Salmon aquaculture and antimicrobial resistance in the marine environment

PLoS ONE

Volumn 7, Issue 8, 2012, Pages

  Buschmann, Alejandro H ^a   Tomova, Alexandra ^b   López, Alejandra ^a   Maldonado, Miguel A ^a   Henríquez, Luis A ^a   Ivanova, Larisa ^b   Moy, Fred ^b   Godfrey, Henry P ^b   Cabello, Felipe C ^b  

^a UNIVERSIDAD DE LOS LAGOS   (Chile)

^b NEW YORK MEDICAL COLLEGE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

DNA 16S; FLORFENICOL; FLUMEQUINE; OXOLINIC ACID; OXYTETRACYCLINE; QUINOLINE DERIVED ANTIINFECTIVE AGENT; RNA 16S;

ANTIBIOTIC RESISTANCE; AQUACULTURE; ARTHROBACTER; ARTICLE; BACTERIUM CULTURE; BACTERIUM IDENTIFICATION; BACTERIUM ISOLATE; CHILE; CONTROLLED STUDY; GENE IDENTIFICATION; GEOGRAPHIC DISTRIBUTION; MARINE ENVIRONMENT; NONHUMAN; PSEUDOALTEROMONAS; SALMON; SEDIMENT; SPECIES IDENTIFICATION; SPOROSARCINA; VIBRIO;

ANIMALS; ANTI-INFECTIVE AGENTS; AQUACULTURE; BACTERIA; BIODIVERSITY; CHILE; ENVIRONMENTAL MONITORING; GEOLOGIC SEDIMENTS; OXOLINIC ACID; OXYTETRACYCLINE; PLASMIDS; RNA, RIBOSOMAL, 16S; SALMON; THIAMPHENICOL; WATER POLLUTANTS, CHEMICAL;

EID: 84864834762     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0042724     Document Type: Article

References (89)

