Correspondence Comment on “Antibiotic Resistance Genes as Emerging Contaminants: Studies in Northern Colorado” Received for review December 6, 2006. Accepted January 24, 2007. These comments are merely qualifications, not criticisms of Dr. Pruden’s fine paper (1). Resistance has been attributed to drug over-use. Pruden notes a less well-understood mechanism for the amplification of multi-drug resistance, sewage. The local sewer-treatment plant releases pathogens and resistance to the environment and agriculture (2). Wastewater treatment intermixes organisms otherwise seldom coming together. Selective pressures increase survival mechanisms (3). Defense strategies include going dormant, entering the viable but non-culturable (VBNC) state. These VBNC organisms are essentially invisible to laboratory tests used in the wastewater industry. Higgins and Murthy recently reconfirmed this (4) in a paper that raises some serious questions about the efficacy of current standards. Those authors noted that during centrifuged dewatering of sewer sludge, indicators in a VBNC state were resuscitated. The results were several magnitudes greater than standard plate counts had indicated (4). Such findings raise logical questions. If dewatering by centrifuge brought out the essence of VBNC, would other products of sewage that had not been subjected to the centrifuge also be in the VBNC state? If so would they revive in the field following agricultural application of sludge or irrigation with reclaimed wastewater? This seems plausible but needs further study. Additionally, as stresses increase organisms can acquire genes from or transfer genes to nonrelated organisms, organisms even within completely different kingdoms (5, 6). There are other materials dumped into the drain that confer resistance. This includes industrial chemicals, heavy metals, and disinfectants. Triclosan, a ubiquitous biocide, is suspected of inducing resistance, as are many other industrial materials found in sewage (7, 8). Changes to the cellular machinery afford the ability to deal with numerous insults, hence cross-resistance (9). Many antimicrobials including metabolites enter sewage essentially unchanged to induce resistance in the environment (10). Kummerer (11-15) and others (16) note levels of antibiotics/pharmaceuticals in sewage able to induce or maintain resistance, hence adding to the risks in crop production through irrigation. Based on wastewater (sewage) industry and regulatory opinion, the standards, the released effluent, and its use for crop irrigation or the land application of sewage sludge are benign and beneficial activities (17). If, however, one reviews the current medical and scientific literature, a different picture emerges, one that raises serious questions about the benevolence of this activity and efficacy of the underlying standards (18). Thus, the issue takes on aspects of a political and not a scientific argument (18, 19). In the interim, most regulatory agencies have backed off (20). This leaves the citizens and patient base essentially standing naked. In 2002 the NAS/NRC (21) called into question the U.S. EPA Part 503 guidelines for land application of sewage sludge 10.1021/es0680156 CCC: $37.00 Published on Web 02/27/2007
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(biosolids) and specifically EPA’s failure to consider antibiotic resistance. As of writing this comment, EPA has shown little if any progress in investigating resistance. A Freedom of Information Act request to EPA on this subject was submitted in February 2005. The agency has not answered that request (20). Additionally, the agency has not done health hazards risk analyses for pathogens. Notwithstanding these shortcomings, the agency and the wastewater industry continue to promote the use of sewage byproducts in crop production. Salinas Valley is an example.
Supporting Information Available Additional information and references. This material is available free of charge via the Internet at http:// pubs.acs.org.
