Published
Domestic wastewater treatment plants as sources of macrolide-lincosamide-streptogramin B- and penicillin-resistant Staphylococcus aureus in Brazil
Plantas de tratamiento de aguas residuales domésticas como fuentes de Staphylococcus aureus resistente a macrólidos-lincosamida-estreptogramina B- y penicilina en Brasil
Estações de tratamento de águas residuais domésticas como fontes de Staphylococcus aureus resistente a macrolídeo-lincosamida-estreptograma e B- e penicilina no Brasil
DOI:
https://doi.org/10.15446/rcciquifa.v49n2.88854Keywords:
Antibiotic resistance, D-test, penicillin zone-edge test, quinolones, Staphylococcus aureus, water environment (en)Resistencia a antibióticos, prueba D, prueba de borde de zona de penicilina, quinolonas, Staphylococcus aureus, ambiente acuático (es)
Resistência a antibióticos, D-teste, teste da borda da zona da penicilina, quinolonas, Staphylococcus aureus, ambiente aquático (pt)
Downloads
Staphylococcus aureus is one of the main bacteria that affect human health. Its reduced susceptibility to beta-lactam antibiotics has driven the clinical use of macrolides and lincosamides. However, the presence of macrolide-lincosamide-streptogramin B (MLSB)-resistant S. aureus strains is increasingly common. Wastewater treatment plants (WWTPs) are the main anthropogenic source of resistance determinants. However, few studies have assessed the importance of this environment on the dissemination of MLSB-resistant S. aureus strains. Thus, we aimed to evaluate the impact of a domestic WWTP on the resistance to MLSB and penicillin in S. aureus in southeast Brazil. Of the 35 isolates tested, 40.6% were resistant to penicillin. Resistance to erythromycin (8.6%) and quinolones (2.8%) was less common. Despite the low rate of resistance to clindamycin (2.8%), many isolates showed reduced susceptibility to this antibiotic (57.1%). Regarding the resistance phenotypes of staphylococci isolates, inducible MLSB resistance (D-test positive) was found in two isolates. In addition, 27 S. aureus isolates showed the ability to produce penicillinase. In this article, we report for the first time the importance of WWTPs in the dissemination of MSLB resistance among S. aureus from southeast Brazil.
Staphylococcus aureus es una de las principales bacterias que afectan la salud humana. Su susceptibilidad reducida a los antibióticos betalactámicos ha impulsado el uso clínico de macrólidos y lincosamidas. Sin embargo, la presencia de cepas resistentes a macrólido-lincosamida-estreptogramina B (MLSB) de S. aureus es cada vez más común. Las plantas de tratamiento de aguas residuales (PTAR) son la principal fuente antropogénica de determinantes de resistencia. Sin embargo, pocos estudios han evaluado la importancia de este entorno en la diseminación de cepas de S. aureus resistentes a MLSB. Nuestro objetivo fue evaluar el impacto de una PTAR doméstica en MLSB y la resistencia a la penicilina en S. aureus en el sureste de Brasil. De los 35 aislamientos analizados, el 40,6% eran resistentes a la penicilina. La resistencia a la eritromicina (8,6%) y quinolonas (2,8%) fue menos común. A pesar de la baja tasa de resistencia a la clindamicina (2,8%), muchos aislamientos mostraron sensibilidad reducida a este antibiótico (57,1%). Con respecto a los fenotipos de resistencia de los aislamientos de estafilococos, la resistencia inducible a MLSB (prueba D positiva) se encontró en dos aislamientos. Además, 27 aislamientos de S. aureus mostraron la capacidad de producir penicilinasa. En este artículo informamos, por primera vez, la importancia de las PTAR en la difusión de la resistencia a MSLB entre S. aureus del sureste de Brasil.
O Staphylococcus aureus é uma das principais bactérias que afetam a saúde humana. Sua reduzida suscetibilidade aos antibióticos beta-lactâmicos tem impulsionado o uso clínico de macrolídeos e lincosamidas. No entanto, a presença de cepas de S. aureus resistentes a macrolídeo-lincosamida-estreptogramina B (MLSB) é cada vez mais comum. As estações de tratamento de esgoto (ETEs) são a principal fonte antropogênica de determinantes de resistência. No entanto, poucos estudos avaliaram a importância desse ambiente na disseminação de cepas de S. aureus resistentes ao MLSB. Assim, nosso objetivo foi avaliar o impacto de uma ETE doméstico na resistência ao MLSB e à penicilina em S. aureus no sudeste do Brasil. Dos 35 isolados testados, 40,6% eram resistentes à penicilina. Resistência à eritromicina (8,6%) e quinolonas (2,8%) foi menos comum. Apesar da baixa taxa de resistência à clindamicina (2,8%), muitos isolados apresentaram sensibilidade reduzida a esse antibiótico (57,1%). Em relação aos fenótipos de resistência dos isolados de estafilococos, a resistência induzível ao MLSB (D-teste positivo) foi encontrada em dois isolados. Além disso, 27 isolados de S. aureus mostraram a capacidade de produzir penicilinase. Neste artigo relatamos pela primeira vez a importância das ETEs na disseminação da resistência do MSLB entre S. aureus do sudeste do Brasil.
