High dissemination of extended-spectrum β-lactamase-producing Enterobacteriaceae ineffluents from wastewater treatment plants

Water Research

Volumn 56, Issue , 2014, Pages 37-47

  Ojer Usoz, Elena ^a   González, David ^a   García Jalón, Isabel ^a   Vitas, Ana Isabel ^a  

^a UNIVERSITY OF NAVARRA   (Spain)

Author keywords

Enterobacteriaceae; ESBL; Extended spectrum beta lactamase; Resistance; Wastewater treatment plant

Indexed keywords

AUTOMATION; EFFLUENT TREATMENT; EFFLUENTS; ESCHERICHIA COLI; RECLAMATION; RESERVOIRS (WATER); SEWAGE PUMPING PLANTS; WASTEWATER TREATMENT; WATER TREATMENT PLANTS;

ENTEROBACTERIACEAE; ESBL; EXTENDED SPECTRUM Β-LACTAMASES; EXTENDED-SPECTRUM BETA LACTAMASE; LACTAMASES; RESISTANCE; RESISTANT BACTERIA; SPECTRA'S; WASTE WATER TREATMENT PLANTS; Β-LACTAMASE;

GENES;

AGAR; ANTIINFECTIVE AGENT; BETA LACTAMASE; CEFPODOXIME; EXTENDED SPECTRUM BETA LACTAMASE; CEFTIZOXIME; WASTE WATER;

ANTIBIOTIC RESISTANCE; AUTOMATION; BACTERIUM; DISINFECTION; EFFLUENT; ENZYME ACTIVITY; HEALTH RISK; POLYMERASE CHAIN REACTION; PUBLIC HEALTH; WASTE MANAGEMENT; WASTEWATER;

ANTIBIOTIC RESISTANCE; ARTICLE; BACTERIAL GENE; BACTERIUM ISOLATION; EFFLUENT; ENTEROBACTERIACEAE; ESCHERICHIA COLI; EXTENDED SPECTRUM BETA LACTAMASE PRODUCING ENTEROBACTERIACEAE; NONHUMAN; POLYMERASE CHAIN REACTION; PREVALENCE; PRIORITY JOURNAL; RESERVOIR; SPECIES IDENTIFICATION; WASTE WATER; WASTE WATER TREATMENT PLANT; ANALOGS AND DERIVATIVES; DRUG EFFECTS; ENVIRONMENTAL MONITORING; ENZYMOLOGY; GENETICS; ISOLATION AND PURIFICATION; METABOLISM; MICROBIOLOGY; SPAIN; WASTE DISPOSAL FACILITY;

NAVARRA; SPAIN;

BETA-LACTAMASES; CEFTIZOXIME; DRUG RESISTANCE, BACTERIAL; ENTEROBACTERIACEAE; ENVIRONMENTAL MONITORING; SPAIN; WASTE DISPOSAL FACILITIES; WASTE WATER; WATER MICROBIOLOGY;

EID: 84896118446     PISSN: 00431354     EISSN: 18792448     Source Type: Journal    
DOI: 10.1016/j.watres.2014.02.041     Document Type: Article

References (75)

