Environ. Sci. Technol. 2003, 37, 5836
Response to Comment on “Evidence for the Absence of Staphylococcus aureus in Land Applied Biosolids” This is our response to Lewis and Gattie’s (1) critique of our peer-reviewed paper (2). First, we did not “dismiss” processed sewage sludges as a source of Staphylococcus aureus in our paper or in our interviews with Ms. Renner (3). We said that our “results suggest that biosolids are not a likely source of S. aureus human exposure or infection” (2) and that our results are “evidence that biosolids are an unlikely source of S. aureus infection” (3). Second, we did not say that Lewis and Gattie proposed that residents are usually directly infected by S. aureus in biosolids. We did say that their paper suggested that the potential existed (4). This is reasonable as these authors write “Although pathogens die off following application, winds may carry dusts embedded with viable pathogens and irritant chemicals for miles.” and “These observations suggest that irritant chemicals may elevate risks of infection from low levels of pathogens in sewage sludges, especially with organisms such as staphylococci ...”. Other statements also address biosolids as a direct source of pathogens as well as irritant chemicals. In addition, their critique provides a rationale for the presence of S. aureus in biosolids in paragraphs 2-5. We acknowledge that the recovery of pathogens from environmental samples is difficult. Our recovery efficiency of 8.9% is reasonable. It compares favorably with the ELISA method of detecting S. aureus thermostable nuclease with a minimum detection limit of 105 S. aureus/mL (5). There are many environmental and microbial factors that influence susceptibility to disinfectants as discussed in an extensive review by Rusin and Gerba (6). It is inappropriate to write that Rusin et al. (2) “assumed” that the 91% of unrecoverable S. aureus cells were as susceptible to disinfection as the recovered cells. We made no such statement. It is true that some S. aureus may be difficult to recover from environmental samples due to being embedded in organic matter. It is also possible that much of the S. aureus is difficult to recover due to the presence of high numbers of background bacteria. High background counts of bacteria can influence the recovery efficiency of pathogens (7). The reasons for the lack of detection of 91% of the seeded S. aureus may be multiple and may remain unknown. It is true that we did not test millions of tons of biosolid samples. This is beyond the realm of reality. However, we tested grab samples of a representative variety of Class A and Class B biosolids. It is typical for a drinking water plant that produces millions of gallons of distribution water per day to test only a few liters per month for coliforms. Similarly, only a small fraction of food products are tested for microbial quality. Whether or not this monitoring offers little, if any, insight into the microbial quality of food and water in the United States is debatable. However, it is impractical for any scientist to test millions of tons of samples. Whether S. aureus is more susceptible than other staphylococci to dissimilar processes used to treat sewage sludge has not been determined. As there are 31 species of staphylococci other than S. aureus, there is a possibility that some species are more likely to survive biosolid treatment processes than others. In addition to disinfection, biosolid bacterial populations are subjected to competition from other flora, high pH, high temperatures, and/or desiccation. 5836
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There is little information available regarding the environmental occurrence of S. aureus and other staphylococci. Information is particularly scarce for nonfood samples and environments not heavily influenced by warm-blooded animals. Therefore, we cannot say that S. aureus is more adept at survival than the other 31 members of the genus. The evidence suggests that S. aureus is not common in the environment. The major habitats of S. aureus are the nares, skin, and (to a lesser extent) the gastrointestinal tract of mammals and birds (8). Rusin and Maxwell (9) identified heterotrophic plate count bacterial populations over a 2-yr period in water samples. The predominant Gram-positive bacteria in reservoir, well, and distribution water samples were coagulase-negative staphylococci. S. aureus was not isolated from reservoir or well samples and was identified in only 1% of the distribution samples. The results of our study suggest that land-applied biosolids are not likely to be direct sources of infection of S. aureus. We also emphasize the importance of rigorous confirmation techniques. Further studies to evaluate the possible effect of pathogens or irritants in biosolids remain to be conducted. These issues will remain topics of scientific debate for some time.
Literature Cited (1) Lewis, D. L.; Gattie, D. K. Comment on “Evidence for the Absence of Staphylococcus aureus in Land Applied Biosolids. Environ. Sci. Technol. 2003, 37, 5834. (2) Rusin, P. A.; Maxwell, S. L.; Brooks, J. P.; Gerba, C. P.; Pepper. I. L. Evidence for the absence of Staphylococcus aureus in Land Applied Biosolids. Environ. Sci. Technol. 2003, 37 (18), 40274030. (3) Renner, R. Staphylococcus not found in sludge, but controversy continues. Environ. Sci. Technol. 2003, 37 (19), 344A. (4) Lewis, D. L.; Gattie, D. K. Pathogen risks from applying sewage sludge to land. Environ. Sci. Technol. 2002, 36, 286A-293A. (5) Yazdankhah, S. P.; Solverod, L.; Simonsen, S.; Olsen, E. Development and evaluation of an immunomagnetic separation-ELISA for the detection of Staphylococcus aureus thermostable nuclease in composite milk. Vet. Microbiol. 1999, 76, 113-115. (6) Rusin, P. A.; Gerba, C. P. Association of chlorination and UV irradiation to increasing antibiotic resistance in bacteria. Rev. Environ. Contam. Toxicol. 2001, 171, 1-52. (7) Geldreich, E. E. Microbial Quality of Water Supply in Distribution Systems; CRC Lewis Publishers: New York, 1996; p 108. (8) Kloos, W. E.; Bannerman, T. L. Staphylococcus and Micrococcus. In Manual of Clinical Microbiology, 7th ed.; Murray, P. R., Ed.; ASM Press: Washington, DC, 1999; pp 264-277. (9) Rusin, P.; Maxwell, S. Comparison of heterotrophic plate count bacteria in source waters and Tucson distribution waters before and after the opening of the Clearwater facility. Report to UA NSF Water Quality Center, April 2003.
Patricia A. Rusin,* Sheri L. Maxwell, John P. Brooks, Charles P. Gerba, and Ian L. Pepper Department of Soil, Water, and Environmental Science University of Arizona Tuscon, Arizona 85721 ES0301222 10.1021/es0301222 CCC: $25.00
2003 American Chemical Society Published on Web 10/31/2003