References
S.Y.C. Tong, J.S. Davis, E. Eichenberger, T.L. Holland, V.G. Fowler, Jr., Staphylococcus aureus infections: Epidemiology, pathophysiology, clinical manifestations, and management, Clin. Microbiol. Rev., 28, 603-661 (2015).
J.A. Lindsay, M.T. Holden, Staphylococcus aureus: superbug, super genome?, Trends Microbiol., 12, 378-385 (2004).
P. Moreillon, New and emerging treatment of Staphylococcus aureus infections in the hospital setting, Clin. Microbiol. Infect., 14, 32-41 (2008).
M. Abbas, M. Paul, A. Huttner, New and improved? A review of novel antibiotics for Gram-positive bacteria, Clin. Microbiol. Infect., 23, 697-703 (2017).
M. Bassetti, E.M. Trecarichi, A. Mesini, T. Spanu, D.R. Giacobbe, M. Rossi, E. Shenone, G.D. Pascale, M.P. Molinari, R. Cauda, C. Viscoli, M. Tumbarello, Risk factors and mortality of healthcare-associated and community-acquired Staphylococcus aureus bacteraemia, Clin. Microbiol. Infect., 18, 862-869 (2012).
H.W. Boucher, G.R. Corey, Epidemiology of methicillin-resistant Staphylococcus aureus, Clin. Infect. Dis., 46, 344-349 (2008).
H. Grundmann, M. Aires-de-Sousa, J. Boyce, E. Tiemersma, Emergence and resurgence of meticillin-resistant Staphylococcus aureus as a public-health threat, Lancet, 368, 874-885 (2006).
A.C. Gales, H.S. Sader, J. Ribeiro, C. Zoccoli, A. Barth, A.C. Pignatari, Antimicrobial susceptibility of gram-positive bacteria isolated in Brazilian hospitals participating in the SENTRY Program (2005-2008), Braz. J. Infect. Dis., 13, 90-98 (2009).
D.M.R. Amorim, O.C. Person, P.J. Amaral, I.I. Tanaka, Inducible resistance to clindamycin among Staphylococcus aureus isolates, O Mundo da Saúde, São Paulo, 33, 401-405 (2009).
H. Chen, M. Zhang, Occurrence and removal of antibiotic resistance genes in municipal wastewater and rural domestic sewage treatment systems in eastern China, Environ. Int., 55, 9-14 (2013).
C.A. Michael, D. Dominey-Howes, M. Labbate, The antimicrobial resistance crisis: Causes, consequences, and management, Front. Public. Health, 145, 1-8 (2014).
K.E. Shannon, D.Y. Lee, J.T. Trevors, L.A. Beaudette, Application of real-time quantitative PCR for the detection of selected bacterial pathogens during municipal wastewater treatment, Sci. Total Environ., 382, 121-9 (2007).
R.E.R. Goldstein, S.A. Micallef, S.G. Gibbs, J.A. Davis, X. He, A. George, L.M. Kleinfelter, N.A. Schreiber, S. Mukherjee, A. Sapkota, S.W. Joseph, A.R. Sapkota, Methicillin-resistant Staphylococcus aureus (MRSA) detected at four U.S. wastewater treatment plants, Environ. Health Perspect., 120, 1551-1558 (2012).
A. Naquin, J. Clement, M. Sauce, R. Grabert, M. Sherpa, R. Boopathy, Presence of antibiotic resistant Staphylococcus aureus in sewage treatment plant, J. Water Sustainabil., 4, 227-236 (2014).
E.W. Koneman, W.C. Winn-Jr, S.D. Allen, W.M. Janda, G.W. Procop, P.C. Schreckenberger, G.L. Woods, “Koneman, diagnóstico microbiológico: texto e atlas colorido”, 6th. ed., Guanabara Koogan, Rio de Janeiro, 2008.
Clinical and Laboratory Standards Institute (CLSI), “Performance Standards for Antimicrobial Disk Susceptibility Testing”, 28th ed., M02-A2, Wayne, PA, 2017.
M. Dadashi, M.J. Nasiri, F. Fallah, P. Owlia, B. Hajikhani, M. Emaneini, M. Mirpour, Methicillin-resistant Staphylococcus aureus (MRSA) in Iran: A systematic review and meta-analysis, J. Glob. Antimicrob. Resist., 12, 96-103 (2017).
