Antibiotic resistance in wastewater: Occurrence and fate of Enterobacteriaceae producers of Class A and Class C β-lactamases

Journal of Environmental Science and Health - Part A Toxic/Hazardous Substances and Environmental Engineering

Volumn 50, Issue 1, 2015, Pages 26-39

  Amador, Paula P ^a   Fernandes, Ruben M ^b   Prudêncio, Maria C ^b   Barreto, Mário P ^c   Duarte, Isabel M ^a  

^a POLYTECHNIC INSTITUTE OF COIMBRA   (Portugal)

^b POLYTECHNIC INSTITUTE OF PORTO   (Portugal)

^c ETA da Boavista ^*  (Portugal)

Author keywords

AmpC; antibiotic resistant bacteria; antibiotic resistant genes; Enterobacteriaceae; environmental contaminants; ESBL; hospital wastewater; multidrug resistance; public health; WWTP

Indexed keywords

AGRICULTURE; ANTIBIOTICS; BACTERIA; EFFLUENT TREATMENT; EFFLUENTS; GENES; HEALTH RISKS; HOSPITALS; PUBLIC HEALTH; SEWAGE; SEWAGE PUMPING PLANTS; WASTEWATER TREATMENT; WATER TREATMENT PLANTS;

AMPC; ANTIBIOTIC-RESISTANT BACTERIA; ANTIBIOTIC-RESISTANT GENES; ENTEROBACTERIACEAE; ENVIRONMENTAL CONTAMINANT; ESBL; HOSPITAL WASTEWATER; MULTIDRUG RESISTANCE; WWTP;

C (PROGRAMMING LANGUAGE);

AMOXICILLIN PLUS CLAVULANIC ACID; AZTREONAM; BETA LACTAM ANTIBIOTIC; CEFOTAXIME; CEFOXITIN; CEFPIROME; CEFTAZIDIME; CHLORAMPHENICOL; GENTAMICIN; MEROPENEM; TETRACYCLINE; TRIMETHOPRIM; WATER; ANTIINFECTIVE AGENT; BETA LACTAM; BETA LACTAMASE; SEWAGE; WASTE WATER;

ARTICLE; CONTROLLED STUDY; ENTEROBACTERIACEAE; MULTIDRUG RESISTANCE; NONHUMAN; PHYSICAL CHEMISTRY; WASTE WATER MANAGEMENT; ANIMAL; ANTIBIOTIC RESISTANCE; BIOSYNTHESIS; DRUG EFFECTS; ENZYMOLOGY; GENETICS; HUMAN; ISOLATION AND PURIFICATION; MICROBIOLOGY; PORTUGAL; RIVER; SEWAGE; WASTE WATER;

ENTEROBACTERIACEAE;

ANIMALS; ANTI-BACTERIAL AGENTS; BETA-LACTAM RESISTANCE; BETA-LACTAMASES; BETA-LACTAMS; ENTEROBACTERIACEAE; HUMANS; PORTUGAL; RIVERS; SEWAGE; WASTE WATER;

EID: 84915750026     PISSN: 10934529     EISSN: 15324117     Source Type: Journal    
DOI: 10.1080/10934529.2015.964602     Document Type: Article

References (66)

