Reclaimed water as a reservoir of antibiotic resistance genes: Distribution system and irrigation implications

Frontiers in Microbiology

Volumn 4, Issue MAY, 2013, Pages

  Fahrenfeld, Nicole ^a   Ma, Yanjun ^a   O'Brien, Maureen ^b   Pruden, Amy ^a  

^a State University   (United States)

^b Department of Geology and Geological Engineering   (United States)

Author keywords

Antibiotic resistance genes; Irrigation; Reclaimed water distribution systems; Water reuse

Indexed keywords

MACROLIDE; METICILLIN; SULFONAMIDE; TETRACYCLINE; WATER;

AGRICULTURAL PARAMETERS; ANTIBIOTIC RESISTANCE GENE; ARTICLE; BACTERIAL GROWTH; BIOFILM; CHLORINATION; CLUSTER ANALYSIS; COPY NUMBER VARIATION; DNA EXTRACTION; ECRFX GENE; ERM F GENE; ESCHERICHIA COLI; GADAB GENE; GENE; GYRB GENE; IRRIGATION (AGRICULTURE); LEGIONELLA PNEUMOPHILA; MICROCOSM; MIP GENE; NONHUMAN; NUCLEOTIDE SEQUENCE; POINT OF ENTRY; POINT OF USE; POLYMERASE CHAIN REACTION; PSEUDOMONAS AERUGINOSA; SUL 2 GENE; VAN A GENE; WASTE WATER RECYCLING;

BACTERIA (MICROORGANISMS); ESCHERICHIA COLI; LEGIONELLA PNEUMOPHILA; PSEUDOMONAS AERUGINOSA;

EID: 84884258044     PISSN: None     EISSN: 1664302X     Source Type: Journal    
DOI: 10.3389/fmicb.2013.00130     Document Type: Article

References (39)