Literature Cited (1) Pruden, A.; Pei, R.; Storteboom, H.; Carlson, K. H. Antibiotic Resistance Genes as Emerging Contaminants: Studies in Northern Colorado. Environ. Sci. Technol. 2006, 40 (23), 74457450. (2) (a) Ribeiro-Dias, J. C.; Vicente, A. C.; Hofer, E. Fecal coliforms in sewage waters. I. Resistance to antibiotics, heavy metals and colicinogeny. Appl. Environ. Microbiol. 1983, 46 (1), 227232. (b) Marcinek, H.; Wirth, R.; Muscholl-Silberhorn, A.; Gauer, M. Enterococcus faecalis gene transfer under natural conditions in municipal sewage water treatment plants. Appl. Environ. Microbiol. 1998, 64 (2), 626-632. (3) Nakamura, S.; Shirota, H. Behavior of drug resistant fecal coliforms and R plasmids in a wastewater treatment plant. Nippon Koshu Eisei Zasshi 1990, 37 (2), 83-90. (4) Higgins, M. J., Murthy, S. Examination of Reactivation and Regrowth of Fecal Coliforms in Anaerobically Digested Sludge; WERF Report: Biosolids and Residuals (03-CTS-13T); Water Environment Research Foundation: Alexandria, VA, 2006. (5) Faguy, D. M. Lateral gene transfer (LGT) between Archaea and Escherichia coli is a contributor to the emergence of novel infectious disease. BMC Infect. Dis. 2003, 3, 13. (6) Nesbo, C. L. Phylogenetic analyses of two “archaeal” genes in Thermotoga maritima reveal multiple transfers between archaea and bacteria. Mol. Biol. Evol. 2001, 18 (3), 362-375. (7) Randall, L. P.; Cooles, S. W.; Piddock, L. J. V.; Woodward, M. J. Effect of Triclosan or phenolic farm disinfectant on the selection of antibiotic resistant Salmonella enterica. J. Antimicrob. Chemother. 2004, 54, 621-627. (8) Kinney, C. A.; Furlong, E. T.; Zaugg, S. D.; Burkhardt, M. R.; Werner, S. L.; Cahill, J. D.; Jorgensen, G. R. Survey of Organic Wastewater Contaminants in Biosolids Destined for Land Application. Environ. Sci. Technol. 2006, 40, 7207-7215. (9) Al-Ahmad, A.; Daschner, F. D.; Kummerer, K. Biodegradability of cefotiam, ciprofloxacin, meropenem, penicillin G, and sulfamethoxazole and inhibition of waste water bacteria. Arch. Environ. Contam. Toxicol. 1999, 37 (2), 158-163. (10) Kinney C. A.; Furlong, E. T.; Werner, S. L.; Cahill, J. D. Presence and distribution of wastewater-derived pharmaceuticals in soil irrigated with reclaimed water. Environ. Toxicol. Chem. 2006, 25 (2), 317-326. (11) Kummerer, K. Resistance in the environment. J. Antimicrob. Chemother. 2004, 54 (2), 311-320. (12) Kummerer, K. Promoting resistance by the emission of antibiotics from hospitals and households into effluent. Clin. Microbiol. Infect. 2003, 9 (12), 1203-1214. (13) Kummerer, K. Standardized tests fail to assess the effects of antibiotics on environmental bacteria. Water Res. 2004, 38 (8), 2111-2116. (14) Kummerer, K. Biodegradability of some antibiotics, elimination of the genotoxicity and affection of wastewater bacteria in a simple test. Chemosphere 2000, 40 (7), 701-710. (15) Kummerer, K. Drugs, diagnostic agents and disinfectants in wastewater and water-a review. Schriftenr. Ver Wasser Boden Lufthyg. 2000, 105, 59-71. VOL. 41, NO. 7, 2007 / ENVIRONMENTAL SCIENCE & TECHNOLOGY
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(16) Rooklidge, S. J. Environmental antimicrobial contamination from terraccumulation and diffuse pollution pathways. Sci. Total Environ. 2004, 325 (1-3), 1-13. (17) Code of Federal Regulations, Appendix B, subpart D of Part 503, Title 40, July 1, 1998. (18) Snyder, C. The Dirty Work of Promoting “Recycling” of America’s Sewage Sludge. Int. J. Occup. Health 2005, 11, 415427. (19) Mintz, J. A. “Treading Water”: A Preliminary Assessment of EPA Enforcement During the Bush II Administration. Environ. Law Reporter 2004, 34, 10933-10953. (20) Personal communications with EPA and CDC.
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(21) National Research Council of the National Academy of Sciences (NAS). Biosolids Applied to Land: Advancing Standards and Practices; National Academy Press: Washington, DC, 2002.
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