1. Kim, S.; Aga, D.S. Potential ecological and human health impacts of antibiotics and antibiotic-resistant bacteria from wastewater treatment plants. J. Toxicol. Env. Health B 2007, 10, 559-573.
2. Kümmerer, K. Antibiotics in the aquatic environment-A review-Part I. Chemosphere 2009a, 75, 417-434.
3. Bouki, C.; Venieri, D.; Diamadopoulos, E. Detection and fate of antibiotic resistant bacteria in wastewater treatment plants: A review. Ecotox. Environ. Saf. 2013, 91, 1-9.
4. Chang, X.; Meyer, M.T.; Liu, X.; Zhao, Q.; Chen, H.; Chen, J.; Qiu, Z.; Yang, L.; Cao, J.; Shu, W. Determination of antibiotics in sewage from hospitals, nursery and slaughter house, wastewater treatment plant and source water in Chongqing region of Three Gorge Reservoir in China. Environ. Pollut. 2010, 158 (5), 1444-1450.
5. Korzeniewska, E.; Korzeniewska, A.; Harnisz, M. Antibiotic resistant Escherichia coli in hospital and municipal sewage and their emission to the environment. Ecotox. Environ. Safe. 2013, 91, 96-102.
6. Oubrim, N. Removal of antibiotic-resistant Salmonella in sewage water from wastewater treatment plants in Settat and Soualem, Morocco. Eur. J. Sci. Res. 2012, 68 (4), 565-573.
7. Silva, J.; Castillo, G.; Callejas, L.; López, H.; Olmos, J. Frequency of transferable multiple antibiotic resistance amongst coliform bacteria isolated from a treated sewage effluent in Antofagasta, Chile. Elect. J. Biotechnol. 2006, 9, 533-540.
8. Kümmerer, K. Antibiotics in the aquatic environment-A review-Part II. Chemosphere 2009b, 75, 435-444.
9. West, B.M.; Liggit, P.; Clemans, D.L.; Francoeur, S.N. Antibiotic resistance, gene transfer, and water quality patterns observed in waterways near CAFO farms and wastewater treatment facilities. Water Air Soil Pollut. 2010, 217, 473-489.
10. Moura, A.; Carolina Pereira, C.; Henriques, I.; Correia, A. Novel gene cassettes and integrons in antibiotic-resistant bacteria isolated from urban wastewaters. Res. Microbiol. 2011, 163, 92-100.
11. Harnisz, M. Total resistance of native bacteria as an indicator of changes in the water environment. Environ. Pollut. 2013, 174, 85-92.
12. Livermore, D.M.; Canton, R.; Gniadkowski, M.; Nordmann, P.; Rossolini, G.M.; Arlet, G.; Ayala, J.; Coque, T.M.; Kern-Zdanowicz, I.; Luzzaro, F.; Poirel, L.; Woodford, N. CTX-M: changing the face of ESBLs in Europe. J. Antimicrob. Chemother. 2007, 59, 165-174.
13. Diallo, A.A.; Brugère, H.; Kérourédan, M.; Dupouy, V.; Toutain, P.L.; Bousquet-Mélou, A.; Oswald, E.; Bibbal, D. Persistence and prevalence of pathogenic and extended-spectrum-lactamase-producing Escherichia coli in municipal wastewater treatment plant receiving slaughterhouse wastewater. Water Res. 2013, 47, 4719-4729.
14. Zarfel, G.; Galler, H.; Feierl, G.; Haas, D.; Kittingera C.; Leitner; E.; Grisold, A.J.; Mascher, F.; Posch, J.; Pertschy, B.; Marth, E.; Reinthaler, F.F. Comparison of extended-spectrum-lactamase (ESBL) carrying Escherichia coli from sewage sludge and human urinary tract infection. Environ. Pollut. 2013, 173, 192-199.
15. Bonnet, R. Growing group of extended-spectrum β-lactamases: the CTX-M enzymes. Antimicrob. Agents Chemother. 2004, 48, 1-14.
16. Pitout, J.D.; Laupland, K.B. Extended-spectrum β-lactamase-producing Enterobacteriaceae: an emerging public-health concern. Lancet Infect. Dis. 2008, 8, 159-166.
17. Dallenne, C.; Costa, A.D.; Decré, D.; Favier, C.; Arlet, G. Development of a set of multiplex PCR assays for the detection of genes encoding important-lactamases in Enterobacteriaceae. J. Antimicrob. Chemother. 2010, 59, 165-174.
18. Pitout, J.D.; Gregson, D.B.; Church, D.L.; Laupland, K.B. Population-based laboratory surveillance for AmpC β-lactamase-producing Escherichia coli, Calgary. Emerg. Infect. Dis. 2007, 13, 443-448.
