Quinolone resistant Aeromonas spp. as carriers and potential tracers of acquired antibiotic resistance in hospital and municipal wastewater

Science of the Total Environment

Volumn 542, Issue , 2016, Pages 665-671

  Varela, Ana Rita ^a,b   Nunes, Olga C ^b   Manaia, Célia M ^a  

^a UNIVERSIDADE CATÓLICA PORTUGUESA   (Portugal)

^b UNIVERSITY OF PORTO   (Portugal)

Author keywords

Aeromonas; Hospital effluent; Quinolone resistance

Indexed keywords

ANTIBIOTICS; EFFLUENT TREATMENT; GENES; HOSPITALS; RNA; WASTEWATER TREATMENT; WATER TREATMENT;

AEROMONAS; AEROMONAS HYDROPHILA; ANTIBIOTIC RESISTANCE; HOSPITAL EFFLUENT; MUNICIPAL WASTEWATERS; QUINOLONES; SPECIES IDENTIFICATION; URBAN WASTEWATER TREATMENT PLANTS;

EFFLUENTS;

AMOXICILLIN; CEFALOTIN; CEFTAZIDIME; CIPROFLOXACIN; COLISTIN; COTRIMOXAZOLE; GENTAMICIN; MEROPENEM; NALIDIXIC ACID; RNA 16S; STREPTOMYCIN; TETRACYCLINE; TICARCILLIN; BETA LACTAMASE; QUINOLONE DERIVATIVE; WASTE WATER;

ANTIBIOTIC RESISTANCE; BACTERIUM; EFFLUENT; HOSPITAL SECTOR; MUNICIPAL SOLID WASTE; WASTEWATER;

AAC 6 1B CR GENE; AEROMONAS; AEROMONAS ALLOSACCHAROPHILA; AEROMONAS CAVIAE; AEROMONAS HYDROPHILA; AEROMONAS SALMONICIDA; AEROMONAS VERONII; ANTIBIOTIC RESISTANCE; ANTIBIOTIC SENSITIVITY; ARTICLE; BACTERIAL GENE; BACTERIUM IDENTIFICATION; BACTERIUM ISOLATE; BLAOXA 101 GENE; BLAOXA GENE; CONTROLLED STUDY; CPN60 GENE; EFFLUENT; ESCHERICHIA COLI; GENE SEQUENCE; GENETIC VARIABILITY; GENOTYPE; GYRB GENE; HOSPITAL WASTE; NONHUMAN; NUCLEOTIDE SEQUENCE; OQXAB GENE; PHENOTYPE; PRIORITY JOURNAL; PSEUDOMONAS AERUGINOSA; QEPA GENE; QNRA GENE; QNRB GENE; QNRC GENE; QNRD GENE; QNRS GENE; QNRS2 GENE; QNRVC GENE; WASTE WATER; WASTE WATER TREATMENT PLANT; ENVIRONMENTAL MONITORING; GENETICS; HOSPITAL; MICROBIAL SENSITIVITY TEST; MICROBIOLOGY; PHYSIOLOGY;

AEROMONAS; AEROMONAS HYDROPHILA; AEROMONAS PUNCTATA; BACTERIA (MICROORGANISMS);

AEROMONAS; BETA-LACTAMASES; DRUG RESISTANCE, BACTERIAL; ENVIRONMENTAL MONITORING; GENES, BACTERIAL; HOSPITALS; MICROBIAL SENSITIVITY TESTS; QUINOLONES; WASTE WATER;

EID: 84946780842     PISSN: 00489697     EISSN: 18791026     Source Type: Journal    
DOI: 10.1016/j.scitotenv.2015.10.124     Document Type: Article

References (50)