1. Akiyama T., Savin M.C. Populations of antibiotic-resistant coliform bacteria change rapidly in a wastewater effluent dominated stream. Sci. Total Environ. 2010, 408(24):6192-6201.
2. Alcaide E., Garay E. R-plasmid transfer in Salmonella spp. isolated from wastewater and sewage-contaminated surface waters. Appl. Environ. Microbiol. 1984, 48(2):435-438.
3. Allen H.K., Donato J., Wang H.H., Cloud-Hansen K.A., Davies J., Handelsman J. Call of the wild: antibiotic resistance genes in natural environments. Nat. Rev. Micro 2010, 8(4):251-259.
4. Amaya E., Reyes D., Paniagua M., Calderón S., Rashid M.U., Colque P., Kühn I., Möllby R., Weintraub A., Nord C.E. Antibiotic resistance patterns of Escherichia coli isolates from different aquatic environmental sources in León, Nicaragua. Clin. Microbiol. Infect. 2012, 18(9):E347-E354.
5. Andersen S.R., Sandaa R.A. Distribution of tetracycline resistance among gram-negative bacteria isolated from polluted and impollutes marine sediments. Appl. Environ. Microbiol. 1994, 60(3):908-912.
6. Armstrong J.L., Calomiris J.J., Seidler R.J. Selection of antibiotic-resistant standard plate count bacteria during water treatment. Appl. Environ. Microbiol. 1982, 44:308-316.
7. Baquero F., Martínez J.L., Cantón R. Antibiotics and antibiotic resistance in water environments. Curr. Opin. Biotech. 2008, 19:260-265.
8. Blaak H., van Hoek A., Veenman C., van Leeuwen A., Lynch G., van Overbeek W., de Roda Husman A.M. Extended spectrum ß-lactamase- and constitutively AmpC-producing Enterobacteriaceae on fresh produce and in the agricultural environment. Intl J. Food Microbiol. 2014, 168-169:8-16.
9. Bonnet R. Growing group of extended-spectrum beta-lactamases: the CTX-M enzymes. Antimicrob. Agents Chemother. 2004, 48(1):1-14.
10. Cantón R., Coque T.M. The CTX-M β-lactamase pandemic. Curr. Opin. Biotech. 2006, 9(5):466-475.
11. 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.
12. Clinical and Laboratory Standards Institute (CLSI) Performance Standards for Antimicrobial. Susceptibility Testing; Twenty-second Informational Supplement 2012, vol. 32(3). Document M100-S22, CLSI, Wayne, USA.
13. Cogliani C., Goossens H., Greko C. Restricting antimicrobial use in food animals: lessons from Europe. Microbe 2011, 6(6):274-279.
14. Colom K., Perez J., Alonso R., Fernandez-Aranguiz A., Larino E., Cisterna R. Simple and reliable multiplex PCR assay for detection of blaTEM, blaSHV and blaOXA 1 genes in Enterobacteriaceae. FEMS Microbiol. Lett. 2003, 223:147-151.
15. Costa D., Poeta P., Sáenz Y., Vinué L., Rojo-Bezares B., Jouini A., Zarazaga M., Rodrigues J., Torres C. Detection of Escherichia coli harbouring extended-spectrum b-lactamases of the CTX-M, TEM and SHV classes in faecal samples of wild animals in Portugal. J. Antimicrob. Chemother. 2006, 58(6):1311-1312.
16. Damoa-Siakwan S. Extended-spectrum beta lactamases: an overview. J. Infect. Prev. 2005, 6:25-28.
17. Derbyshire H., Kay G., Evans K., Vaughan C., Kavuri U., Winstanley T. A simple disc diffusion method for detecting AmpC and extended spectrum b-lactamases in clinical isolates of Enterobacteriaceae. J. Antimicrob. Chemother. 2009, 63:497-501.
18. Doi Y., Paterson D.L. Detection of plasmid-mediated class C b-lactamases. Int. J. Infect. Dis. 2007, 11:191-197.
19. Dolejska M. CTX-M-15-producing Escherichia coli clone B2-O25b-ST131 and Klebsiella spp. isolates in municipal wastewater treatment plant effluents. J. Antimicrob. Chemother. 2011, 66(12):2784-2790.
20. Food and Drug Administration (FDA) Cephalosporin Rule 2012, FDA-2008-N-0326.
21. Gniadkowski M. Evolution of extended-spectrum b-lactamases by mutation. Clin. Microbiol. Infect. 2008, 14(Suppl. 1):11-32.
