antimicrobial Agents and Chemotherapy. 54(8): 3527–3528.
Bottenfield, G. W., Burch, D. J., Hedrick, J. A., Schaten, R., Rowinski, C. A., and Davies, J. T. (1998). Safety and tolerability of a new formulation (90 mg/kg/day divided every 12 h) of amoxicillin/clavulanate (Augmentin®) in the empiric treatment of pediatric acute otitis media caused by drug-resistant Streptococcus pneumoniae. The Pediatric infectious disease journal, 17(10), 963-968.
Chander, A., and Shrestha, C. D. (2013) Prevalence of extended spectrum beta lactamase producing Escherichia coli and Klebsiella pneumoniae urinary isolates in a tertiary care hospital in Kathmandu, Nepal. BMC Research Notes, 6:487–92.
Chandran, A., and Mazumder, A. (2014). Occurrence of diarrheagenic virulence genes and genetic diversity in Escherichia coli isolates from fecal material of various avian hosts in British Columbia, Canada. Applied and environmental microbiology, 80(6), 1933-1940.
Cheesbrough, M. (2005) District laboratory practice in tropical countries. Part 2, Second Edition, Cambridge University Press; 2
Chukwu, E. E., Oladele, D. A., and Anwuru, L. A. (2021) Antimicrobial resistance awareness and antibiotic prescribing behaviour among health workers in Nigeria: a national survey. BMC infectious Disease, 21:22. Available: https://doi.org/10.1186/s12879- 020-05689-x
Clark, C., Bozdogan, B., Peric, M. et al. (2002). In vitro selection of resistance in Haemophilus influenzae by amoxicillin/clavulanate, cefpodoxime, cefprozil, azithromycin and clarithromycin. Antimicrobial Agents and Chemotherapy 46, 2956–62.
Cleaveland, S., Laurenson, M. K. and Taylor, L. H. (2001). –Diseases of humans and their domestic mammals: pathogen characteristics, host range and the risk of emergency. Philosophical Transaction of the royal Society, London., B, biological Sciences, 356 (1411), 991-999
CLSI. Clinical and Laboratory Standards Institute. Performance standards for antimicrobial susceptibility testing. 26th informational supplement; M100-S22. Wayne, PA; 2016
Coura, F. M., Lage, A. P., and Heinemann, M. B. (2014). Escherichia coli pathotypes associated with diarrhea in calves: an update. Pesquisa Veterinária Brasileira, 34, 811-818.
Daszak, P., Cunningham, A.A. and Hyatt, A.D. (2000). – Emerging infectious diseases of wildlife: threats to biodiversity and human health. Science, 287 (5452), 443-449.
Dhingra, S., Rahman, N. A., Peile, E., Rahman, M., Sartelli, M., Hassali, M. A., Islam, T., Islam, S., and Haque, M. (2020) Microbial Resistance Movements: An Overview of Global Public Health Threats Posed by Antimicrobial Resistance, and How Best to Counter (Frontiers in Public Health Public Health Education and Promotion) Fronters, Public Health 2020. Available: https://doi.org/10.3389/fpubh.202 0.535668
Dipeolu, M. A. (2010) Healthy meat for wealth. 29th Inaugural Lecture, Federal University of Agriculture, Abeokuta, Nigeria.
Egbule, O. S., and Yusuf, I. (2019). Multiple Antibiotic Resistances in Escherichia coli Isolated from Cattle and Poultry Faeces in Abraka, South-South Nigeria. Pertanika Journal of Tropical Agricultural Science, 42(2).
Egbule, O. S., and Iweriebor B. C. (2021). Beta-Lactamase-Producing Escherichia Coli Isolates Recovered from Pig Handlers in Retail Shops and Abattoirs in Selected Localities in Southern Nigeria: Implications for Public Health. Antibiotics 10 (9), 1–10. doi: 10.3390/antibiotics10010009.
Ejeh, F. E., Lawan, F. A., Abdulsalam, H., Mamman, P. H., and Kwanashie, C. N. (2017). Multiple antimicrobial resistance of Escherichia coli and Salmonella species isolated from broilers and local chickens retailed along the roadside in Zaria, Nigeria. Sokoto Journal of Veterinary Sciences, 15(3), 45-53.
Ejikeugwu, C., Morteza, S., Nwakaeze, E., Eze, P., Chinedu, O., Carissa, D., Edeh, C., Esimone, C., Iroha, I., and Adikwu, M (2019) Characterization of metallo-β-lactamases-encoding genes blaIMP-1 and blaVIM-1 amongst Klebsiella pneumoniae from abattoir samples of Ebonyi state, southeastern Nigeria. Gene Reports, 16, https://doi.org/10.1016/j.genrep.2019.100428. (https://www.sciencedirect.com/science/article/pii/S2452014419300706)
Fashae, K., Engelmann, I., Monecke, S. et al. (2021) Molecular characterisation of extended-spectrum ß-lactamase producing Escherichia coli in wild birds and cattle, Ibadan, Nigeria. BMC Veterinary Research, 17, 33. https://doi.org/10.1186/s12917-020-02734-4
Guss, S. B (1977) Management and diseases of dairy goats. Dairy Goat Journal, 138–139.
