Assessment of antimicrobial resistance profiles in fish farms using shared groundwater sources

Lucas Ataide de Oliveira; Marjory Lais da Costa Lima; Chuadê Cachoeira do Nascimento; Juliana Isis Araujo Pereira; Danielle de Sousa Rufino; Rafael dos Santos Rocha; Fátima Cristiane Teles de Carvalho; Taiane Maria de Oliveira; Oscarina Viana de Sousa; Rosa Helena Rebouças

doi:10.20950/1678-2305/bip.2024.51.e907

Authors

Lucas Ataide de Oliveira Universidad International Iberoamericana – Arecibo, Puerto Rico. https://orcid.org/0009-0000-4177-5644
Marjory Lais da Costa Lima Universidade Federal do Delta do Parnaíba – Parnaíba (PI), Brazil. https://orcid.org/0009-0005-7549-7394
Chuadê Cachoeira do Nascimento Universidade Federal do Delta do Parnaíba – Parnaíba (PI), Brazil. https://orcid.org/0009-0004-9112-6211
Juliana Isis Araujo Pereira Universidade Federal do Delta do Parnaíba – Parnaíba (PI), Brazil. https://orcid.org/0000-0001-8211-4463
Danielle de Sousa Rufino Universidade Federal do Delta do Parnaíba – Parnaíba (PI), Brazil. https://orcid.org/0009-0000-4462-4083
Rafael dos Santos Rocha Universidade Federal do Ceará – Fortaleza (CE), Brazil. https://orcid.org/0000-0001-9265-6311
Fátima Cristiane Teles de Carvalho Universidade Federal do Ceará – Fortaleza (CE), Brazil. https://orcid.org/0000-0001-9114-1180
Taiane Maria de Oliveira Universidade Federal do Delta do Parnaíba – Parnaíba (PI), Brazil. https://orcid.org/0000-0001-5276-0894
Oscarina Viana de Sousa Universidade Federal do Ceará – Fortaleza (CE), Brazil. https://orcid.org/0000-0003-3907-7964
Rosa Helena Rebouças Universidade Federal do Delta do Parnaíba – Parnaíba (PI), Brazil. https://orcid.org/0000-0002-5415-6575

DOI:

https://doi.org/10.20950/1678-2305/bip.2024.51.e907

Keywords:

Bacterial resistance, Fish farming, Antibiogram, Groundwater

Abstract

The indiscriminate use of antimicrobials in aquaculture is a concerning practice due to the risk of spreading drugresistant bacterial strains. This study aimed to assess the bacterial resistance profile in water sourced from a fish farming supply located in Buriti dos Lopes, Piauí, Brazil. Bacterial counts for the P1 supply point reached 6.5 log CFU/mL, while counts ranged from 3.31 to 3.66 log CFU/mL at Farm A (FA) and 2.56 to 2.79 log CFU/mL at Farm B (FB). Among the 40 strains (67.8%) tested for antimicrobial resistance, resistance was observed to quinolone (15.25%), first-generation cephalosporins (16.95%), third-generation cephalosporins (35.6%), aminopenicillin (30.51%), sulfonamide (8.47%), and carbapenem (1.7%). Similarity analysis revealed a resistance profile similarity of over 85% between isolates from P1-FA and P1-FB, suggesting the water source significantly influences the spread of resistance. Alarmingly, bacterial strains exhibiting multiple antimicrobial resistances were found in the groundwater supplying fish farms. Therefore, investigating the dissemination of phenotypic and genotypic resistance profiles is crucial to informing public policies that address the impacts of indiscriminate drug use and its environmental dissemination.

References

Adinortey, C. A., Aheto, D. W., Boateng, A. A., & Agbeko, R. (2020). Multiple antibiotic resistance-coliform bacteria in some selected fish farms of the Central Region of Ghana. Scientifica, 1-11. https://doi.org/10.1155/2020/6641461

Amarasiri, M., Sano, D., & Suzuki, S. (2020). Understanding human health risks caused by antibiotic resistant bacteria (ARB) and antibiotic resistance genes (ARG) in water environments: Current knowledge and questions to be answered. Critical Reviews in Environmental Science and Technology, 50(19), 2016-2059. https://doi.org/10.1080/10643389.2019.1692611