1. Aminov, R., Garrigues-Jeanjean, N., and Mackie, R. (2001). Molecular ecology of tetracycline resistance: development and validation of primers for detection of tetracycline resistance genes encoding ribosomal protection proteins. Appl. Environ. Microbiol. 67, 22-32.
2. Aminov, R. I., Chee-Sanford, J. C., Garrigues, N., Teferedegne, B., Krapac, I. J., White, B. A., et al. (2002). Development, validation, and application of PCR primers for detection of tetracycline efflux genes of Gram-negative bacteria. Appl. Environ. Microbiol. 68, 1786-1793.
3. Anuj, S. N., Whiley, D. M., Kidd, T. J., Bell, S. C., Wainwright, C. E., Nissen, M. D., et al. (2009). Identification of Pseudomonas aeruginosa by a duplex real-time polymerase chain reaction assay targeting the ecfX and the gyrB genes. Diagn. Microbiol. Infect. Dis. 63, 127-131.
4. Auerbach, E. A., Seyfried, E. E., and McMahon, K. D. (2007). Tetracycline resistance genes in activated sludge wastewater treatment plants. Water Res. 41, 1143- 1151.
5. Böckelmann, U., Dörries, H.-H., Ayuso-Gabella, M. N., Salgot de Marçay, M., Tandoi, V., Levantesi, C., et al. (2009). Quantitative PCR monitoring of antibiotic resistance genes and bacterial pathogens in three European artificial groundwater recharge systems. Appl. Environ. Microbiol. 75, 154-163.
6. Brunkard, J. M., Ailes, E., Roberts, V. A., Hill, V., Hilborn, E. D., Craun, G. F., et al. (2011). Surveillance for waterborne disease outbreaks associated with drinking water - United States. MMWR Surveill. Summ. 60, 38-75.
7. Carlet, J., Jarlier, V., Harbarth, S., Voss, A., Goossens, H., and Pittet, D. (2012). Ready for a world without antibiotics? The pensières antibiotic resistance call to action. Antimicrob. Resist. Infect. Control 1, 11.
8. Chen, J., Yu, Z., Michel, F. C., Wittum, T., and Morrison, M. (2007). Development and application of real-time PCR assays for quantification of erm genes conferring resistance to macrolides-lincosamides-streptogramin B in livestock manure and manure management systems. Appl. Environ. Microbiol. 73, 4407-4416.
9. Chen, Y.-C., Higgins, M. J., Maas, N. A., and Murthy, S. N. (2006). DNA extraction and Escherichia coli quantification of anaerobically digested biosolids using the competitive touchdown PCR method. Water Res. 40, 3037-3044.
10. Clark, N. C., Cooksey, R. C., Hill, B. C., Swenson, J. M., and Tenover, F. C. (1993). Characterization of glycopeptide-resistant enterococci from U.S. hospitals. Antimicrob. Agents Chemother. 37, 2311-2317.
11. Czekalski, N., Berthold, T., Caucci, S., Egli, A., and Buergmann, H. (2012). Increased levels of multiresistant bacteria and resistance genes after wastewater treatment and their dissemination into Lake Geneva, Switzerland. Front. Microbiol. 3:106. doi: 10.3389/fmicb.2012.00106
12. Dodd, M. C. (2012). Potential impacts of disinfection processes on elimination and deactivation of antibiotic resistance genes during water and wastewater treatment. J. Environ. Monit. 14, 1754-1771.
13. Dutka-Malen, S., Evers, S., and Courvalin, P. (1995). Detection of glycopeptide resistance genotypes and identification to the species level of clinically relevant enterococci by PCR. J. Clin. Microbiol. 33, 24-27.
14. Forsberg, K. J., Reyes, A., Wang, B., Selleck, E. M., Sommer, M. O. A., and Dantas, G. (2012). The shared antibiotic resistome of soil bacteria and human pathogens. Science 337, 1107-1111.
15. Grant, M. A., Weagant, S. D., and Feng, P. (2001). Glutamate decarboxylase genes as a prescreening marker for detection of pathogenic Escherichia coli groups. Appl. Environ. Microbiol. 67, 3110-3114.
16. Grant, S. B., Saphores, J.-D., Feldman, D. L., Hamilton, A. J., Fletcher, T. D., Cook, P. L. M., et al. (2012). Taking the "waste" out of "wastewater" for human water security and ecosystem sustainability. Science 337, 681-686.
17. Kim, S., Park, H., and Chandran, K. (2010). Propensity of activated sludge to amplify or attenuate tetracycline resistance genes and tetracycline resistant bacteria: a mathematical modeling approach. Chemosphere 78, 1071-1077.
18. LaPara, T. M., Burch, T. R., McNamara, P. J., Tan, D. T., Yan, M., and Eichmiller, J. J. (2011). Tertiary-treated municipal wastewater is a significant point source of antibiotic resistance genes into Duluth-Superior harbor. Environ. Sci. Technol. 45, 9543-9549.