22. Gómez M., Díaz M.T., Araujo M., Sueiro R., Garrido J. Waste water treatment plants as redistributors of resistance genes in bacteria. Water Pollut. X 2010, 135:83-94.
23. Hernández J.R., Martínez-Martínez L., Cantón R., Coque T.M., Pascual A. Nationwide study of Escherichia coli and Klebsiella pneumoniae producing extended-spectrum beta-lactamases in Spain. Antimicrob. Agents Chemother. 2005, 49(5):2122-2125.
24. Hu Y.Y., Cai J.C., Zhou H.W., Chi D., Zhang X.F., Chen W.L., Zhang R., Chen G.X. Molecular typing of CTX-M-producing Escherichia coli isolates from environmental water, swine feces, specimens from healthy humans, and human patients. Appl. Environ. Microbiol. 2013, 79(19):5988-5996.
25. Huang J.J., Hu H.Y., Tang F., Li Y., Lu S.Q., Lu Y. Inactivation and reactivation of antibiotic-resistant bacteria by chlorination in secondary effluents of a municipal wastewater treatment plant. Water Res. 2011, 45(9):2775-2781.
26. Isozumi R., Yoshimatsu K., Yamashiro T., Hasebe F., Nguyen B., Ngo T.C., Yasuda S.P., Koma T., Shimizu K., Arikawa J. blaNDM-1-positive Klebsiella pneumoniae from environment, Vietnam. Emerg. Infect. Dis. 2012, 18(8):1383-1384.
27. Jarlier V., Philippon A., Nicolas M.H., Bismuth R., Paul G., Fusciardi J. Enterobacter cloacae. Invivo emergence of a variant resistant to new beta-lactams during treatment with lamoxactam-gentamicin. Pathol. Biol. (Paris) 1984, 32:399-403.
28. Jarlier V., Nicolas M.H., Fournier G., Philippon A. Extended broad-spectrum beta lactamases conferring transferable resistance to newer beta-lactam agents in Enterobacteriaceae: hospital prevalence and susceptibility patterns. Rev. Infect. Dis. 1988, 10(4):867-878.
29. Jorgensen J.H., McElmeel M.L., Fulcher L.C., Zimmer B.L. Detection of CTX-M-type extended-spectrum beta-lactamase (ESBLs) by testing with MicroScan overnight and ESBL confirmation panels. J. Clin. Microbiol. 2010, 48(1):120-123.
30. Koh T.H., Cao D.Y.H., Chan K.S., Wijaya L., Low S.B.G., Lam M.S., Ooi E.E., Hsu L.Y. blaOXA-181-positive Klebsiella pneumoniae, Singapore. Emerg. Infect. Dis. 2012, 18(9):1524-1525.
31. Komatsu M., Aihara M., Shimakawa K., Iwasaki M., Nagasaka Y., Fukuda S., Matsuo S., Iwatani Y. Evaluation of MicroScan ESBL confirmation panel for Enterobacteriaceae-producing, extended-spectrum beta-lactamases isolated in Japan. Diagn. Microbiol. Infect. Dis. 2003, 46(2):125-130.
32. Korzeniewska E., Harnisz M. Extended-spectrum beta-lactamase (ESBL)-positive Enterobacteriaceae in municipal sewage and their emission to the environment. J. Environ. Manage. 2013, 128:904-911.
33. Levy S.B., Marshall B. Antibacterial resistance worldwide: causes, challenges and responses. Nat. Med. 2004, 10(12 Suppl.):S122-S129.
34. Lezameta L. Comparación de cuatro métodos fenotípicos para la detección de beta-lactamasas de espectro extendido. Rev. Peru. Med. Exp. Salud Publica 2010, 27(3):345-351.
35. 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(6):1506-1517.
36. Livermore D.M., Cantón 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(2):165-174.
37. Lu S.Y., Zhang Y.L., Geng S.N., Li T.Y., Ye Z.M., Zhang D.S., Zou F., Zhou H.W. High diversity of extended-spectrum beta-lactamase-producing bacteria in an urban river sediment habitat. Appl. Environ. Microbiol. 2010, 76:5972-5976.
38. Machado E., Coque T.M., Cantón R., Baquero F., Sousa J.C., Peixe L. Dissemination in Portugal of CTX-M-15-, OXA-1-, and TEM-1-producing Enterobacteriaceae strains containing the aac(6')-Ib-cr gene, which encodes an aminoglycoside- and fluoroquinolone-modifying enzyme. Antimicrob. Agents Chemother. 2006, 50(9):3220-3221. The Portuguese Resistance Study Group.