Igbinosa, E. O., Beshiru, A., Igbinosa, I. H., Cho G-S, and Franz C. M. A. P (2023) Multidrug-resistant extended spectrum β-lactamase (ESBL)-producing Escherichia coli from farm produce and agricultural environments in Edo State, Nigeria. PLoS ONE 18(3): e0282835. https://doi.org/10.1371/journal.pone.0282835
Matthews, L., Cameron, C., Sheahan, A., Kolver, E., and Roche, J. (2012) Associations among dairy cow body condition and welfare-associated behavioral traits. Journal of Dairy Science. 95, 2595–2601.
Miller, V. M. (2014). Why are sex and gender important to basic physiology and translational and individualized medicine?. American Journal of Physiology-Heart and Circulatory Physiology, 306: H781–H788
Mueller, L., Cimen, C., Poirel, L., Descombes, M. C., and Nordmann, P. (2016) Prevalence of fosfomycin resistance among ESBL-producing Escherichia coli isolates in the community, Switzerland. European Journal of Clinical Microbiology and Infectious Diseases. 38, 945–949
Mukherjee, M., Basu, S., Mukherjee, S. K., and Majumder, M. (2013) Multidrug-resistance and extended spectrum beta-lactamase production in uropathogenic E. coli which were isolated from hospitalized patients in Kolkata, Indian Journal of Clinical Diagnostic Research; 7:449–53. 6.
Ogefere, H.O., Osikobia, J.G., and Omoregie, R. (2016) Prevalence of AMPC B-lactemose among Gram-negative bacteria recovered from clinical specimens in Benin city; Nigeria: Tropical Journal of Pharmaceutical Research 15(9):1947-1953. DOI: 10.4314/tjpr.v15i9.20
Ogunleye, A. O., Okunlade, A. O., Jeminlehin, F. O., and Ajuwape, A. T. P. (2013). Antibiotic resistance in Escherichia coli isolated from healthy cattle at a major cattle market in Ibadan, Oyo State, Southwestern, Nigeria. African Journal of Microbiology Research, 7(37), 4572-4575.
Olaitan, J. O., Shittu, O. B., and Akinliba, A. A. (2011). Antibiotic resistance of enteric bacteria isolated from duck droppings. Journal of Applied Biosciences, 45, 3008-3018.
Onuoha, C., Stephenson-Clarke, S., Thoms-Rodriguez, C. A., and Brown, P. (2023). Mixed-species biofilms and resistance to heavy metals and disinfectants: implications for UPEC and UTIS. International Journal of Infectious Diseases, 130, S29.
Rahimi, E., Kazemeini, H. R., Salajegheh, M (2012) Escherichia coli O157:H7/NM prevalence in raw beef, camel, sheep, goat, and water buffalo meat in Fars and Khuzestan provinces, Iran. Veterinary Research Forum; 3:13-17
Raimondi, S., Righini, L., Candeliere, F., Musmeci, E., Bonvicini, F., Gentilomi, G., Erjavec, M.S., Amaretti, A., and Rossi, M. (2019) Antibiotic resistance, virulence factors, phenotyping, and genotyping of E. coli isolated from the feces of healthy subjects. Microorganisms, 7, 251.
Raji, M. A. (2014) General overview of Escherichia coli infections in animals in Nigeria. Epidemiology; 4:153. DOI: 10.4172/2161-1165.1000153
Raji, M., Ojemeh. O., and Rotimi, O (2015) Sequence analysis of genes mediating extended-spectrum beta lactamase production in isolates of enterobacteriaceae in Lagos Teaching Hospital. BioMed Central Infectious Diseases; 15:259.
Rawat, D., and Nair, D (2010) Extended-spectrum β-lactamases in Gram Negative Bacteria. Journal of Global Infectious Diseases. 2010 Sep;2(3):263-74. doi: 10.4103/0974-777X.68531. PMID: 20927289; PMCID: PMC2946684.
Rottier, W. C., Ammerlaan, H. S. M. and Bonten, M. J. M. (2012). Effects of confounders and intermediates on the association of bacteraemia caused by extendedspectrum β-lactamase producing Enterobacteriacea e and patient outcome: a meta-analysis, Journal of Antimicrobial Chemotherapy, 67(6): 1311–1320.
Rural Electrification Agency (2021); Livelihood Restoration Plan (LRP) for University of Maiduguri (UNIMAID) and Teaching Hospital, Maiduguri, Borno State.
Shaikh, S., Fatima, J., Shakil, S., Rizvi, S. M. D., and Kamal, M. A. (2015). Antibiotic resistance and extended spectrum beta-lactamases: Types, epidemiology and treatment. Saudi journal of biological sciences, 22(1), 90-101.
Schmiedel, J., Falgenhauer, L., Domann, E., Bauerfeind, R., Prenger-Berninghoff, E., Imirzalioglu, C., and Chakraborty, T. (2014). Multi resistant extended-spectrum β-lactamase- producing Enterobacteriaceae from humans, companion animals and horses in central Hesse, Germany. BMC microbiology, 14(1), 1-13.
Schrijver, R., Stijntjes, M., Rodríguez-Baño, J., Tacconelli, E., Babu Rajendran, N., and Voss, A. (2018) Review of antimicrobial resistance surveillance programmes in livestock and meat in EU with focus on humans. Clinical Microbiology and Infection, 24, 577–590
World Health Organization WHO antimicrobial resistance; 2020 Home/Newsroom/Fact. sheets/Detail. Available:https:www.who int Accessed 26/07/2021.