Acta Limnologica Brasiliensia
https://app.periodikos.com.br/journal/alb/article/doi/10.1590/S2179-975X4719
Acta Limnologica Brasiliensia
Thematic Section: Opinions about Aquatic Ecology in a Changing World

Aquatic environments in the One Health context: modulating the antimicrobial resistance phenomenon

Ambientes aquáticos no contexto One Health: modulação do fenômeno da resistência aos antimicrobianos

Juliana Alves Resende; Vânia Lúcia da Silva; Claudio Galuppo Diniz

Downloads: 0
Views: 1192

Abstract

Abstract: : From an anthropocentric perspective, aquatic environments are important to maintain health and survival, however, as they are sometimes managed based on misconception, they are considered a convergent pathway for anthropogenic residues and sanitation. Thus, it is observed that these ecosystems have been threatened by chemical pollution due to xenobiotics, especially from a more contemporary approach, by the selective pressure associated with antimicrobials. There are several studies that report the enrichment of antimicrobial resistant bacteria and mobilizable antimicrobial resistance genes in aquatic and adjacent ecosystems. From the perspective of the emerging and reemerging number of diseases related to the interplay of human, animal, and environmental factors, a new conception arose to address these issues holistically, which is known as the One Health approach. Scientific and political discourse on this conception should lead to effective action plans for preventing and controlling the spread of infectious diseases in open environment, including those impacted by anthropogenic activities. Therefore, nowadays, discussions on antimicrobial resistance are becoming broader and are requiring a multi-disciplinary view to address health and environmental challenges, which includes aquatic environment management. Water may represent one of the most important ecosystems for the in antimicrobial resistance phenomenon that arises when a dynamic and singular microbial community may be influenced by several characteristics. As antimicrobial substances do not all degrade at the same time under the same treatment, strategies concerning their removal from the environment should consider their individualized chemical characteristics.

Keywords

One Health, antimicrobial resistance genes, dissemination routes, aquatic environment, human activities

Resumo

Resumo: : Em uma perspectiva antropocêntrica, os ambientes aquáticos são importantes para manutenção da saúde e da sobrevivência, entretanto, gerenciados muitas vezes de maneiras equivocadas, são considerados uma via convergente para os resíduos gerados por atividades humanas e saneamento. Desta forma, observa-se que esses ecossistemas têm sido ameaçados pela poluição química devido a xenobióticos, sobretudo em uma abordagem mais contemporânea, pela pressão seletiva associada aos antimicrobianos. Vários estudos têm reportado o enriquecimento de bactérias resistentes aos antimicrobianos e genes mobilizáveis relacionados a esse fenômeno em ambientes aquáticos e ecossistemas adjacentes. Do ponto de vista das doenças emergentes e reemergentes relacionadas à interação de fatores humanos, animais e ambientais, surgiu uma nova concepção para abordar, em uma visão holística, essas questões, conhecidas como abordagem de saúde única (One Health). Discussões científicas e políticas nessa concepção devem levar a planos de ação eficazes para prevenir e controlar a disseminação de doenças infecciosas em ambiente aberto, incluindo aquelas afetadas por atividades antropogênicas. Portanto, hoje em dia, as discussões sobre resistência antimicrobiana estão se tornando mais amplas e exigindo uma visão multidisciplinar para enfrentar os desafios de saúde e ambientais, que incluem a gestão do ambiente aquático. A água pode ser um dos ecossistemas mais importantes no fenômeno da resistência antimicrobiana que surge quando uma comunidade microbiana dinâmica e singular pode ser influenciada por várias características. Como as substâncias antimicrobianas não são degradadas, ao mesmo tempo sob um mesmo tratamento, as estratégias relativas à sua remoção do meio ambiente devem considerar suas características químicas individuais.
 

Palavras-chave

One Health, genes de resistência a antimicrobianos, vias de disseminação, ambiente aquáticos, atividades humanas

Referências

ANDERSSON, D.I. and HUGHES, D. Microbiological effects of sublethal levels of antibiotics. Nature Reviews. Microbiology, 2014, 12(7), 465-478. http://dx.doi.org/10.1038/nrmicro3270. PMid:24861036.

ANDERSSON, D.I. and HUGHES, D. Selection and transmission of antibiotic-resistant bacteria. Microbiology Spectrum, 2017, 5(4). http://dx.doi.org/10.1128/microbiolspec.MTBP-0013-2016. PMid:28752817.