39. Machado E., Coque T.M., Cantón R., Novais A., Sousa J.C., Baquero F., Peixe L. High diversity of extended-spectrum b-lactamases among clinical isolates of Enterobacteriaceae from Portugal. J. Antimicrob. Chemother. 2007, 60:1370-1374.
40. Machado E., Coque T.M., Cantón R., Sousa J.C., Silva D., Ramos M., Rocha J., Ferreira H., Peixe L. Leakage into Portuguese aquatic environments of extended-spectrum-beta-lactamase-producing Enterobacteriaceae. J. Antimicrob. Chemother. 2009, 63(3):616-618.
41. McDermott P.F., Zhao S., Wagner D.D., Simjee S., Walker R.D., White D.G. The food safety perspective of antibiotic resistance. Anim. Biotechnol. 2002, 13(1):71-84.
42. Medeiros A. Evolution and dissemination of β-lactamases accelerated by generations of β-lactam antibiotics. Clin. Infect. Dis. 1997, 24(Suppl. 1):S19-S45.
43. Moland E.S., Hanson N.D., Black J.A., Hossain A., Song W., Thomson K.S. Prevalence of newer β-lactamases in gram-negative clinical isolates collected in the United States from 2001 to 2002. J. Clin. Microbiol. 2006, 44(9):3318-3324.
44. Naas T., Poirel L., Nordmann P. Minor extended-spectrum beta-lactamases. Clin. Microbiol. Infect. 2008, 14(Suppl. 1):42-52.
45. Ojer-Usoz E., González D., Vitas A.I., Leiva J., García-Jalón I., Febles Casquero A., Escolano M.S. Prevalence of extended-spectrum β-lactamase-producing Enterobacteriaceae in meat products. Meat Sci. 2012, 93(2):316-321.
46. Oteo J., Garduño E., Bautista V., Cuevas O., Campos J. Antibiotic-resistant Klebsiella pneumoniae in Spain: analyses of 718 invasive isolates from 35 hospitals and report of one outbreak caused by an SHV-12-producing strain. J. Antimicrob. Chemother. 2008, 61(1):222-224.
47. Oteo J., Navarro C., Cercenado E., Delgado-Iribarren A., Wilhelmi I., Orden B. 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.
48. Paterson D.L., Bonomo R.A. Extended-Spectrum β-Lactamases: a clinical update. Clin. Microbiol. Rev. 2005, 18(4):657-686.
49. Pavlov D., de Wet C.M., Grabow W.O., Ehlers M.M. Potentially pathogenic features of heterotrophic plate count bacteria isolated from treated and untreated drinking water. Int. J. Food Microbiol. 2004, 92(3):275-287.
50. Philippon A., Arlet G., Lagrange P.H. Origin and impact of plasmid-mediated extended-spectrum beta-lactamases. Eur. J. Clin. Microbiol. Infect. Dis. 1994, 13(Suppl. 1):S17-S29.
51. Poirel L., Gniadkowski M., Nordmann P. Biochemical analysis of the ceftazidime-hydrolysing extended-spectrum beta-lactamase CTX-M-15 and of its structurally related beta-lactamase CTX-M-3. J. Antimicrob. Chemother. 2002, 50(6):1031-1034.
52. Pulcrano G., Iula D.V., deLuca C., Roscetto E., Vollaro A., Rossano F., Catania M.R. Clonal dissemination of Klebsiella pneumoniae ST512 carrying blaKPC-3 in a hospital in southern Italy. APMIS 2014, 122:42-46.
53. Randall L.P., Clouting C., Horton R.A., Coldham M.G., Wu G., Clifton-Hadley F.A., Davies R.H., Teale C.J. Prevalence of Escherichia coli carrying extended-spectrum b-lactamases (CTX-M and TEM-52) from broiler chickens and turkeys in Great Britain between 2006 and 2009. J. Antimicrob. Chemother. 2011, 66:86-95.
54. Reinthaler F.F., Feierl G., Galler H., Haas D., Leitner E., Mascher F., Melkes A., Posch J., Winter I., Zarfel G., Marth E. ESBL-producing E. coli in Austrian sewage sludge. Water Res. 2010, 44(6):1981-1985.
55. Sande-Bruinsma N., Grundmann H., Verloo D., Tiemersma E., Monen J., Goossens H., Ferech M. Antimicrobial drug use and resistance in Europe. Emerg. Infect. Dis. 2008, 14(11):1722-1730.
56. 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.
57. 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. Electron J. Biotechn. 2006, 9(5):533-540.