S. Teeraputon, P. Santanirand, T. Wongchai, W. Songjang, N. Lapsomthob, D. Jaikrasun, S. Toonkaew, P. Tophon, Prevalence of methicillin resistance and macrolide-lincosamide-streptogramin B resistance in Staphylococcus haemolyticus among clinical strains at a tertiary-care hospital in Thailand, New Microbes New Infect., 19, 28-33 (2017).
G. Maravić, Macrolide resistance based on the Erm-mediated rRNA methylation, Curr. Drug Targets Infect. Disord., 4, 193-202 (2004).
M.C. Paiva, M.P. Ávila, M.P. Reis, P.S Costa, R.M. Nardi, A.M. Nascimento, The microbiota and abundance of the Class 1 Integron-Integrase gene in tropical sewage treatment plant influent and activated sludge, PLoS One, 10, 1-12 (2015).
P. Gómez, C. Lozano, D. Benito, V. Estepa, C. Tenorio, M. Zarazaga, C. Torres, Characterization of staphylococci in urban wastewater treatment plants in Spain, with detection of methicillin resistant Staphylococcus aureus ST398, Environ. Pollut., 212, 71-76 (2016).
S. Hess, C. Gallert, Demonstration of staphylococci with inducible macrolide-lincosamide-streptogramin B (MLSB) resistance in sewage and river water and of the capacity of anhydroerythromycin to induce MLSB, FEMS Microbiol. Ecol., 88, 48-59 (2014).
J. Li, X. Zhao, X. Tian, J. Li, J. Sjollema, A. Wang, Retention in treated wastewater affects survival and deposition of Staphylococcus aureus and Escherichia coli in sand columns, Appl. Environ. Microbiol., 81, 2199-2205 (2015).
S.M. Ben, M.S. Abbassi, P. Gómez, L. Ruiz-Ripa, S. Sghaier, C. Ibrahim, C. Torres, A. Hassen, Staphylococcus aureus isolated from wastewater treatment plants in Tunisia: occurrence of human and animal associated lineages, J. Water Health, 15, 638-643 (2017).
C. Faria, I. Vaz-Moreira, E. Serapicos, O.C. Nunes, C.M. Manaia, Antibiotic resistance in coagulase negative staphylococci isolated from wastewater and drinking water, Sci. Total Environ., 407, 3876-3882 (2009).
C.M. Luna, E. Rodriguez-Noriega, L. Bavestrello, M. Guzmán-Blanco, Gram-negative infections in adult intensive care units of Latin America and the Caribbean, Crit. Care Res. Pract., 2014, 480463 (2014).
J.M. Thompson, A. Gündoğdu, H.M. Stratton, M. Katouli, Antibiotic resistant Staphylococcus aureus in hospital wastewaters and sewage treatment plants with special reference to methicillin-resistant Staphylococcus aureus (MRSA), J. Appl. Microbiol., 114, 44-54 (2013).
M.T. Wan, C.C. Chou, Class 1 integrons and the antiseptic resistance gene (qacEΔ1) in municipal and swine slaughterhouse wastewater treatment plants and wastewater-associated methicillin-resistant Staphylococcus aureus, Int. J. Environ. Res. Public Health, 12, 6249-6260 (2015).
N. Dorival-García, A. Zafra-Gómez, F.J. Camino-Sánchez, A. Navalón, J.L. Vílchez, Analysis of quinolone antibiotic derivatives in sewage sludge samples by liquid chromatography-tandem mass spectrometry: comparison of the efficiency of three extraction techniques, Talanta, 106, 104-118 (2013).
D. Jelić, R. Antolović, From erythromycin to azithromycin and new potential ribosome-binding antimicrobials, Antibiotics (Basel), 5, 1-29 (2016).
M. Kaase, S. Lenga, S. Friedrich, F. Szabados, T. Sakinc, B. Kleine, S.G. Gatermann, Comparison of phenotypic methods for penicillinase detection in Staphylococcus aureus, Clin. Microbiol. Infect., 14, 614-616 (2008).
How to Cite
APA
ACM
ACS
ABNT
Chicago
Harvard
IEEE
MLA
Turabian
Vancouver
Download Citation
License
Copyright (c) 2020 Revista Colombiana de Ciencias Químico-Farmacéuticas
This work is licensed under a Creative Commons Attribution 4.0 International License.
The Department of Pharmacy of the Faculty of Sciences of the National University of Colombia authorizes the photocopy of articles and texts for academic or internal purposes of the institutions, citing the source. The ideas issued by the authors are the express responsibility of these and it does not necessarily reflect the views of this journal.
The entire contents of this journal, except when is identified, are subject to a Creative Commons Attribution License 4.0 adopted by Colombia. Consult the regulation: http://co.creativecommons.org/?page_id=13