Abstract
Bacterial antibiotic resistance has long been a public health concern worldwide. Although antibiotic abuse highly correlates with occurrence of resistant pathogens in hot spots like animal feedlots, it remains obscure how frequently these resistance genotypes would emerge and/or retain in natural circumstances. In this study, we monitored seven antibiotic resistance genes in various surface waters. All seven resistance genes were detectable in Puzih River samples, including strA (40.6 %), cmlA (29.7 %), blaTEM (9.1 %), tet(B) (8.5 %), sul1 (7.9 %), mecA (3.6 %), and tet(A) (2.4 %). Among these genes, strA was observed in four out of five sampling occasions during the 1.5-year monitoring period and most of the genes were detected at least two times over five samplings. These results imply that surface waters in Taiwan act as potential reservoirs for several resistance genotypes. Moreover, high prevalence of tet(A) (92.0 %) and sul1 (96.0 %) in swine farm wastewater samples suggests routine antibiotic usage and particularly, the fodder supplements could indeed be a risk factor to antibiotic resistance in environments. sul1, tet(A), blaTEM, and strA were detectable in domestic water treatment plants and reservoirs, suggesting that several resistance genotypes against antibiotics as streptomycin, ampicillin, tetracycline, and sulfonamides are likely to persist in natural circumstance and may consequently contaminate the drinking water systems.
Similar content being viewed by others
References
Aarestrup, F. M., Seyfarth, A. M., Emborg, H. D., Pedersen, K., Hendriksen, R. S., & Bager, F. (2001). Effect of abolishment of the use of antimicrobial agents for growth promotion on occurrence of antimicrobial resistance in fecal enterococci from food animals in Denmark. Antimicrobial Agents and Chemotherapy, 45, 2054–2059.
Alpay-Karaoglu, S., Ozgumus, O. B., Sevim, E., Kolayli, F., Sevimi, A., & Yesilgil, P. (2007). Investigation of antibiotic resistance profile and TEM-type beta-lactamase gene carriage of ampicillin-resistant Escherichia coli strains isolated from drinking water. Annals of Microbiology, 57, 281–288.
Boerlin, P., Wissing, A., Aarestrup, F. M., Frey, J., & Nicolet, J. (2001). Antimicrobial growth promoter ban and resistance to macrolides and vancomycin in enterococci from pigs. Journal of Clinical Microbiology, 39, 4193–4195.
Carlson, S. A., Bolton, L. F., Briggs, C. E., Hurd, H. S., Sharma, V. K., Fedorka-Cray, P. J., & Jones, B. D. (1999). Detection of multiresistant Salmonella typhimurium DT104 using multiplex and fluorogenic PCR. Molecular and Cellular Probes, 13, 213–222.
CDC (2013): http://www.cdc.gov/drugresistance. Accessed December 1, 2013.
Chee-Sanford, J. C., Aminov, R. I., Krapac, I. J., Garrigues-Jeanjean, N., & Mackie, R. I. (2001). Occurrence and diversity of tetracycline resistance genes in lagoons and groundwater underlying two swine production facilities. Applied and Environmental Microbiology, 67, 1494–1502.
Chen, Y. P., Tsao, M. Y., Lee, S. H., Chou, C. H., & Tsai, H. J. (2010). Prevalence and molecular characterization of chloramphenicol ressistance in Riemerella anatipestifer isolated from ducks and geese in Taiwan. Avian Pathology, 39, 333–338.
Council of Agriculture, Executive Yuan, Taiwan (2014): http://www.coa.gov.tw/. Accessed December 1, 2013.
Daghrir, R., & Drogui, P. (2013). Tetracycline antibiotics in the environment: a review. Environmental Chemistry Letters, 11, 209–227.
Else, T. A., Pantle, C. R., & Amy, P. S. (2003). Boundaries for biofilm formation: humidity and temperature. Applied and Environmental Microbiology, 69, 5006–5010.
Environmental Protection Bureau of Kaohsiung City Government, Taiwan (2014): http://kses.ksepb.gov.tw/. Accessed December 1, 2013.
Gibbs, S. G., Green, C. F., Tarwater, P. M., Mota, L. C., Mena, K. D., & Scarpino, P. V. (2006). Isolation of antibiotic-resistant bacteria from the air plume downwind of a swine confined or concentrated animal feeding operation. Environmental Health Perspectives, 114, 1032–1037.