1. Abbott S.L., Cheung W.K.W., Janda J.M. The genus Aeromonas: biochemical characteristics, atypical reactions, and phenotypic identification schemes. J. Clin. Microbiol. 2003, 41:2348-2357.
2. Berendonk T.U., Manaia C.M., Merlin C., Kassinos D.F., Cytryn E., Walsh F., Bürgmann H., Huovinen P., Stefani S., Schwartz T., Kisand V., Baquero F., Martinez J.L., Martínez J.L., Fatta-Kassinos D., Cytryn E., Walsh F., Bürgmann H., Sørum H., Norström M., Pons M.-N., Kreuzinger N., Huovinen P., Stefani S., Schwartz T., Kisand V., Baquero F., Martínez J.L., Group E.C.A.D. Tackling antibiotic resistance: the environmental framework. Nat. Rev. Microbiol. 2015, 13.
3. Bönemann G., Stiens M., Pühler A., Schlüter A. Mobilizable IncQ-related plasmid carrying a new quinolone resistance gene, qnrS2, isolated from the bacterial community of a wastewater treatment plant. Antimicrob. Agents Chemother. 2006, 50:3075-3080.
4. Cantón R., Morosini M.I. Emergence and spread of antibiotic resistance following exposure to antibiotics. FEMS Microbiol. Rev. 2011, 35:977-991.
5. Carattoli A., Bertini A., Villa L., Falbo V., Hopkins K.L., Threlfall E.J. Identification of plasmids by PCR-based replicon typing. J. Microbiol. Methods 2005, 63:219-228.
6. Cattoir V., Poirel L., Rotimi V., Soussy C.-J., Nordmann P. Multiplex PCR for detection of plasmid-mediated quinolone resistance qnr genes in ESBL-producing enterobacterial isolates. J. Antimicrob. Chemother. 2007, 60:394-397.
7. Cattoir V., Poirel L., Aubert C., Soussy C.-J., Nordmann P. Unexpected occurrence of plasmid-mediated quinolone resistance determinants in environmental Aeromonas spp. Emerg. Infect. Dis. 2008, 14:231-237.
8. Cattoir V., Poirel L., Nordmann P. Plasmid-mediated quinolone resistance pump QepA2 in an Escherichia coli isolate from France. Antimicrob. Agents Chemother. 2008, 52:3801-3804.
9. Cavaco L.M., Hasman H., Xia S., Aarestrup F.M. qnrD, a novel gene conferring transferable quinolone resistance in Salmonella enterica serovar Kentucky and Bovismorbificans strains of human origin. Antimicrob. Agents Chemother. 2009, 53:603-608.
10. Chang Y.-C., Shih D.Y.-S., Wang J.-Y., Yang S.-S. Molecular characterization of class 1 integrons and antimicrobial resistance in Aeromonas strains from foodborne outbreak-suspect samples and environmental sources in Taiwan. Diagn. Microbiol. Infect. Dis. 2007, 59:191-197.
11. Chen X., Zhang W., Pan W., Yin J., Pan Z., Gao S., Jiao X. Prevalence of qnr, aac(6')-Ib-cr, qepA, and oqxAB in Escherichia coli isolates from humans, animals, and the environment. Antimicrob. Agents Chemother. 2012, 56:3423-3427.
12. CLSI M100-S21 Performance standards for antimicrobial susceptibility testing; twenty-first informational supplement. CLSI Document M100-S21 2012, Clinical and Laboratory Standards Institute, Wayne, PA, USA.
13. Czekalski N., Gascón Díez E., Bürgmann H. Wastewater as a point source of antibiotic-resistance genes in the sediment of a freshwater lake. ISME J. 2014, 8:1381-1390.
14. Dobiasova H., Kutilova I., Piackova V., Vesely T., Cizek A., Dolejska M. Ornamental fish as a source of plasmid-mediated quinolone resistance genes and antibiotic resistance plasmids. Vet. Microbiol. 2014, 171:413-421.
15. European Centre For Disease Prevention and Control Point prevalence survey of healthcare-associated infections and antimicrobial use in European acute care hospitals. Protocol 2012, 4:3.