58. Tacão M., Correia A., Henriques I. Resistance to broad-spectrum antibiotics in aquatic systems: anthropogenic activities modulate the dissemination of blaCTX-M-like genes. Appl. Environ. Microbiol. 2012, 78:4134-4140.
59. 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.
60. Tan T.Y., Ng L.S., He J., Koh T.H., Hsu L.Y. Evaluation of screening methods to detect plasmid-mediated AmpC in Escherichia coli, Klebsiella pneumoniae and Proteus mirabilis. Antimicrob. Agents Chemother. 2009, 53(1):146-149.
61. Thomas C., Moore L., Elamin N., Doumith M., Zhang J., Maharjan S., Warner M., Perry C., Turton J., Johnstone C., Jepson A., Duncan N., Holmes A., Livermore D.M., Woodford N. Early (2008-2010) hospital outbreak of Klebsiella pneumoniae producing OXA-48 carbapenemase in the UK. Int. J. Antimicrob. Ag. 2013, 42(6):531-536.
62. Thomson K.S., Sanders C.C. Detection of extended spectrum beta-lactamases in members of the family Enterobacteriaceae: comparison of the double-disk and three-dimensional tests. Antimicrob. Agents Chemother. 1992, 36(9):1877-1882.
63. Thomson K. Extended-Spectrum-β-Lactamase, AmpC, and carbapenemase issues. J. Clin. Microbiol. 2010, 48(4):1019-1025.
64. Tissera S., Lee S.M. Isolation of extended spectrum β-lactamase (ESBL) producing bacteria from urban surface waters in Malaysia. Malays. J. Med. Sci. 2013, 20(3):14-22.
65. Torres C., Zarazaga M. BLEE en animales y su importancia en la trasmisión a humanos. Enferm. Infecc. Microbiol. Clin. 2007, 25(2):29-37.
66. Valverde A., Coque T.M., Sánchez-Moreno M.P., Rollán A., Baquero F., Cantón R. Dramatic increase in prevalence of fecal carriage of extended-spectrum beta-lactamase-producing Enterobacteriaceae during nonoutbreak situations in Spain. J. Clin. Microbiol. 2004, 42(10):4769-4775.
67. Vieira A.R., Collignon P., Aarestrup F.M., McEwen S.A., Hendriksen R.S., Hald T., Wegener H.C. Association between antimicrobial resistance in Escherichia coli isolates from food animals and Blood stream isolates from humans in Europe: an ecological study. Foodborne Pathog. Dis. 2011, 8(12):1295-1301.
68. Wiegand I., Geiss H.K., Mack D., Stürenburg E., Seifert H. Detection of extended-spectrum beta-lactamases among Enterobacteriaceae by use of semiautomates Microbiology Systems and manual detection procedures. J. Clin. Microbiol. 2007, 45(4):1167-1174.
69. Wise R., Hart T., Cars O., Streulens M., Helmuth R., Huovinen P., Sprenger M. Antimicrobial resistance: is a major threat to public health. Br. Med. J. 1998, 5(317):609-610.
70. Woodford N., Fagan E.J., Ellington M.J. Multiplex PCR for rapid detection of genes encoding CTX-M extended-spectrum (beta)-lactamases. J. Antimicrob. Chemother. 2006, 57(1):154-155.
71. Woodford N., Turton J.F., Livermore D.M. Multiresistant gram-negative bacteria: the role of high-risk clones in the dissemination of antibiotic resistance. FEMS Microbiol. Rev. 2011, 35:736-755.
72. World Health Organization (WHO) Critically Important Antimicrobials for Human Medicine: Categorization for the Development of Risk Management Strategies to Contain Antimicrobial Resistance Due to Non-human Antimicrobial Use 2007, Report of the Second WHO Expert Meeting. Copenhagen. May 29-31, 2007.
73. Wright G. Antibiotic resistance in the environment: a link to the clinic?. Curr. Opin. Microbiol. 2010, 13(5):589-594.
74. Zhang X.X., Zhang T., Fang H.H. Antibioitic resistance genes in water environment. Appl. Microbiol. Biotechnol. 2009, 82(3):397-414.
75. Zurfluh K., Hächler H., Nüesch-Inderbinen M., Stephan R. Characteristics of extended-spectrum β-lactamase- and carbapenemase-producing Enterobacteriaceae isolates from rivers and lakes in Switzerland. Appl. Environ. Microbiol. 2013, 79(9):3021-3026.