Amenyogbe, E., Chen, G., Wang, Z., Huang, J., Huang, B., & Li, H. (2020). The exploitation of probiotics, prebiotics and synbiotics in aquaculture: Present study, limitations and future directions. Aquaculture International, 28, 1017-1041. https://doi.org/10.1007/s10499-020-00509-0

Andrade, L., Kelly, M., Hynds, P., Weatherill, J., Majury, A., & O’Dwyer, J. (2020). Groundwater resources as a global reservoir for antimicrobial-resistant bacteria. Water Research, 170, 115360. https://doi.org/10.1016/j.watres.2019.115360

Bilal, M., Mehmood, S., Rasheed, T., & Iqbal, H. M. N. (2020). Antibiotic traces in the aquatic environment: Persistence and adverse environmental impact. Current Opinion in Environmental Science and Health, 14, 68-74. https://doi.org/10.1016/j.coesh.2019.11.005

Brito, J. M. de, Ferreira, A. H. C., Santana Júnior, H. A., Oliveira, A. P. A., Santos, C. H. L., & Oliveira, L. T. S. (2019). Desempenho zootécnico de juvenis de tilápias do Nilo (Oreochromis niloticus) alimentados com cepas probióticas e submetidas a desafio sanitário. Ciência Animal Brasileira, 20, e4964. https://doi.org/10.1590/1809-6891v20e-37348

Burridge, L., Weis, J. S., Cabello, F., Pizarro, J., & Bostick, K. (2010). Chemical use in salmon aquaculture: A review of current practices and possible environmental effects. Aquaculture, 306(1-4), 7-23. https://doi.org/10.1016/j.aquaculture.2010.05.020

Carvalho, M. F. M., Sousa, R. S., & Conceição, J. M. (2023). Expansão urbana e impactos socioambientais na paisagem em Buriti dos Lopes, Piauí, Brasil. Ciências Geográficas, 20(2), 578-588. https://agbbauru.org.br/publicacoes/revista/anoXXVII_2/agb_xxvii_2_web/agb_xxvii_2-12.pdf

Chidinma, M. M. (2024). Bacteriological evaluation of fish pond wastewater from different fish ponds in Owerri, Imo State, Nigeria. World News of Natural Sciences, 53, 223-230.

Dong, K., Pan, H., Yang, D., Rao, L., Zhao, L., Wang, Y., & Liao, X. (2020). Induction, detection, formation, and resuscitation of viable but non-culturable state microorganisms. Comprehensive Reviews in Food Science and Food Safety, 19(1), 149-183. https://doi.org/10.1111/1541-4337.12513

Eckert, E. M., Di Cesare, A., Coci, M., & Corno, G. (2018). Persistence of antibiotic resistance genes in large subalpine lakes: The role of anthropogenic pollution and ecological interactions. Hydrobiologia, 824, 93-108. https://doi.org/10.1007/s10750-017-3480-0

Eckert, E. M., Di Cesare, A., Malki, L.-S., Villiger, J., Pernthaler, J., Callieri, C., Bertoni, R., & Corno, G. (2019). Seasonality of the antibiotic resistance gene blaCTX-M in temperate Lake Maggiore. Hydrobiologia, 843, 143-153. https://doi.org/10.1007/s10750-019-04043-w

Felske, A., Akkermans, A. D. L., & De Vos, W. M. (1998). Quantification of 16S rRNAs in complex bacterial communities by multiple competitive reverse transcription-PCR in temperature gradient gel electrophoresis fingerprints. Applied and Environmental Microbiology, 64(11), 4581-4587. https://doi.org/10.1128/aem.64.11.4581-4587.1998

Gao, P., Mao, D., Luo, Y., Wang, L., Xu, B., & Xu, L. (2012). Occurrence of sulfonamide and tetracycline resistant bacteria and resistance genes in aquaculture environment. Water Research, 46(7), 2355-2364. https://doi.org/10.1016/j.watres.2012.02.004

Gastalho, S., Da Silva, G. J., Ramos, F., & De Revisão, A. (2014). Uso de antibióticos em aquacultura e resistência bacteriana: Impacto em saúde pública. Acta Farmacêutica Portuguesa, 3(1), 29-45. Retrieved from https://actafarmaceuticaportuguesa.com/index.php/afp/article/view/40/52