ASLAM, B., WANG, W., ARSHAD, M.I., KHURSHID, M., MUZAMMIL, S., RASOOL, M.H., NISAR, M.A., ALVI, R.F., ASLAM, M.A., QAMAR, M.U., SALAMAT, M.K.F. and BALOCH, Z. Antibiotic resistance: a run down of a global crisis. Infection and Drug Resistance, 2018, 11, 1645-1658. http://dx.doi.org/10.2147/IDR.S173867. PMid:30349322.

BAQUERO, F., MARTÍNEZ, J.L. and CANTÓN, R. Antibiotics and antibiotic resistance in water environments. Current Opinion in Biotechnology, 2008, 19(3), 260-265. http://dx.doi.org/10.1016/j.copbio.2008.05.006. PMid:18534838.

BASTOS, M.C., SANTOS, D.R., AUBERTHEAU, É., LIMA, J.A.M.C., LE GUET, T., CANER, L., MONDAMERT, L. and LABANOWSKI, J. Antibiotics and microbial resistance in brazilian soils under manure application. Land Degradation & Development, 2018, 29(8), 2472-2484. http://dx.doi.org/10.1002/ldr.2964.

BENGTSSON-PALME, J. and LARSSON, D.G.J. Antibiotic resistance genes in the environment: prioritizing risks. Nature Reviews. Microbiology, 2015, 13(6), 396. http://dx.doi.org/10.1038/nrmicro3399-c1. PMid:25915637.

BERGLUND, B. Environmental dissemination of antibiotic resistance genes andcorrelation to anthropogenic contamination with antibiotics. Infection Ecology & Epidemiology, 2015, 5(1), 28564. http://dx.doi.org/10.3402/iee.v5.28564. PMid:26356096.

BEVAN, E.R., JONES, A.M. and HAWKEY, P.M. Global epidemiology of CTX-M β-lactamases: temporal and geographical shifts in genotype. The Journal of Antimicrobial Chemotherapy, 2017, 72(8), 2145-2155. http://dx.doi.org/10.1093/jac/dkx146. PMid:28541467.

BRASIL. Ministério da Agricultura, Pecuária e Abastecimento. Sumário executivo: carnes [online]. Brasília, 2018 [viewed 7 Dec. 2018]. Available from: http://www.agricultura.gov.br/assuntos/politica-agricola/todas-publicacoes-de-politica-agricola/sumarios-executivos-de-produtos-agricolas/carnes.pdf/view

BROWN, K., UWIERA, R.R.E., KALMOKOFF, M.L., BROOKS, S.P.J. and INGLIS, G.D. Antimicrobial growth promoter use in livestock: a requirement to understand their modes of action to develop effective alternatives. International Journal of Antimicrobial Agents, 2017, 49(1), 12-24. http://dx.doi.org/10.1016/j.ijantimicag.2016.08.006. PMid:27717740.

BUENO, G.W., OSTRENSKY, A., CANZI, C., DE MATOS, F.T. and ROUBACH, R. Implementation of aquaculture parks in Federal Government waters in Brazil. Reviews in Aquaculture, 2015, 7(1), 1-12. http://dx.doi.org/10.1111/raq.12045.

CABELLO, F.C. Heavy use of prophylactic antibiotics in aquaculture: a growing problem for human and animal health and for the environment. Environmental Microbiology, 2006, 8(7), 1137-1144. http://dx.doi.org/10.1111/j.1462-2920.2006.01054.x. PMid:16817922.

CAVALLI, L.S., BRITO, K.C.T. and BRITO, B.G. One Health, One Aquaculture: aquaculture under one health umbrella. Journal of Marine Biology and Aquaculture, 2015, 1(1), 1-2. http://dx.doi.org/10.15436/2381-0750.15.005.

COLLIGNON, P. and MCEWEN, S.A. One Health: its importance in helping to better control antimicrobial resistance. Tropical Medicine and Infectious Disease, 2019, 4(1), 22. http://dx.doi.org/10.3390/tropicalmed4010022. PMid:30700019.

COLOMBO, S., ARIOLI, S., NERI, E., DELLA SCALA, G., GARGARI, G. and MORA, D. Viromes as genetic reservoir for the microbial communities in aquatic environments: a focus on antimicrobial-resistance genes. Frontiers in Microbiology, 2017, 8, 1095. http://dx.doi.org/10.3389/fmicb.2017.01095. PMid:28663745.