Guerra, B., Soto, S. M., Arguelles, J. M., & Mendoza, M. C. (2001). Multidrug resistance is mediated by large plasmids carrying a class 1 integron in the emergent Salmonella enterica serotype [4,5,12:i:-]. Antimicrobial Agents and Chemotherapy, 45, 1305–1308.
Guerri, M. L., Aladuena, A., Echeita, A., & Rotger, R. (2004). Detection of integrons and antibiotic-resistance genes in Salmonella enterica serovar Typhimurium, isolates with resistance to ampicillin and variable susceptibility to amoxicillin-clavulanate. International Journal of Antimicrobial Agents, 24, 327–333.
Hellweger, F. L., Ruan, X. D., & Sanchez, S. (2011). A simple model of tetracycline antibiotic resistance in the aquatic environment (with application to the Poudre River). International Journal of Environmental Research and Public Health, 8, 480–497.
Henriques, I., Moura, A., Alves, A., Saavedra, M. J., & Correia, A. (2006). Analysing diversity among beta-lactamase encoding genes in aquatic environments. FEMS Microbiology Ecology, 56, 418–429.
Ho M, McDonald LC, Lauderdale TL, Yeh LL, Chen PC, Shiau YR (1999). Surveillance of antibiotic resistance in Taiwan, 1998. Journal of Microbiology, Immunology, and Infection = Wei mian yu gan ran za zhi 32, 239–49
Hruska, K., & Franek, M. (2012). Sulfonamides in the environment: a review and a case report. Veterinary Medical Czechoslovak, 57, 1–35.
Hsu, S. C., Chiu, T. H., Pang, J. C., Hsuan-Yuan, C. H., Chang, G. N., & Tsen, H. Y. (2006). Characterisation of antimicrobial resistance patterns and class I integrons among Escherichia coli and Salmonella enterica serovar Choleraesuis strains isolated from humans and swine in Taiwan. International Journal of Antimicrobial Agents, 27, 383–391.
Hsueh, P. R., Liu, C. Y., & Luh, K. T. (2002). Current status of antimicrobial resistance in Taiwan. Emerging Infectious Diseases, 8, 132–137.
Kao, P. M., Tung, M. C., Hsu, B. M., Chou, M. Y., Yang, H. W., She, C. Y., & Shen, S. M. (2013). Quantitative detection and identification of Naegleria spp. in various environmental water samples using real-time quantitative PCR assay. Parasitology Research, 112, 1467–1474.
Kassem, I. I., Esseili, M. A., & Sigler, V. (2008). Occurrence of mecA in nonstaphylococcal pathogens in surface waters. Journal of Clinical Microbiology, 46, 3868–3869.
Knapp, C. W., Lima, L., Olivares-Rieumont, S., Bowen, E., Werner, D., & Graham, D. W. (2012). Seasonal variations in antibiotic resistance gene transport in the Almendares River, Havana, Cuba. Frontiers in Microbiology, 3, 396.
Koike, S., Krapac, I. G., Oliver, H. D., Yannarell, A. C., Chee-Sanford, J. C., Aminov, R. I., & Mackie, R. I. (2007). Monitoring and source tracking of tetracycline resistance genes in lagoons and groundwater adjacent to swine production facilities over a 3-year period. Applied and Environmental Microbiology, 73, 4813–4823.
Kuo, H. C., Chou, C. C., Chang, C. D., Gong, S. R., Wang, M. H., & Chang, S. K. (2009). Characterization of quinolone-resistant enterococcus faecalis isolates from healthy chickens and pigs in Taiwan. Journal of Food and Drug Analysis, 17, 443–450.
Lauderdale, T. L., Aarestrup, F. M., Chen, P. C., Lai, J. F., Wang, H. Y., Shiau, Y. R., Huang, I. W., & Hung, C. L. (2006). Multidrug resistance among different serotypes of clinical Salmonella isolates in Taiwan. Diagnostic Microbiology and Infectious Disease, 55, 149–155.
Lauderdale, T. L., Shiau, Y. R., Wang, H. Y., Lai, J. F., Huang, I. W., Chen, P. C., Chen, H. Y., Lai, S. S., Liu, Y. F., & Ho, M. (2007). Effect of banning vancomycin analogue avoparcin on vancomycin-resistant enterococci in chicken farms in Taiwan. Environmental Microbiology, 9, 819–823.
Lima-Bittencourt, C. I., Cursino, L., Goncalves-Dornelas, H., Pontes, D. S., Nardi, R. M., Callisto, M., Chartone-Souza, E., & Nascimento, A. M. (2007). Multiple antimicrobial resistance in Enterobacteriaceae isolates from pristine freshwater. Genetics and Molecular Research, 6, 510–21.