16. Ferreira da Silva M., Tiago I., Veríssimo A., Boaventura R.a.R., Nunes O.C., Manaia C.M. Antibiotic resistance of enterococci and related bacteria in an urban wastewater treatment plant. FEMS Microbiol. Ecol. 2007, 55:322-329.
17. Figueira V., Vaz-Moreira I., Silva M., Manaia C.M. Diversity and antibiotic resistance of Aeromonas spp. in drinking and waste water treatment plants. Water Res. 2011, 45:5599-5611.
18. Götz A., Pukall R., Smit E., Tietze E., Prager R., Tschäpe H., van Elsas J.D., Smalla K. Detection and characterization of broad-host-range plasmids in environmental bacteria by PCR. Appl. Environ. Microbiol. 1996, 62:2621-2628.
19. Henriques I., Fonseca F., Alves A., Saavedra M.J., Correia A. Occurrence and diversity of integrons and beta-lactamase genes among ampicillin-resistant isolates from estuarine waters. Res. Microbiol. 2006, 157:938-947.
20. Janda J.M., Abbott S.L. The genus Aeromonas: taxonomy, pathogenicity, and infection. Clinical Microbiology Reviews 2010, 35-73.
21. Juan C., Zamorano L., Pérez J.L., Ge Y., Oliver A. Activity of a new antipseudomonal cephalosporin, CXA-101 (FR264205), against carbapenem-resistant and multidrug-resistant Pseudomonas aeruginosa clinical strains. Antimicrob. Agents Chemother. 2010, 54:846-851.
22. Jukes T.H., Cantor C.R. Evolution of Protein Molecules. Mammalian Protein Metabolism 1969, vol. 3:21-132. Academic Press, New York. H.N. Munro (Ed.).
23. Kim O.S., Cho Y.J., Lee K., Yoon S.H., Kim M., Na H., Park S.C., Jeon Y.S., Lee J.H., Yi H., Won S., Chun J. Introducing EzTaxon-e: a prokaryotic 16s rRNA gene sequence database with phylotypes that represent uncultured species. Int. J. Syst. Evol. Microbiol. 2012, 62:716-721.
24. Kümmerer K., Henninger A. Promoting resistance by the emission of antibiotics from hospitals and households into effluent. Clin. Microbiol. Infect. Dis. 2003, 9:1203-1214.
25. Lee M.F., Peng C.F., Lin Y.H., Lin S.R., Chen Y.H. Molecular diversity of class 1 integrons in human isolates of Aeromonas spp. from southern Taiwan. Jpn. J. Infect. Dis. 2008, 61:343-349.
26. Liu B.-T., Wang X.-M., Liao X.-P., Sun J., Zhu H.-Q., Chen X.-Y., Liu Y.-H. Plasmid-mediated quinolone resistance determinants oqxAB and aac(6')-Ib-cr and extended-spectrum β-lactamase gene blaCTX-M-24 co-located on the same plasmid in one Escherichia coli strain from China. J. Antimicrob. Chemother. 2011, 66:1638-1639.
27. Marti E., Balcázar J.L. Multidrug resistance-encoding plasmid from Aeromonas sp. strain P2G1. Clin. Microbiol. Infect. 2012, 18:9-11.
28. Martinez E., Pérez J.E., Buelvas F., Tovar C., Vanegas N., Stokes H.W. Establishment and multi drug resistance evolution of ST235 Pseudomonas aeruginosa strains in the intensive care unit of a Colombian hospital. Res. Microbiol. 2014, 165:852-856.
29. Miñana-Galbis D., Urbizu-Serrano A., Farfán M., Fusté M.C., Lorén J.G. Phylogenetic analysis and identification of Aeromonas species based on sequencing of the cpn60 universal target. Int. J. Syst. Evol. Microbiol. 2009, 59:1976-1983.
30. Moura A., Oliveira C., Henriques I., Smalla K., Correia A. Broad diversity of conjugative plasmids in integron-carrying bacteria from wastewater environments. FEMS Microbiol. Lett. 2012, 330:157-164.
31. TEM and vanA as indicator genes of antibiotic resistance contamination in a hospital - urban wastewater treatment plant system. J. Glob. Antimicrob. Resist. 2014, 2:309-315.
32. Parker J.L., Shaw J.G. Aeromonas spp. clinical microbiology and disease. J. Infect. 2011, 62:109-118.