Gibbs, E. P. J. (2014). The evolution of One Health: A decade of progress and challenges for the future. Veterinary Record, 174(4), 85-91. https://doi.org/10.1136/vr.g143

Gomes, I. B., Maillard, J. Y., Simões, L. C., & Simões, M. (2020). Emerging contaminants affect the microbiome of water systems—Strategies for their mitigation. npj Clean Water, 3, 39. https://doi.org/10.1038/s41545-020-00086-y

Harnisz, M., Korzeniewska, E., & Gołaś, I. (2015). The impact of a freshwater fish farm on the community of tetracyclineresistant bacteria and the structure of tetracycline resistance genes in river water. Chemosphere, 128, 134-141. https://doi.org/10.1016/j.chemosphere.2015.01.035

Hossain, A., Habibullah-Al-Mamun, M., Nagano, I., Masunaga, S., Kitazawa, D., & Matsuda, H. (2022). Antibiotics, antibioticresistant bacteria, and resistance genes in aquaculture: Risks, current concern, and future thinking. Environmental Science and Pollution Research, 29(9), 11054-11075. https://doi.org/10.1007/s11356-021-17825-4

Hucheng, J., Xiaohui, C., Wenji, B., Longlong, F., Qin, Q., Liqiang, Z., & Minghua, W. (2020). Comparison of bacterial communities in channel catfish Ictalurus punctatus culture ponds of an industrial ecological purification recirculating aquaculture system. Aquaculture Research, 51(6), 2432-2442. https://doi.org/10.1111/are.14587

Instituto Brasileiro de Geografia e Estatística (IBGE) (2023). Cidades. Buriti dos Lopes. IBGE. Retrieved from https://cidades.ibge.gov.br/brasil/pi/buriti-dos-lopes/panorama

Kovalenko, K. E. (2019). Interactions among anthropogenic effects on aquatic food webs. Hydrobiologia, 841, 1-11. https://doi.org/10.1007/s10750-019-04018-x

Lima, R. M. S., Figueiredo, H. C. P., Faria, F. C. D., Picolli, R. H., Bueno Filho, J. S. D. S., & Logato, P. V. R. (2006). Resistência a antimicrobianos de bactérias oriundas de ambiente de criação e filés de tilápias do Nilo (Oreochromis niloticus). Ciência e Agrotecnologia, 30(1), 126-132. https://doi.org/10.1590/S1413-70542006000100016

Liu, X., Wang, H., & Zhao, H. (2021). Prevalence of antibiotic resistance genes in wastewater collected from ornamental fish markets in northern China. Environmental Pollution, 271, 116316. https://doi.org/10.1016/j.envpol.2020.116316

Lu, Z., Lin, W., Li, Q., Wu, Q., Ren, Z., Mu, C., Wang, C., Shi, C., & Ye, Y. (2024). Recirculating aquaculture system as microbial community and water quality management strategy in the larviculture of Scylla paramamosain. Water Research, 252, 121218. https://doi.org/10.1016/j.watres.2024.121218

Machado, A., & Bordalo, A. A. (2014). Prevalence of antibiotic resistance in bacteria isolated from drinking well water available in Guinea-Bissau (West Africa). Ecotoxicology and Environmental Safety, 106, 188-194. https://doi.org/10.1016/j.ecoenv.2014.04.037

McAleese, N., Gage, J. D. G., & Lambshead, P. J. D. (1997). BioDiversity Professional statistics analysis software. Scottish Association for Marine Science and the Natural History Museum.

Milijasevic, M., Veskovic-Moracanin, S., Milijasevic, J. B., Petrovic, J., & Nastasijevic, I. (2024). Antimicrobial resistance in aquaculture: Risk mitigation within the One Health context. Foods, 13(15), 2448. https://doi.org/10.3390/foods13152448

Novais, C., Campos, J., Freitas, A. R., Barros, M., Silveira, E., Coque, T. M., Antunes, P., & Peixe, L. (2018). Water supply and feed as sources of antimicrobial-resistant Enterococcus spp. in aquacultures of rainbow trout (Oncorhynchus mykiss), Portugal. Science of the Total Environment, 625, 1102-1112. https://doi.org/10.1016/j.scitotenv.2017.12.265

