Environmental Reservoirs of bla, qnr and mcr-1 Resistance Genes in Enterobacteriaceae from Animal and Wastewater Sources in Daloa, Côte d’Ivoire

Zébré Arthur Constant^1, , Gbogbo Moussa¹, Ouina Toualy Serge Thibaut¹, N’zi N’goran Parfait¹, Momo Sié Prince Raphaël¹, Kouassi Kra Athanase¹, Konaté Ibrahim¹, Connil Nathalie² and Kouassi Kouassi Clément¹

¹Laboratory of Agrovalorisation, Department of Biochemistry and Microbiology, Jean LOROUGNON GUEDE University, Daloa, Côte d’Ivoire

²Research Unit – Bacterial Communication and Anti-infectious Strategies (CBSA, UR4312), University of Rouen Normandy, Evreux, France

Cite this paper:
Zébré Arthur Constant, Gbogbo Moussa, Ouina Toualy Serge Thibaut, N’zi N’goran Parfait, Momo Sié Prince Raphaël, Kouassi Kra Athanase, Konaté Ibrahim, Connil Nathalie and Kouassi Kouassi Clément. Environmental Reservoirs of bla, qnr and mcr-1 Resistance Genes in Enterobacteriaceae from Animal and Wastewater Sources in Daloa, Côte d’Ivoire. American Journal of Microbiological Research. 2025; 13(5):117-123. doi: 10.12691/ajmr-13-5-3

Abstract

The environmental spread of antibiotic resistance genes is an increasing public health concern, particularly in resource-limited countries where waste management systems are often inadequate. This study aimed to identify Enterobacteriaceae in different ecosystems of Daloa city (Côte d’Ivoire) and to assess the occurrence of critical resistance genes, including bla-TEM, bla-SHV, bla-CTX-M, qnrA, qnrB, qnrS, and mcr-1. Forty samples were collected from poultry and pig feces, wastewater from gutters, and a water body receiving domestic waste. Bacteria were isolated on selective media, identified using the API 20E system, and subjected to multiplex PCR for resistance gene detection. A total of 60 isolates were recovered, primarily Escherichia coli (73.3%), followed by Salmonella spp. (13.3%), Enterobacter cloacae (8.3%), and Klebsiella oxytoca (5%). The most frequently detected genes were qnrB (30%) and bla-SHV (15%), whereas mcr-1 was not detected in any isolate. Analysis of gene distribution across environments revealed that quinolone resistance genes were generally more widespread and prevalent than β-lactam resistance genes. These findings underscore the role of environmental ecosystems in the dissemination of antibiotic resistance and highlight the urgent need to strengthen surveillance and waste management strategies.

Keywords:
Antibiotic resistance genes β-lactamases Enterobacteriaceae Environmental reservoirs Quinolones

This work is licensed under a Creative Commons Attribution 4.0 International License. To view a copy of this license, visit http://creativecommons.org/licenses/by/4.0/

Figures

References:

[1]	Omar, B. A., Alfadel, O. O., Atif H. A. and Mogahid M,. "Prevalence of TEM, SHV and CTX-M genes in Escherichia coli and Klebsiella spp urinary isolates from Sudan with confirmed ESBL phenotype", Life Science Journal, 10(2): 191-195.2013.
[2]	Effendi, M.H., Hartadi E.B., Witaningrum, A.M, Permatasari, D.A., and Ugbo E.N., "Molecular identification of blaTEM gene of extended-spectrum beta-lactamase-producing Escherichia coli from healthy pigs in Malang district, East Java, Indonesia", Journal of. Advanced Veterinary, Animal. Research, 9 (3): 447-452. 2022.
[3]	Adenaya, A., Adeniran, A.A., Ugwuoke, C. L., Saliu, K., Raji, M. A., Rakshit, A., Ribas-Ribas, M., and Könneke, M., "Environmental risk factors contributing to the spread of antibiotic resistance in west Africa", Microorganisms, 13 (951): 1-24.2025.
[4]	Nwobodo, D.N., Ugwu, M.C, Okoye, F.B.C., Oranu, C.O, Obi, I.E., and Anie, C.O., "Antibiotic resistance: The challenges and some emerging strategies for tackling a global menace", J Clin Lab Anal, 36(9): 1-10. 2022.
[5]	Poirel, L., Rodriguez-Martinez, J.M., Mammeri, H., Liard, A., and Nordmann, P., "Origin of plasmid-mediated quinolone resistance determinant QnrA", Antimicrobial agents and chemotherapy, 49 (8): 3523-3525.2005.
[6]	Guillard, T., and Cambau, E., " Une brève histoire des résistances plasmidiques aux quinolonesA brief history of the plasmid-mediated quinolone resistance determinants", Journal des Anti-infectieux, 15 (1): 1-8.2012.
[7]	Gaynes, R., and Edwards, J.R., "National nosocomial infections surveillance system. overview of nosocomial infections caused by gram-negative bacilli", Clinical Infectious Diseases, 41(6): 848-54. 2005.
[8]	Mammeri, H., Van De Loo, M., and Poirel, L., "Martinez-Martinez, L., Nordmann, P., Emergence of plasmid-mediated quinolone resistance in Escherichia coli in Europe", Antimicrob. Agents Chemother, 49: 71-76.2005.
[9]	Pishtiwan, A.H., and Khadija, K.M., "Prevalence of blaTEM, blaSHV, and blaCTX-M genes among ESBL-producing Klebsiella pneumoniae and Escherichia coli isolated from thalassemia patients in Erbil, Iraq", Mediterr J Hematol Infectious Diseases, 11(1): 1-7.2019.
[10]	Zurfuh, K., Poirel, L., Nordamann, P., Kuhnert, P., Hachler, H., and Stephan, R., "Occurrence of the plasmid-borne mcr-1 colistin resistance gene in extended spectrum Beta lactamase producing Enterobacteriaceae in river water and imported vegetable samples in Switzerland", Antimicrobial agent and chemotherapy, 60 (4): 2594-2595.2016.
[11]	Berendonk, T.U., Manaia, C.M., Merlin, C., Fatta-Kassino, D., Cytryn, E., Walsh, F., and Martinez J.L., (2015). "Tackling antibiotic resistance: The environnemental framework", Nature Reviews Microbiology, 13(5): 310-317.2015.
[12]	Zébré A. C., Attien Y., Sina H., Yao A.B., Koffi-Nevry Rose, Connil N., Konaté I., and Baba-Moussa L., "Physicochemical and microbiological characteristics of surface and groundwater frequently used by households in some districts of Daloa, Côte d'Ivoire", Journal of Advances in Microbiology, 25 (3): 1-12.2025.
[13]	Ema, F.A, Shanta, R.N, Rahman, M.Z, Islam, M.A., and Khatun, M.M., "Isolation, identification, and antibiogram studies of Escherichia coli from ready-to-eat foods in Mymensingh, Bangladesh", Vet World, 15(6): 1497-1505. 2022.
[14]	Bonkoungou, I.J.O., Nikiema, M.E.M., Garba, Z., Bako, E., Belem, S., Soma D., Diarra, F.B.J., Zoma, B.S., Gampene, M., Somda, N.S., Sore, S., and Barro N., 2025. "Detection of blaCTX-M, blaTEM, and blaSHV genes in ESBL-producing enterobacterales from poultry farms in the peri-urban area of Ouagadougou, Burkina-Faso"Journal of Microbiology and Antimicrobials, 17(1): 14-22. 2025.
[15]	Park, S.H., Byun J.H., Choi S.M., Lee D.G., Kim, S.H., Kwon J.C., Park.C., Choi J.H. and J. Yoo H.J., "Molecular epidemiology of extended-spectrum b-lactamase–producing Escherichia coli in the community and hospital in Korea: emergence of ST131 producing CTX-M-15", BMC Infect Dis, 12: 1-11. 2012.