33. Périchon B., Courvalin P., Galimand M. Transferable resistance to aminoglycosides by methylation of G1405 in 16S rRNA and to hydrophilic fluoroquinolones by QepA-mediated efflux in Escherichia coli. Antimicrob. Agents Chemother. 2007, 51:2464-2469.
34. Picão R.C., Poirel L., Demarta A., Silva C.S.F., Corvaglia A.R., Petrini O., Nordmann P. Plasmid-mediated quinolone resistance in Aeromonas allosaccharophila recovered from a Swiss lake. J. Antimicrob. Chemother. 2008, 62:948-950.
35. Piotrowska M., Popowska M. The prevalence of antibiotic resistance genes among Aeromonas species in aquatic environments. Ann. Microbiol. 2014, 64:921-934.
36. Poirel L., Cattoir V., Nordmann P. Plasmid-mediated quinolone resistance; interactions between human, animal, and environmental ecologies. Front. Microbiol. 2012, 3:1-7.
37. Porto A., Ayala J., Gutkind G., Di Conza J. A novel OXA-10-like β-lactamase is present in different enterobacteriaceae. Diagn. Microbiol. Infect. Dis. 2010, 66:228-229.
38. Rizzo L., Manaia C.M., Merlin C., Schwartz T., Dagot C., Ploy M.C., Michael I., Fatta-Kassinos D. Urban wastewater treatment plants as hotspots for antibiotic resistant bacteria and genes spread into the environment: a review. Sci. Total Environ. 2013, 447:345-360.
39. Rodríguez-Martínez J.M., Cano M.E., Velasco C., Martínez-Martínez L., Pascual A. Plasmid-mediated quinolone resistance: an update. J. Infect. Chemother. 2011, 17:149-182.
40. Strahilevitz J., Jacoby G.A., Hooper D.C., Robicsek A. Plasmid-mediated quinolone resistance: a multifaceted threat. Clin. Microbiol. Rev. 2009, 22:664-689.
41. 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.
42. Tamura K., Stecher G., Peterson D., Filipski A., Kumar S. MEGA6: molecular evolutionary genetics analysis version 6.0. Mol. Biol. Evol. 2013, 30:2725-2729.
43. Varela A.R., André S., Nunes O.C., Manaia C.M. Insights into the relationship between antimicrobial residues and bacterial populations in a hospital-urban wastewater treatment plant system. Water Res. 2014, 54:327-336.
44. Varela A.R., Macedo G.N., Nunes O.C., Manaia C.M. Genetic characterization of fluoroquinolone resistant Escherichia coli from urban streams and municipal and hospital effluents. FEMS Microbiol. Ecol. 2015, 1-34.
45. Varela A.R., Manageiro V., Ferreira E., Guimarães M.A., da Costa P.M., Caniça M., Manaia C. Molecular evidence of the close relatedness of clinical, gull and wastewater isolates of quinolone-resistant Escherichia coli. J. Glob. Antimicrob. Resist. 2015.
46. Vaz-Moreira I., Nunes O.C., Manaia C.M. Bacterial diversity and antibiotic resistance in water habitats: searching the links with the human microbiome. FEMS Microbiol. Rev. 2014, 1-18.
47. Vredenburg J., Varela A.R., Hasan B., Bertilsson S., Olsen B., Narciso-da-Rocha C., Bonnedahl J., Stedt J., Da Costa P.M., Manaia C.M. Quinolone-resistant Escherichia coli isolated from birds of prey in Portugal are genetically distinct from those isolated from water environments and gulls in Portugal, Spain and Sweden. Environ. Microbiol. 2014, 16:995-1004.
48. Wang M., Guo Q., Xu X., Wang X., Ye X., Wu S., Hooper D.C., Wang M. New plasmid-mediated quinolone resistance gene, qnrC, found in a clinical isolate of Proteus mirabilis. Antimicrob. Agents Chemother. 2009, 53:1892-1897.
49. World Health Organization Antimicrobial resistance - global report on surveillance. World Heal. Organ. 2014 All 2014.
50. Yáñez M.A., Catalán V., Apráiz D., Figueras M.J., Martínez-Murcia A.J. Phylogenetic analysis of members of the genus Aeromonas based on gyrB gene sequences. Int. J. Syst. Evol. Microbiol. 2003, 53:875-883.