19. Ma, Y., Wilson, C. A., Novak, J. T., Riffat, R., Aynur, S., Murthy S., et al. (2011). Effect of various sludge digestion conditions on sulfonamide, macrolide, and tetracycline resistance genes and class I Integrons. Environ. Sci. Technol. 45, 7855-7861.
20. McKinney, C. W., and Pruden, A. (2012). Ultraviolet disinfection of antibiotic resistant bacteria and their antibiotic resistance genes in water and wastewater. Environ. Sci. Technol. 46, 13393-13400.
21. McLain, J. T., and Williams, C. (2012). Assessing environmental impacts of treated wastewater through monitoring of fecal indicator bacteria and salinity in irrigated soils. Environ. Monit. Assess. 184, 1559-1572.
22. Munir, M., and Xagoraraki, I. (2011). Levels of antibiotic resistance genes in manure, biosolids, and fertilized soil. J. Environ. Qual. 40, 248-255.
23. Nazarian, E. J., Bopp, D. J., Saylors, A., Limberger, R. J., and Musser, K. A. (2008). Design and implementation of a protocol for the detection of Legionella in clinical and environmental samples. Diagn. Microbiol. Infect. Dis. 62, 125-132.
24. Negreanu, Y., Pasternak, Z., Jurkevitch, E., and Cytryn, E. (2012). Impact of treated wastewater irrigation on antibiotic resistance in agricultural soils. Environ. Sci. Technol. 46, 4800-4808.
25. Pruden, A. (2011). "Unique challenges in the health risk assessment of antibiotic resistance genes in the environment," in Society for Environmental Toxicology and Chemistry (SETAC) 32nd Annual Meeting, November 13-16, Boston, MA.
26. Pruden, A., Arabi, M., and Storteboom, H. N. (2012). Correlation between upstream human activities and riverine antibiotic resistance genes. Environ. Sci. Technol. 46, 11541-11549.
27. Pruden, A., Edwards, M., and Falkinham, J. O. III. (2013). "State of the Science of opportunistic pathogens in premise plumbing: methodology, microbial ecology, and epidemiology," in Water Research Foundation Project 4379 Final Report. Denver, CO: Water Research Foundation.
28. Pruden, A., Pei, R., Storteboom, H., and Carlson, K. H. (2006). Antibiotic resistance genes as emerging contaminants: studies in Northern Colorado. Environ. Sci. Technol. 40, 7445-7450.
29. Rubiano, M.-E., Agulló-Barceló, M., Casas-Mangas, R., Jofre, J., and Lucena, F. (2012). Assessing the effects of tertiary treated wastewater reuse on a Mediterranean river (Llobregat, NE Spain), part III: pathogens and indicators. Environ. Sci. Pollut. Res. 19, 1026-1032.
30. Ryu, H., Alum, A., and Abbaszadegan, M. (2005). Microbial characterization and population changes in nonpotable reclaimed water distribution systems. Environ. Sci. Technol. 39, 8600-8605.
31. Schwartz, T., Kohnen, W., Jansen, B., and Obst, U. (2003). Detection of antibiotic-resistant bacteria and their resistance genes in wastewater, surface water, and drinking water biofilms. FEMS Microbiol. Ecol. 43, 325-335.
32. Stevens, D. L. (2006). The role of vancomycin in the treatment paradigm. Clin. Infect. Dis. 42, S51-S57.
33. Storteboom, H., Arabi, M., Davis, J. G., Crimi, B., and Pruden, A. (2010). Tracking antibiotic resistance genes in the South Platte River basin using molecular signatures of urban, agricultural, and pristine sources. Environ. Sci. Technol. 44, 7397-7404.
34. Suzuki, M. T., Taylor, L. T., and DeLong, E. F. (2000). Quantitative analysis of small-subunit rRNA genes in mixed microbial populations via 5'-nuclease assays. Appl. Environ. Microbiol. 66, 4605-4614.
35. Trautmann, M., Lepper, P. M., and Haller, M. (2005). Ecology of Pseudomonas aeruginosa in the intensive care unit and the evolving role of water outlets as a reservoir of the organism. Am. J. Infect. Control 33, S41-S49.
36. US Environmental Protection Agency (USEPA). (2012). Guidelines for Water Reuse. Washington, DC: USEPA.
37. Wang, H., Edwards, M., Falkinham, J. O., and Pruden, A. (2012). Molecular survey of the occurrence of Legionella spp., Mycobacterium spp., Pseudomonas aeruginosa, and Amoeba hosts in two chloraminated drinking water distribution systems. Appl. Environ. Microbiol. 78, 6285-6294.
38. Webber, M. A., and Piddock, L. J. V. (2003). The importance of efflux pumps in bacterial antibiotic resistance. J. Antimicrob. Chemother. 51, 9-11.
39. Xi, C., Zhang, Y., Marrs, C. F., Ye, W., Simon, C., Foxman, B., et al. (2009). Prevalence of antibiotic resistance in drinking water treatment and distribution systems. Appl. Environ. Microbiol. 75, 5714-5718.