[16]	Gundran, R.S., Cardenio, P.A., Villanueva, M.A., Sison, F.B., Benigno, C.C., Kreausukon, K., Pichpo, D., and Punyapornwithaya V., "Prevalence and distribution of blaCTX-M, blaSHV, blaTEM genes in extended- spectrum β- lactamase- producing E. coli isolates from broiler farms in the Philippines, BMC Vet Res 15(227): 1-8.2019.
[17]	Rodriguez-Martinez, J.M., Velasco, C., Pascual, A., Garcıa, I. and Martinez-Martinez, L., "Correlation of quinolone resistance levels and differences in basal and quinolone- induced expression from three qnrA-containing plasmids", Clin Microbiol Infect, 12: 440-445.2005.
[18]	Cissé, H., Kagambèga, A., Bouda, C S., Sawadogo A. and Barro N., "Phenotypic and genotypic antibiotic resistant diarrheagenic Escherichia coli isolated from patients with diarrhea in Ouagadougou, Burkina Faso", Adv.Microbiol, 13: 347-359. 2023.
[19]	Liu, Y.Y., Wang, Y., Walsh, T.R., Yi, L.X., Zhang, R. and Spencer J., "Emergence of plasmid-mediated colistin resistance mechanism mcr-1 in animals and human beings in China: a microbiological and molecular biological study", Lancet Infect Dis, 16: 161-8.2016.
[20]	Wang, H., Gao, Y., Zheng, L., Ji, L., Kong, X., Du, J., Wang, H., Duan, L., Niu, T., Liu, J., and Shang, M., "Identification and distribution of antibiotic resistance genes and antibiotic resistance bacteria in the feces treatment process: A case study in a dairy farm, China", Water, 16(11): 1-15.2024.
[21]	Leclerc, H., Mossel, D. A. A., Edberg, S. C., and Struijk, C. B., "Advances in the bacteriology of the coliform group: their suitability as markers of microbial water safety", Annual Review of Microbiology, 55(1): 201-234. 2001.
[22]	Sabença, C., Romero-Rivera, M., Barbero-Herranz, R., Sargo, R., Sousa, L., Silva, F., Lopes, F., Abrantes, A.C, Vieira-Pinto, M., Torres, C., Igrejas, G., Del Campo, R., and Poeta P., " Molecular characterization of multidrug-resistant Escherichia coli from fecal samples of wild animals", Vet Sci, 1; 11(10): 469.2024.
[23]	Blount, Z.D., "The unexhausted potential of E. coli ", Elife, 4: 1-12.2015.
[24]	Jang, J., Hur, H.G., Sadowsky, M.J., Byappanahalli, M.N., Yan, T., and Ishii S., "Environmental Escherichia coli: ecology and public health implications-a review", Journal of Applied Microbiology, 123(3): 570-581.2017.
[25]	Baker, S., Hombach, J., and Marks, F., "What have we learned from the typhoid fever surveillance in Africa program? ", Clin Infect Dis, 62 (Suppl 1): 1-3. 2016.
[26]	Matheou, A., Abousetta, A., Pascoe, A.P, Papakostopoulos, D., Charalambous, L., Panagi S., Panagiotou, S., Yiallouris, A., Filippou, C., and Johnson, E.O., "Antibiotic use in livestock farming: a driver of multidrug resistance? ", Microorganisms, 13(4): 779.2025.
[27]	Ugbo, E.N., Kotey, F.C.N., and Donkor, E.S., "Antibiotic resistance genes circulating in Nigeria: a systematic review and meta-analysis from the One Health perspective", BMC Med Genomics, 18 (1): 1-13.2025.
[28]	Shitta, G., Makanjuola, O., Adefioye, O., and Olowe, O.A., "Extended spectrum beta lactamase (ESBL), blaTEM,blaSHV and blaCTX-M, resistance genes in community and healthcare associated Gram negative bacteria from Osun State, Nigeria", Infect Disord Drug Targets, 21(4): 595-602.2021.
[29]	Gao, Y., Lu, C., Shen, D., Liu, J., Ma, Z., Yang, B., Ling, W., and Waigi, M.G., "Elimination of the risks of colistin resistance gene (mcr-1) in livestock manure during composting". Environ Int, 126: 61-68. 2019.
[30]	Anyanwu, M.U., Jaja, I.F., Okpala, C.O.R., Njoga, E.O., Okafor, N.A., and Oguttu, J.W., "Mobile Colistin Resistance (mcr) gene-containing organisms in poultry sector in low- and middle-income countries: Epidemiology, characteristics, and One Health control strategies", Antibiotics, 12(7): 1-53.2023.
[31]	Yang, D., Qiu, Z., Shen, Z., Zhao, H., Jin, M., Li, H., Liu, W., and Li, J.W., "The occurrence of the colistin resistance gene mcr-1 in the Haihe river (China) ", Int J Environ Res Public Health, 14(6): 1-10. 2017.
[32]	Cherak, Z., Loucif, L., Bendjama, E., Moussi, A., Benbouza, A., Grainat, N., and Rolain, J.M.,"Dissemination of carbapenemases and mcr-1 producing gram-negative bacteria in aquatic environments in Batna, Algeria", Antibiotics, 11(10): 1314.2022.