CONTE, D., PALMEIRO, J.K., NOGUEIRA, K. S., LIMA, T.M., CARDOSO, M.A., PONTAROLO, R., DEGAUT PONTES, F.L. and DALLA-COSTA, L.M. Characterization of CTX-M enzymes, quinolone resistance determinants, and antimicrobial residues from hospital sewage, wastewater treatment plant, and river water. Ecotoxicology and Environmental Safety, 2017, 136, 62-69. http://dx.doi.org/10.1016/j.ecoenv.2016.10.031. PMid:27816836.

D’COSTA, V.M., MCGRANN, K.M., HUGHES, D.W. and WRIGHT, G.D. Sampling the antibiotic resistome. Science, 2006, 311(5759), 374-377. http://dx.doi.org/10.1126/science.1120800. PMid:16424339.

EWERS, C., BETHE, A., SEMMLER, T., GUENTHER, S. and WIELER, L.H. Extended-spectrum beta-lactamase-producing and AmpC-producing Escherichia coli from livestock and companion animals, and their putative impact on public health: a global perspective. Clinical Microbiology and Infection, 2012, 18(7), 646-655. http://dx.doi.org/10.1111/j.1469-0691.2012.03850.x. PMid:22519858.

FINLEY, R.L., COLLIGNON, P., LARSSON, D.G., MCEWEN, S.A., LI, X.Z., GAZE, W.H., REID-SMITH, R., TIMINOUNI, M., GRAHAM, D.W. and TOPP, E. The scourge of antibiotic resistance: the important role of the environment. Clinical Infectious Diseases, 2013, 57(5), 704-710. http://dx.doi.org/10.1093/cid/cit355. PMid:23723195.

GONZALEZ RONQUILLO, M. and ANGELES HERNANDEZ, J.C. Antibiotic and synthetic growth promoters in animal diets: Review of impact and analytical methods. Food Control, 2017, 72, 255-267. http://dx.doi.org/10.1016/j.foodcont.2016.03.001.

GRAHAM, D.W., KNAPP, C.W., CHRISTENSEN, B.T., MCCLUSKEY, S. and DOLFING, J. Appearance of β-lactam resistance genes in agricultural soils and clinical isolates over the 20(th) century. Scientific Reports, 2016, 6(1), 21550. http://dx.doi.org/10.1038/srep21550. PMid:26878889.

GROS, M., RODRÍGUEZ-MOZAZ, S. and BARCELÓ, D. Fast and comprehensive multi-residue analysis of a broad range of human and veterinary pharmaceuticals and some of their metabolites in surface and treated waters by ultra-high-performance liquid chromatography coupled to quadrupole-linear ion trap tandem. Journal of Chromatography A, 2012, 1248, 104-121. http://dx.doi.org/10.1016/j.chroma.2012.05.084. PMid:22704668.

HEUER, H., SCHMITT, H. and SMALLA, K. Antibiotic resistance gene spread due to manure application on agricultural fields. Current Opinion in Microbiology, 2011, 14(3), 236-243. http://dx.doi.org/10.1016/j.mib.2011.04.009. PMid:21546307.

HEUER, O.E., KRUSE, H., GRAVE, K., COLLIGNON, P., KARUNASAGAR, I. and ÂNGULO, F.J. Human health consequences of use of antimicrobial agents in aquaculture. Clinical Infectious Diseases, 2009, 49(8), 1248-1253. http://dx.doi.org/10.1086/605667. PMid:19772389.

HOWARD, K.J., MARTIN, E., GENTRY, T., FEAGLEY, S. and KARTHIKEYAN, R. Effects of dairy manure management practices on E. coli concentration and diversity. Water, Air, and Soil Pollution, 2017, 228(1), 4. http://dx.doi.org/10.1007/s11270-016-3182-7.

HUSS, H.H., REILLY, A. and EMBAREK, P.K.B. Prevention and control of hazards in seafood. Food Control, 2000, 11(2), 149-156. http://dx.doi.org/10.1016/S0956-7135(99)00087-0.

KARKMAN, A., PÄRNÄNEN, K. and LARSSON, D.G.J. Fecal pollution can explain antibiotic resistance gene abundances in anthropogenically impacted environments. Nature Communications, 2019, 10(1), 80. http://dx.doi.org/10.1038/s41467-018-07992-3. PMid:30622259.