19. Coque, T.M.; Baquero, F.; Canton, R. Increasing prevalence of ESBL-producing Enterobacteriaceae in Europe. Euro Surveill. 2008, 13, 1-11.
20. Corvec, S.; Crémet, L.; Leprince, C.; Dauvergne, S.; Reynaud, A.; Lepelletier, D.; Caroff, N. Epidemiology of Escherichia coli clinical isolates producing AmpC plasmidic β-lactamase during a 5-year period in a French teaching Hospital. Diagn. Microbiol. Infect. Dis. 2010, 67 (3), 277-281.
21. Carattoli, A. Animal reservoirs for extended spectrum β-lactamase producers. Clin. Microbiol. Infect. 2008, 14 (Suppl. 1), 117-123.
22. Hussain, M.; Hasan, F.; Shah, A.A.; Hameed, A.; Jung, M.; Rayamajhi, N.; Cha, S.B.; Yoo, H.S. Prevalence of class A and AmpC-lactamases in clinical Escherichia coli isolates from Pakistan Institute of Medical Science, Islamabad, Pakistan. Jpn. J. Infect. Dis. 2011, 64 (3), 249-252.
23. Bush, K.; Jacoby, G.A. Updated functional classification of β-Lactamases. Antimicrob. Agents Chemother. 2010, 54 (3), 969-976.
24. Drechsel, P.; Scott, C.A.; Raschid-Sally, L.; Redwood, M.; Bahri, A. Wastewater irrigation and health-assessing and mitigating risk in low-income countries. International Water Management Institute (IWMI), first published by Earthscan with the International Development Research Centre (IDRC) and the International Water Management Institute (IWMI) in the UK and USA in 2010, 2010.
25. Varela, A.R.; Manaia, C. Human health implications of clinically relevant bacteria in wastewater habitats. Environ. Sci. Pollut. Res. 2013, 20, 3550-3569.
26. Prüss-Üstün A.; Corvalán C. Preventing disease through healthy environments. Towards an estimate of the environmental burden of disease World Health Organization; WHO Press: Geneva, 2006; 1-104.
27. DGRN. Direcção Geral dos Recursos Naturais. Aproveitamento hidráulico do Vale do Mondego, Lisboa, 1988.
28. Pina Barreto, M. Contribuição para o estudo de eficiências e custos de tratamento com possível reutilização de águas residuais domésticas. Tese de Mestrado em Hidráulica, Recursos Hídricos e Ambiente, Universidade de Coimbra, 2005.
29. CLSI. Clinical and Laboratory Standards Institute. Performance standards for antimicrobial susceptibility testing; Twenty-First Informational Supplement. Document M100-S21, Vol. 31 (1), CLSI: Wayne, PA, 2011.
30. Krumperman, P.H. Multiple antibiotic resistance indexing of Escherichia coli to identify high-risk sources of fecal contamination of foods. Appl. Environ. Microbiol. 1983, 46, 165-170.
31. Marecos do Monte, H.; Albuquerque, A. Reutilização de águas residuais. Série Guias Técnicos-14. Eds: Entidade Reguladora dos Serviços de Aguas e Resíduos e Instituto Superior de Engenharia de Lisboa, 2010.
32. Li, D.; Yang, M.; Hu, J.; Zhang, J.; Liu, R.; Gu, X.; Zhang, Y.; Wang, Z. Antibiotic-resistance profile in environmental bacteria isolated from penicillin production wastewater treatment plant and the receiving river. Environ. Microbiol. 2009, 11, 1506-1517.
33. INFARMED. Autoridade Nacional do Medicamento e Produtos de Saúde, Lisboa, 2012.
34. Clemente, L.; Manageiro, V.; Ferreira, E.; Jones-Dias, D.; Correia, I.; Themudo, P.; Albuquerque, T.; Caniça, M. Occurrence of extended-spectrum-lactamases among isolates of Salmonella enterica subsp.enterica from food-producing animals and food products, in Portugal. Int. J. Food Microbiol. 2013, 167, 221-228.
35. EMA. European Medicines Agency. Sales of veterinary antimicrobial agents in 19 EU/EEA countries in 2010. Second ESVAC report (EMA./88728/2012), 2012.
36. Nawaz, M.; Khan, A.A.; Khan, S.; Sung, K.; Steele, R. Isolation and characterization of tetracycline-resistant Citrobacter spp. from catfish. Food Microbiol. 2008, 25, 85-91.