Lo, Y. P., Wan, M. T., Chen, M. M., Su, H. Y., Lauderdale, T. L., & Chou, C. C. (2012). Molecular characterization and clonal genetic diversity of methicillin-resistant Staphylococcus aureus of pig origin in Taiwan. Comparative Immunology Microbiology and Infectious Diseases, 35, 513–521.
McDonald LC, Chen MT, Lauderdale TL, Ho M (2001). The use of antibiotics critical to human medicine in food-producing animals in Taiwan. Journal of Microbiology, Immunology, and Infection = Wei mian yu gan ran za zhi 34, 97–102
Mellon, M., Benbrook, C., & Benbrook, K. L. (2001). Hogging it: estimates of antimicrobial abuse in livestock (p. 109). Cambridge: Union of Concerned Scientists.
Mohapatra, H., Mohapatra, S. S., Mantri, C. K., Colwell, R. R., & Singh, D. V. (2008). Vibrio cholerae non-O1, non-O139 strains isolated before 1992 from Varanasi, India are multiple drug resistant, contain intSXT, dfr18 and aadA5 genes. Environmental Microbiology, 10, 866–873.
Ng, L. K., Martin, I., Alfa, M., & Mulvey, M. (2001). Multiplex PCR for the detection of tetracycline resistant genes. Molecular and Cellular Probes, 15, 209–215.
Peak, N., Knapp, C. W., Yang, R. K., Hanfelt, M. M., Smith, M. S., Aga, D. S., & Graham, D. W. (2007). Abundance of six tetracycline resistance genes in wastewater lagoons at cattle feedlots with different antibiotic use strategies. Environmental Microbiology, 9, 143–151.
Read, A. F., & Huijben, S. (2009). Evolutionary biology and the avoidance of antimicrobial resistance. Evolutionary Applications, 2, 40–51.
Sandvang, D. (1999). Novel streptomycin and spectinomycin resistance gene as a gene cassette within a class 1 integron isolated from Escherichia coli. Antimicrobial Agents and Chemotherapy, 43, 3036–3038.
Schwartz, T., Kohnen, W., Jansen, B., & Obst, U. (2003). Detection of antibiotic-resistant bacteria and their resistance genes in wastewater, surface water, and drinking water biofilms. FEMS Microbiology Ecology, 43, 325–335.
Stefani, S., Chung, D. R., Lindsay, J. A., Friedrich, A. W., Kearns, A. M., Westh, H., & MacKenzie, F. M. (2012). Meticillin-resistant Staphylococcus aureus (MRSA): global epidemiology and harmonisation of typing methods. International Journal of Antimicrobial Agents, 39, 273–282.
Tao, C. W., Hsu, B. M., Ji, W. T., Hsu, T. K., Kao, P. M., Hsu, C. P., Shen, S. M., Shen, T. Y., Wang, T. J., & Huang, Y. L. (2014). Evaluation of five antibiotic resistance genes in wastewater treatment systems of swine farms by real-time PCR. Science of the Total Environment, 496, 116–121.
Tolba, S., Egan, S., Kallifidas, D., & Wellington, E. M. H. (2002). Distribution of streptomycin resistance and biosynthesis genes in streptomycetes recovered from different soil sites. FEMS Microbiology Ecology, 42, 269–276.
Water Resources Management and Policy Research Center TU, Taiwan (2014) http://www.water.tku.edu.tw/. Accessed December 1, 2013.
Wegener, H. C., Aarestrup, F. M., Jensen, L. B., Hammerum, A. M., & Bager, F. (1999). Use of antimicrobial growth promoters in food animals and Enterococcus faecium resistance to therapeutic antimicrobial drugs in Europe. Emerging Infectious Diseases, 5, 329–335.
Author information
Authors and Affiliations
Corresponding author
Additional information
Wen-Tsai Ji and Tien-Yu Chang have equal contribution to the first author.
Rights and permissions
About this article
Cite this article
Hsu, CY., Hsu, BM., Ji, WT. et al. A Potential Association Between Antibiotic Abuse and Existence of Related Resistance Genes in Different Aquatic Environments. Water Air Soil Pollut 226, 2235 (2015). https://doi.org/10.1007/s11270-014-2235-z
Received:
Accepted:
Published:
DOI: https://doi.org/10.1007/s11270-014-2235-z