LIMA, L.B., OLIVEIRA, F.J.M., GIACOMINI, H.C. and LIMA‐JUNIOR, D.P. Expansion of aquaculture parks and the increasing risk of non‐native species invasions in Brazil. Reviews in Aquaculture, 2018, 10(1), 111-122. http://dx.doi.org/10.1111/raq.12150.

LOPES, R., CERDEIRA, L.T., FERNANDES, M.R., PÉREZ-CHAPARRO, P.J., MCCULLOCH, J.A. and LINCOPAN, N. Draft genome sequence of a CTX-M-15-producing endophytic Klebsiella pneumoniae ST198 isolate from commercial lettuce. Journal of Global Antimicrobial Resistance, 2017, 10, 19-20. http://dx.doi.org/10.1016/j.jgar.2017.03.005. PMid:28576742.

MAGALHÃES, M.J.T.L., PONTES, G., SERRA, P.T., BALIEIRO, A., CASTRO, D., PIERI, F.A., CRAINEY, J.L., NOGUEIRA, P.A. and ORLANDI, P.P. Multidrug resistant Pseudomonas aeruginosa survey in a stream receiving effluents from ineffective wastewater hospital plants. BMC Microbiology, 2016, 16(1), 193. http://dx.doi.org/10.1186/s12866-016-0798-0. PMid:27558582.

MANAIA, C.M., MACEDO, G., FATTA-KASSINOS, D. and NUNES, O.C. Antibiotic resistance in urban aquatic environments: can it be controlled? Applied Microbiology and Biotechnology, 2016, 100(4), 1543-1557. http://dx.doi.org/10.1007/s00253-015-7202-0. PMid:26649735.

MANYI-LOH, C., MAMPHWELI, S., MEYER, E. and OKOH, A. Antibiotic use in agriculture and its consequential resistance in environmental sources: potential public health implications. Molecules, 2018, 23(4), 795. http://dx.doi.org/10.3390/molecules23040795. PMid:29601469.

MARTI, E., VARIATZA, E. and BALCAZAR, J.L. The role of aquatic ecosystems as reservoirs of antibiotic resistance. Trends in Microbiology, 2014, 22(1), 36-41. http://dx.doi.org/10.1016/j.tim.2013.11.001. PMid:24289955.

MCALLISTER, T.A. and TOPP, E. Role of livestock in microbiological contamination of water: commonly the blame, but not always the source. Animal Frontiers, 2012, 2(2), 17-27. http://dx.doi.org/10.2527/af.2012-0039.

MUGNIER, P.D., POIREL, L., NAAS, T. and NORDMANN, P. Worldwide dissemination of the bla OXA-23 carbapenemase gene of Acinetobacter baumannii. Emerging Infectious Diseases, 2009, 16(1), 35-40. http://dx.doi.org/10.3201/eid1601.090852. PMid:20031040.

NA, G., LU, Z., GAO, H., ZHANG, L., LI, Q., LI, R., YANG, F., HUO, C. and YAO, Z. The effect of environmental factors and migration dynamics on the prevalence of antibiotic-resistant Escherichia coli in estuary environments. Scientific Reports, 2018., 8(1), 1663. PMid:29374235.

NICHOLSON, F.A., GROVES, S.J. and CHAMBERS, B.J. Pathogen survival during livestock manure storage and following land application. Bioresource Technology, 2005, 96(2), 135-143. http://dx.doi.org/10.1016/j.biortech.2004.02.030. PMid:15381209.

O’NEILL, J. Review on antimicrobial resistance: antimicrobial resistance: tackling a crisis for the health and wealth of nations. London: UK Government and the Wellcome Trust, 2014 [viewed 19 Oct. 2019]. Available from: https://amr-review.org/sites/default/files/AMR%20Review%20Paper%20-%20Tackling%20a%20crisis%20for%20the%20health%20and%20wealth%20of%20nations_1.pdf

OGAWA, V.A., SHAH, C.M., HUGHES, J.M. and KING, L.J. Prioritizing a one health approach in the immediate fight against antimicrobial resistance. EcoHealth, 2019, 16(3), 410-413. PMid:29524056.

RESENDE, J.A., SILVA, V.L., FONTES, C.O., SOUZA-FILHO, J.A., OLIVEIRA, T.L.R., COELHO, C.M., CÉSAR, D.E. and DINIZ, C.G. Multidrug-resistance and toxic metal tolerance of medically important bacteria isolated from an aquaculture system. Microbes and Environments, 2012, 27(4), 449-455. http://dx.doi.org/10.1264/jsme2.ME12049. PMid:22972388.