37. Amador, P.; Fernandes, R.; Brito, L.; Prudêncio, C. Antibiotic resistance in Enterobacteriaceae isolated from portuguese deli meats. J. Food Saf. 2011, 31 (1), 1-20.
38. Papp-Wallace, K.M.; Endimiani, A.; Taracila, M.A.; Bonomo, R.A. Carbapenems: past, present, and future. Antimicrob. Agents Chemother. 2011, 55 (11), 4943-4960.
39. DCosta, V.M.; McGram, K.M.; Hughes, D.W.; Wright, G.D. Sampling the antibiotic resistome. Science. 2006, 311, 374-377.
40. Koczura, R.; Mokracka, J.; Jabłońska, L.; Gozdecka, E.; Kubek, M.; Kaznowski, A. Antimicrobial resistance of integron-harboring Escherichia coli isolates from clinical samples, wastewater treatment plant and river water. Sci. Total Environ. 2012, 414, 680-685.
41. Thomson, K.S. Extended-Spectrum-β-Lactamase, AmpC, and carbapenemase issues. J. Clin. Microbiol. 2010, 48 (4), 1019-1025.
42. Ojer-Usoz, E.; González, D.; García-Jalón, I.; Vitas, A.I. High dissemination of extended-spectrum-lactamase-producing Enterobacteriaceae in effluents from wastewater treatment plants. Water Res. 2014, 56, 37-47.
43. Castanheira, M.; Farrell, S.E.; Deshpande, L.M.; Mendes, R.E.; Jones, R.N. Prevalence of-lactamase-encoding genes among Enterobacteriaceae bacteremia isolates collected in 26 U.S. hospitals: Report from the SENTRY Antimicrobial Surveillance Program (2010). Antimicrob. Agents Chemother. 2013, 57 (7), 3012-3020.
44. Reich, F.; Atanassova, V.; Klein, G. Extended-spectrum ß-lactamase-and AmpC-producing Enterobacteria in healthy broiler chickens, Germany. Emerg. Infect. Dis. 2013, 19 (8), 1253-1259.
45. Jong, A.; Smet, A.; Ludwig, C.; Stephan, B.; De Graef, E.; Vanrobaeys, M.; Haesebrouck, F. Antimicrobial susceptibility of Salmonella isolates from healthy pigs and chickens (2008-2011). Vet. Microbiol. 2014, 171, 298-306.
46. Sana, T.; Rami, K.; Racha, B.; Fouad, D.; Marcel, A.; Hassan, M.; Sani, H. Monzer, H. Detection of genes TEM, OXA, SHV and CTX-M in 73 clinical isolates of Escherichia coli producers of extended spectrum Beta-lactamases and determination of their susceptibility to antibiotics. Int. Arab. J. Antimicrob. Agents. 2011, 1 (1:5), doi: 10.3823/704.
47. Machado, E.; Coque, T.M.; Cantó n, R.; Baquero, F.; Sousa, J.C.; Peixe, L. The portuguese resistance study group. Dissemination in Portugal of CTX-M-15-, OXA-1-, and TEM-1-producing Enterobacteriaceae strains containing the aac(60)-Ibcr gene, which encodes an aminoglycoside-and fluoroquinolone-modifying enzyme. Antimicrob. Agents Chemother. 2006, 50 (9), 3220-3221.
48. Mendonça, N.; Louro, D.; Castro, A.P.; Diogo, J.; Caniça, M. CTX-M-15, OXA-30 and TEM-1-producing Escherichia coli in two Portuguese regions. J. Antimicrob. Chemother. 2006, 57, 1014-1016.
49. Shibl, A.M.; Al-Agamy, M.H.; Khubnani, H.; Senok, A.C.; Tawfik, A.F.; Livermore, D.M. High prevalence of acquired quinolone-resistance genes among Enterobacteriaceae from Saudi Arabia with CTX-M-15 β-lactamase. Diagn. Microbiol. Infect. Dis. 2012, 73 (4), 350-353.
50. Cerquetti, M.; Giufrè, M.; García-Fernández, A.; Accogli, M.; Fortini, D.; Luzzi, I.; Carattoli, A. Ciprofloxacin-resistant, CTX-M-15-producing Escherichia coli ST131 clone in extraintestinal infections in Italy. Clin. Microbiol. Infect. 2010, 16 (10), 1555-1558.
51. Tacão, M.; Moura, A.; Correia, A.; Henriques, I. Co-resistance to different classes of antibiotics among ESBL-producers from aquatic systems. Water Res. 2014, 48, 100-107.
