Abstract
In order to investigate the influence of a duckweed aquaculture based hospital sewage water recycling plant on the prevalence and dissemination of antibiotic resistance, we made use of an existing collection of 1,315 Aeromonas isolates that were previously typed by the biochemical fingerprinting PhP-AE system. In these treatment plant, hospital raw sewage water is first collected in a settlement pond (referred to as sewage water in this study) and is then transferred to a lagoon, where the duckweed (Lemnaceae) is grown (referred to as lagoon). The duckweed is harvested and used as feed for the fish in a separate pond (referred to as fish pond). From this collection, representatives of 288 PhP types were subjected to antibiotic susceptibility testing for eight antimicrobials by broth microdilution method. The overall resistance rates among Aeromonas isolates from the treatment plant were highest for ampicillin (87%) and erythromycin (79%) followed by cephalothin (58%), nalidixic acid (52%), streptomycin (51%), tetracycline (31%), chloramphenicol (13%) and gentamicin (8%). A significantly lower prevalence of antibiotic resistance was found in Aeromonas from environmental control water, patient stool samples, duckweed and fish compared to sewage water isolates. The prevalence of resistance in the sewage water was not significantly reduced compared to the lagoon water and fish pond. Throughout the treatment system, the frequencies of resistant strains were found to diminish during the sewage water purification process, i.e. in the lagoon where sewage water is used to grow the duckweed. However, the frequency of resistant strains again increased in the fish pond where sewage grown duckweed is used for aquaculture. Among the selected isolates, two multiresistant clonal groups of Aeromonas caviae HG4 were identified that exhibited indistinguishable PhP and amplified fragment length polymorphism fingerprints and shared a common plasmid of approximately 5 kb. Representatives of both groups were recovered from almost every part of the sewage treatment plant but not in the control ponds nor in human samples, which suggests that specific multiresistant Aeromonas clones are able to persist and spread throughout the entire purification process.
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References
Alaerts GJ, Rahman M, Kilderman P (1996) Performance analysis of a full scale duckweed covered lagoon. Water Res 30:843–852. doi:10.1016/0043-1354(95)00234-0
Bager F, Madsen M, Christensen J, Aarestrup FM (1997) Avoparcin used as a growth promoter is associated with the occurrence of vancomycin-resistant Enterococcus faecium on Danish poultry and pig farms. Prev Vet Med 31:95–112. doi:10.1016/S0167-5877(96)01119-1
Bates J, Jordens JZ, Griffiths DT (1994) Farm animals as a putative reservoir for vancomycin-resistant enterococcal infection in man. J Antimicrob Chemother 34:507–514. doi:10.1093/jac/34.4.507
Bogaard AE, Stobberingh EE (2000) Epidemiology of resistance to antibiotics links between animals and humans. Int J Antimicrob Agents 14:327–335. doi:10.1016/S0924-8579(00)00145-X
Calvert N, Stewart WC, Reilly WJ (1998) Salmonella typhimurium DT104 infection in people and animals in Scotland: a collaborative epidemiological study 1993–96. Vet Rec 143:351–354
Carr RM, Blumenthal UJ, Mara DD (2004) Guidelines for the safe use of wastewater in agriculture: revisiting WHO guidelines. Water Sci Technol 50:31–38
Chee-Sanford JC, Aminov RI, Krapac IJ, Garrigues-Jeanjean N, Mackie RI (2001) Occurrence and diversity of tetracycline resistance genes in lagoons and groundwater underlying two swine poduction facilities. Appl Environ Microbiol 67:1494–1502. doi:10.1128/AEM.67.4.1494-1502.2001
Davison J (1999) Genetic exchange between bacteria in the environment. Plasmid 42:73–91. doi:10.1006/plas.1999.1421
Dinesh SD, Grundmann H, Pitt TL, Romling U (2003) European-wide distribution of Pseudomonas aeruginosa clone C. Clin Microbiol Infect 9:1228–1233. doi:10.1111/j.1469-0691.2003.00793.x
Goni-Urriza M, Capdepuy M, Arpin C, Raymond N, Caumette P, Quentin C (2000a) Impact of an urban effluent on antibiotic resistance of riverine enterobacteriaceae and Aeromonas spp. Appl Environ Microbiol 66:125–132
Goni-Urriza M, Pineau L, Capdepuy M, Roques C, Caumette P, Quentin C (2000b) Antimicrobial resistance of mesophilic Aeromonas spp. isolated from two European rivers. J Antimicrob Chemother 46:297–301. doi:10.1093/jac/46.2.297
Goodyear KL (2002) Veterinary surveillance for antimicrobial resistance. J Antimicrob Chemother 50:612–614. doi:10.1093/jac/dkf154
Guardabassi L, Petersen A, Olsen JE, Dalsgaard A (1998) Antibiotic resistance in Acinetobacter spp. isolated from sewers receiving waste effluent from a hospital and a pharmaceutical plant. Appl Environ Microbiol 64:3499–3502