Odeyemi, A. T., Akinjogunla, O. J., Ajayi, A. O., Thomas, R. M., & Adeoye, O. O. (2023). Stream and well water samples from two rural communities in Ekiti State, Nigeria: Assessment of physicochemical parameters, bacteriological quality and public health significance. Acta Scientiarum. Biological Sciences, 45(1), e64296. https://doi.org/10.4025/actascibiolsci.v45i1.64296

Preena, P. G., Swaminathan, T. R., Kumar, V. J. R., & Singh, I. S. B. (2020). Antimicrobial resistance in aquaculture: A crisis for concern. Biologia, 75(12), 1497-1517. https://doi.org/10.2478/s11756-020-00456-4

Read, P., & Fernandes, T. (2003). Management of environmental impacts of marine aquaculture in Europe. Aquaculture, 226(1-4), 139-163. https://doi.org/10.1016/S0044-8486(03)00474-5

Silva, G. C., Rissi, L. B., & Menezes, D. B. (2014). Avaliação da qualidade dos recursos subterrâneos no município de Buriti dos Lopes-Pi. Águas Subterrâneas, 28(2), 63-74. https://aguassubterraneas.abas.org/asubterraneas/article/view/28306

Soares, J. B., Casimiro, A. R. S., & Aguiar, L. M. B. (1991). Método de coloração de Gram. In J. B. Soares, A. R. S. Casimiro & L. M. B. Albuquerque (Eds.), Microbiologia Básica. Editora da UFC.

Szekeres, E., Chiriac, C. M., Baricz, A., Szőke-Nagy, T., Lung, I., Soran, M. L., Rudi, K., Dragos, N., & Coman, C. (2018). Investigating antibiotics, antibiotic resistance genes, and microbial contaminants in groundwater in relation to the proximity of urban areas. Environmental Pollution, 236, 734-744. https://doi.org/10.1016/j.envpol.2018.01.107

Tolentino, F. M., De Almeida, I. A. Z. C., Dos Santos, C. C. M., Teixeira, I. S. D. C., Silva, S. I. D. L. E., Nogueira, M. C. L., Arroyo, M. G., Faim, W. R., De Almeida, M. T. G., & Peresi, J. T. M. (2021). Phenotypic and genotypic profile of the antimicrobial resistance of bacterial isolates and evaluation of physical and chemical potability indicators in groundwater in Brazil. International Journal of Environmental Health Research, 31(2), 186-201. https://doi.org/10.1080/09603123.2019.1640354

Vestrum, R. I., Attramadal, K. J., Winge, P., Li, K., Olsen, Y., Bones, A. M., Vadstein, O., & Bakke, I. (2018). Rearing water treatment induces microbial selection influencing the microbiota and pathogen-associated transcripts of cod (Gadus morhua) larvae. Frontiers in Microbiology, 9, 851. https://doi.org/10.3389/fmicb.2018.00851

Watts, J., Schreier, H., Lanska, L., & Hale, M. (2017). The rising tide of antimicrobial resistance in aquaculture: Sources, sinks and solutions. Marine Drugs, 15(6), 158. https://doi.org/10.3390/md15060158

Wu, D. L., Zhang, M., He, L. X., Zou, H. Y., Liu, Y. S., Li, B. B., Yang, Y. Y., Liu, C., He, L. Y., & Ying, G. G. (2020). Contamination profile of antibiotic resistance genes in groundwater in comparison with surface water. Science of the Total Environment, 715, 136975. https://doi.org/10.1016/j.scitotenv.2020.136975

Xiao, G., Cheng, X., Zhu, D., Li, Z., Feng, L., Peng, X., Lu, Z., & Xie, J. (2023). Exploring the mechanism of a novel recirculating aquaculture system based on water quality parameters and bacterial communities. Environmental Science and Pollution Research, 30(12), 34760-34774. https://doi.org/10.1007/s11356-022-24585-2

Zainab, S. M., Junaid, M., Xu, N., & Malik, R. N. (2020). Antibiotics and antibiotic resistant genes (ARGs) in groundwater: A global review on dissemination, sources, interactions, environmental and human health risks. Water Research, 187, 116455. https://doi.org/10.1016/j.watres.2020.116455

Assessment of antimicrobial resistance profiles in fish farms using shared groundwater sources

Authors

DOI:

Keywords:

Abstract

References

Downloads

Published

Issue

Section

License

Most read articles by the same author(s)

Language

Information

Make a Submission

mapa

INDEXING