52. Oteo, J.; Hernández, J.M.; Espasa, M.; Fleites, A.; Sáez, D.; Bautista, V.; Pérez-Vázquez, M.; Fernández-García, M.D.; Delgado-Iribarren, A.; Sánchez-Romero, I.; García-Picazo, L.; Miguel, M.D., Solís, S.; Aznar, E.; Trujillo, G.; Mediavilla, C.; Fontanals, D.; Rojo, S.; Vindel, A.; Campos, J. Emergence of OXA-48-producing Klebsiella pneumoniae and the novel carbapenemases OXA-244 and OXA-245 in Spain. J Antimicrob Chemother. 2013, 68, 317-321.
53. Philippon, A.; Arlet, G.; Jacoby, G.A. Plasmid-determined AmpC type β-lactamases. Antimicrob. Agents Chemother. 2002, 46, 1-11.
54. Mataseje, L.F.; Neumann, N.; Crago, B.; Baudry, P.; Zhanel, G.G.; Louie, M.; Mulvey, M.R.; ARO Water Study Group. Characterization of cefoxitin-resistant Escherichia coli isolates from recreational beaches and private drinking water in Canada between 2004 and 2006. Antimicrob. Agents Chemother. 2009, 53 (7), 3126-3130.
55. Li, Y.; Li, Q.; Du, Y.; Jiang, X.; Tan, J.; Wang, J.; Li, G.; Jiang, Y. Prevalence of plasmid-mediated AmpC beta-lactamases in a Chinese university hospital from 2003 to 2005: first report of CMY-2-Type AmpC beta-lactamase resistance in China. J. Clin. Microbiol. 2008, 46, 1317-1321.
56. Oteo, J.; Navarro, C.; Cercenado, E.; Delgado-Iribarren, A.; Wilhelmi, I.; Orden, B.; García, C.; Miguelañez, S.; Pérez-Vázquez, M.; García-Cobos, S.; Aracil, B.; Bautista, V.; Campos, J. Spread of Escherichia coli strains with high-level cefotaxime and ceftazidime resistance between the community, long-term care facilities, and hospital institutions. J. Clin. Microbiol. 2006, 44 (7), 2359-2366.
57. Jacoby, G.A. AmpC-lactamases. Clin. Microbiol. Rev. 2009, 22 (1), 161-182.
58. Galán-Sánchez, F.; Aznar-Marín, P.; Marín-Casanova, P.; Rodríguez-Iglesias, M. Diversity of bla genes and low incidence of CTX-M in plasmid-mediated AmpC-producing Escherichia coli clinical isolates. APMIS 2013, 122 (9), 796-799.
59. Mulvey, M.R.; Susky, E.; McCracken, M.; Morck, D.W.; Read, R.R. Similar cefoxitin-resistance plasmids circulating in Escherichia coli from human and animal sources. Vet. Microbiol. 2009, 134, 279-287.
60. Carmo, L.P.; Nielsen, L.R.; Costa, P.M.; Alban, L. Exposure assessment of extended-spectrum beta-lactamases/AmpC beta-lactamases-producing Escherichia coli in meat in Denmark. Infect. Ecol. Epidemiol. 2014, 4, 22924-http://dx.doi.org/10.3402/iee.v4.22924.
61. Pitout, J.D.; Gregson, D.B.; Church, D.L.; Laupland. K.B. Population-based laboratory surveillance for AmpC-lactamase-producing Escherichia coli, Calgary. Emerg. Infect. Dis. 2007, 13, 443-448.
62. Ding, H.; Yang, Y.; Lu, Q.; Wang, Y.; Chen, Y.; Deng, L.; Wang, A.; Deng, Q.; Zhang, H.; Wang, C.; Liu, L.; Xu, X.; Wang, L.; Shen, X. The prevalence of plasmid-mediated AmpC-lactamases among clinical isolates of Escherichia coli and Klebsiella pneumoniae from five children's hospitals in China. Eur. J. Clin. Microbiol. Infect. Dis. 2008, 27, 915-921.
63. Mohamudha, P.R.; Harish, B.N.; Parija, S.C. Molecular description of plasmid-mediated AmpC-lactamases among nosocomial isolates of Escherichia coli and Klebsiella pneumoniae from six different hospitals in India. J. Med. Res. 2012, 135 (1), 114-119.
64. Al-karawyi, A.M.A.; Al-Jubouri, S.A.; Alasadiy, Y.D.K. Molecular detection of AmpC family genes encoding antibiotic resistance among Escherichia coli isolated from patients with urinary tract infection (UTI) in Najaf hospitals. Kufa J. Vet. Med. Sci. 2013, 4 (1), 152-161.
65. Alvarez, M.; Tran, J.H.; Chow, N.; Jacoby G.A. Epidemiology of conjugative plasmid-mediated AmpC-lactamases in the United States. Antimicrob. Agents Chemother. 2004, 48 (2), 533-537.
66. CTX-M genogroups and association with mobile genetic elements IS Ecp1, IS 26, IS CR1, and sul1-type class 1 integrons in Escherichia coli and Klebsiella pneumoniae isolates originating from India. J. Clin. Microbiol. 2012, 50, 1779-1782.