RESENDE, J.A., SILVA, V.L., OLIVEIRA, T.L.R., FORTUNATO, S.O., CARNEIRO, J.C., OTENIO, M.H. and DINIZ, C.G. Prevalence and persistence of potentially pathogenic and antibiotic resistant bacteria during anaerobic digestion treatment of cattle manure. Bioresource Technology, 2014, 153, 284-291. http://dx.doi.org/10.1016/j.biortech.2013.12.007. PMid:24374028.

ROUSHAM, E.K., UNICOMB, L. and ISLAM, M.A. Human, animal and environmental contributors to antibiotic resistance in low-resource settings: integrating behavioral, epidemiological and One Health approaches. BProceedings of the Royal Society B: Biological Sciences, 2018, 285(1876), 20180332. http://dx.doi.org/10.1098/rspb.2018.0332.

SANDERSON, H., BROWN, R.S., HANIA, P., MCALLISTER, T.A., MAJURY, A. and LISS, S.N. Antimicrobial resistant genes and organisms as environmental contaminants of emerging concern: addressing global public health risks. In: B. ROIG, K. WEISS and V. THIREAU, eds. Management of emerging public health issues and risks: multidisciplinary approaches to the changing environment. London: Academic Press Elsevier, 2019, pp. 147-187. http://dx.doi.org/10.1016/B978-0-12-813290-6.00007-X.

SCHAUSS, T., GLAESER, S.P., GÜTSCHOW, A., DOTT, W. and KÄMPFER, P. Improved detection of extended spectrum beta-lactamase (ESBL)-producing Escherichia coli in input and output samples of German biogas plants by a selective pre-enrichment procedure. PLoS One, 2015, 10(3), e0119791. http://dx.doi.org/10.1371/journal.pone.0119791.

SCHLEMPER, V. and SACHET, A.P. Antibiotic residues in pasteurized and unpasteurized milk marketed in southwest of Paraná, Brazil. Ciência Rural, 2017, 47(12), e20170307. http://dx.doi.org/10.1590/0103-8478cr20170307.

SELLERA, F.P., FERNANDES, M.R., MOURA, Q., CARVALHO, M.P. and LINCOPAN, N. Extended-spectrum-β-lactamase (CTX-M)-producing Escherichia coli in wild fishes from a polluted area in the Atlantic Coast of South America. Marine Pollution Bulletin, 2018, 135, 183-186. http://dx.doi.org/10.1016/j.marpolbul.2018.07.012. PMid:30301029.

TAMMINEN, M., KARKMAN, A., LOHMUS, O., MUZIASARI, W.I., TAKASU, H., WADA, S., SUZUKI, S. and VIRTA, M. Tetracycline resistance genes persist at aquaculture farms in the absence of selection pressure. Environmental Science & Technology, 2011, 45(2), 386-391. http://dx.doi.org/10.1021/es102725n. PMid:21158437.

VAN BOECKEL, T.P., BROWER, C., GILBERT, M., GRENFELL, B.T., LEVIN, S.A., ROBINSON, T.P., TEILLANT, A. and LAXMINARAYAN, R. Global trends in antimicrobial use in food animals. Proceedings of the National Academy of Sciences of the United States of America, 2015, 112(18), 5649-5654. http://dx.doi.org/10.1073/pnas.1503141112. PMid:25792457.

WEBSTER, J.P., GOWER, C.M., KNOWLES, S.C., MOLYNEUX, D.H. and FENTON, A. One Health: an ecological and evolutionary framework for tackling Neglected Zoonotic Diseases. Evolutionary Applications, 2016, 9(2), 313-333. http://dx.doi.org/10.1111/eva.12341. PMid:26834828.

ZHANG, X., ZHANG, T. and FANG, H.H.P. Antibiotic resistance genes in water environment. Applied Microbiology and Biotechnology, 2009, 82(3), 397-414. http://dx.doi.org/10.1007/s00253-008-1829-z. PMid:19130050.
 


Submetido em:
25/04/2019

Aceito em:
28/02/2020

Publicado em:
03/08/2020

5f28642b0e8825292f0e4938 alb Articles
Links & Downloads

Acta Limnol. Bras. (Online)

Share this page
Page Sections