Halling-Sorensen B, Nors Nielsen S, Lanzky PF, Ingerslev F, Holten Lutzhoft HC, Jorgensen SE (1998) Occurrence, fate and effects of pharmaceutical substances in the environment—A review. Chemosphere 36:357–393. doi:10.1016/S0045-6535(97)00354-8
Haustein AT, Gilman WR, Skillicorn PW (1990) Duckweed, a useful strategy for feeding chickens in Third World countries: performance of layers fed with sewage-grown Lemnaceae. Poult Sci 69:1835–1844
Havelaar AH, During M, Versteegh JF (1987) Ampicillin-dextrin agar medium for the enumeration of Aeromonas species in water by membrane filtration. J Appl Bacteriol 279:87
Homsi ZJ, Reed SC (1988) The use of duckweed for wastewater treatment. J WPCF 60:1253–1258
Huys G, Avncanneyt M, Coopman R, Jansson P, Falsen E, Altwegg M, Kersters K (1994) Cellulor fatty acid, composition as a chemotaxonomic marker for the identification of phenospecies and the hybridization groups in the genus Aeromonas. Int J Syst Bacteriol 44:651–658
Huys G, Coopman R, Janssen P, Kersters K (1996) High resolution genotypic analysis of the genus Aeromonas by AFLP fingerprinting. Int J Syst Bacteriol 46:572–580
Iversen A, Kuhn I, Rahman M, Franklin A, Burman LG, Olsson-Liljequist B, Torell E, Mollby R (2004) Evidence for transmission between humans and the environment of a nosocomial strain of Enterococcus faecium. Environ Microbiol 6:55–59. doi:10.1046/j.1462-2920.2003.00534.x
Kampfer P, Christmann C, Swings J, Huys G (1999) In vitro susceptibilities of Aeromonas genomic species to 69 antimicrobial agents. Syst Appl Microbiol 22:662–669
Mazel D, Davies J (1999) Antibiotic resistance in microbes. Cell Mol Life Sci 56:742–754. doi:10.1007/s000180050021
Möllby R, Kühn I, Katouli M (1993) Computerized biochemical fingerprinting. A new tool for typing of bacteria. Rev Med Microbiol 4:231–241
Petersen A, Andersen JS, Kaewmak T, Somsiri T, Dalsgaard A (2002) Impact of integrated fish farming on antimicrobial resistance in a pond environment. Appl Environ Microbiol 68:6036–6042. doi:10.1128/AEM.68.12.6036-6042.2002
Rahman M, Kuhn I, Rahman M, Olsson-Liljequist B, Mollby R (2004) Evaluation of a scanner-assisted colorimetric MIC method for susceptibility testing of gram-negative fermentative bacteria. Appl Environ Microbiol 70:2398–2403. doi:10.1128/AEM.70.4.2398-2403.2004
Rahman M, Huys G, Rahman M, Albert MJ, Kuhn I, Mollby R (2007) Persistence, transmission, and virulence characteristics of Aeromonas strains in a duckweed aquaculture-based hospital sewage water recycling plant in Bangladesh. Appl Environ Microbiol 73:1444–1451. doi:10.1128/AEM.01901-06
Sambrook J, Fritsch EF, Maniatis T (1989) Molecular cloning: a laboratory manual, vol 2. Cold Spring Harbor Laboratory Press, Cold Spring Harbor
Schmidt AS, Bruun MS, Dalsgaard I, Larsen JL (2001) Incidence, distribution, and spread of Tetracycline resistance determinants and integron-associated antibiotic resistance genes among motile Aeromonads from a fish farming environment. Appl Environ Microbiol 67:5675–5682. doi:10.1128/AEM.67.12.5675-5682.2001
Son R, Rusul G, Sahilah AM, Zainuri A, Raha AR, Salmah I (1997) Antibiotic resistance and plasmid profile of Aeromonas hydrophila isolates from cultured fish, Telapia (Telapia mossambica). Lett Appl Microbiol 24:479–482. doi:10.1046/j.1472-765X.1997.00156.x
Tennstedt T, Szczepanowski R, Braun S, Puhler A, Schluter A (2003) Occurrence of integron-associated resistance gene cassettes located on antibiotic resistance plasmids isolated from a wastewater treatment plant. FEMS Microbiol Ecol 45:239–252. doi:10.1016/S0168-6496(03)00164-8
Wegener HC, Aarestrup FM, Jensen LB, Hammerum AM, Bager F (1999) Use of antimicrobial growth promoters in food animals and Enterococcus faecium resistance to therapeutic antimicrobial drugs in Europe. Emerg Infect Dis 5:329–335
Acknowledgments
This work was supported by SIDA/SAREC grant 1999-255 for PhD fellowship for Mokhlasur Rahman and the Karolinska Institutet fund. We thank G. B. Nair at the International Centre for Diarrheal Disease Research in Bangladesh for laboratory support; Prism Bangladesh Ltd. staffs and Kumudini Hospital staffs for sampling supports. Geert Huys is a postdoctoral fellow of the Fund for Scientific Research—Flanders (Belgium) (F·W.O.-Vlaanderen).
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Rahman, M., Huys, G., Kühn, I. et al. Prevalence and transmission of antimicrobial resistance among Aeromonas populations from a duckweed aquaculture based hospital sewage water recycling system in Bangladesh. Antonie van Leeuwenhoek 96, 313–321 (2009). https://doi.org/10.1007/s10482-009-9348-1
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DOI: https://doi.org/10.1007/s10482-009-9348-1