1. Costa-Pierce BA, (2010) Sustainable ecological aquaculture systems: the need for a new social contract for aquaculture development. Mar Technol Soc J 44: 88-112.
2. Tett P (2008) Fish farm wastes in the ecosystem. In: Holmer M, Black K, Duarte CM, Marbà N, Karakassis I, editors. Aquaculture in the Ecosystem. Berlin Heidelberg, German: Springer-Verlag. 1-46.
3. Moore PR, Evenson A, Luckey TD, McCoy E, Elvehjemande CA, et al. (1946) Use of sulfasuxidine, streptothricin, and streptomycin in nutritional studies with the chick. J Biol Chem 165: 437-441.
4. Grumbles LC, Delaplane JP, Higgins TC, (1948) Sulfaquinoxaline in the control of Eimeria tenella and Eimeria necatrix in chickens on a commercial broiler farm. Science 107: 196.
5. Jukes TH, Stokstad ELR, Taylor RR, Cunha TJ, Edwards HM, et al. (1950) Growth promoting effect of aureomycin on pigs. Arch Biochem 26: 324-330.
6. Marshall BM, Levy SB, (2011) Food animals and antimicrobials: impacts on human health. Clin Microbiol Rev 24: 718-733.
7. Barnes EM, (1958) The effect of antibiotic supplements on the faecal streptococci (Lancefield group D) of poultry. Br Vet J 114: 333-344.
8. Dibner JJ, Richards JD, (2005) Antibiotic growth promoters in agriculture: history and mode of action. Poult Sci 84: 634-643.
9. Castanon JI, (2007) History of the use of antibiotic as growth promoters in European poultry feeds. Poult Sci 86: 2466-2471.
10. Marshall BM, Levy SB Food animals and antimicrobials: impacts on human health. Clin Microbiol Rev 24: 718-733.
11. Wegener HC, (2003) Antibiotics in animal feed and their role in resistance development. Curr Opin Microbiol 6: 439-445.
12. Aarestrup FM, Duran CO, Burch DGS, (2008) Antimicrobial resistance in swine production. Anim Health Res Rev 9: 135-148.
13. Aarestrup FM, Jensen VF, Emborg HD, Jacobsen E, Wegener HC, (2010) Changes in the use of antimicrobials and the effects on productivity of swine farms in Denmark. Am J Vet Res 71: 726-733.
14. Asche F, Roll KH, Tveterås S (2008) Future trends in aquaculture: productivity growth and increased production. In: Holmer M, Black K, Duarte CM, Marba' N, Karakassis I, editors. Aquaculture in the Ecosystem: Springer. 271-292.
15. Barton JR, Fløysand A (2010) The political ecology of Chilean salmon aquaculture, 1982-2010. A trajectory from economic development to global sustainability Global Environ Change 739-752.
16. Bravo S, Midtlyng PJ, (2007) The use of fish vaccines in the Chilean salmon industry 1999-2003. Aquaculture 270: 36-42.
17. Bustos PA, Young ND, Rozas MA, Bohle HM, Ildefonso RS, et al. (2011) Amoebic gill disease (AGD) in Atlantic salmon (Salmo salar) farmed in Chile. Aquaculture 110: 281-288.
18. Heuer OE, Kruse H, Grave K, Collignon P, Karunasagar I, et al. (2009) Human health consequences of use of antimicrobial agents in aquaculture. Clin Infect Dis 49: 1248-1253.
19. Burridge L, Weis JS, Cabello F, Pizarro J, Bostick K, (2010) Chemical use in salmon aquaculture: A review of current practices and possible environmental effects. Aquaculture 306: 7-23.
20. Buschmann AH, Cabello F, Young K, Carvajal J, Varela DA, et al. (2009) Salmon aquaculture and coastal ecosystem health in Chile: analysis of regulations, environmental impacts and bioremediation systems. Ocean Coast Manage 52: 243-249.
21. Buschmann AH, Riquelme VA, Hernández-González MC, Varela DA, Jiménez JE, et al. (2006) A review of the impacts of salmon farming on marine coastal ecosystems in the southeast Pacific. ICES J Mar Sci 63: 1338-1345.
22. Sørum H (2006) Antimicrobial drug resistance in fish pathogens. In: Aarestrup FM, editor. Antimicrobial Resistance in Bacteria of Animal Origin. Washington, DC: ASM Press. 213-238.
23. Millanao BA, Barrientos HM, Gomez CC, Tomova A, Buschmann A, et al. (2011) Uso inadecuado y excesivo de antibióticos: salud pública y salmonicultura en Chile.[Injudicious and excessive use of antibiotics: public health and salmon aquaculture in Chile]. Rev Med Chil 139: 107-118.
24. Barrientos M (2006) Estudio cualitativo y cuantitativo de las quinolonas y fluoroquinolonas importadas y autorizadas para uso y disposicion en medicina y en veterinaria en Chile, en el periodo 2002-2005. Consideraciones sobre su impacto para la salud pública y el medio ambiente. [Qualitative and quantitative study of quinolines and fluorquinolines imported and authorized for veterinary and medical use in Chile, 2002-2005. Considerations of its impact on public health and the environment]. Universidad Austral de Chile, Valdivia, Chile. Tesis Electrónicas UACh website. Available: http://cybertesis.uach.cl/tesis/uach/2006/fcb2751e/doc/fcb2751e.pdf. Accessed 2012 Jul 13. 122 p.
25. Millanao A (2002) Estudio cualitativo y cuantitativo de las quinolonas y fluoroquinolonas importadas y autorizadas para uso y disposicion en medicina y en veterinaria en Chile, en el periodo 1998-2001. Consideraciones sobre su impacto para la salud pública y el medio ambiente. [Qualitative and quantitative study of quinolines and fluorquinolines imported and authorized for medical and veterinary use and disposition in Chile, 1998-2001. Considerations of its impact on public health and the envrionment]. Universidad Austral de Chile, Valdivia, Chile. Tesis Electrónicas UACh website. Available: http://cybertesis.uach.cl/tesis/uach/2002/fcm645e/doc/fcm645e.pdf. Accessed 2012 Jul 13. 121.
26. Capone DG, Weston DP, Miller V, Shoemaker C, (1996) Antibacterial residues in marine sediments and invertebrates following chemotherapy in aquaculture. Aquaculture 145: 55-75.
27. Hektoen H, Berge JA, Hormazabal V, Yndestad M, (1995) Persistence of antibacterial agents in marine sediments. Aquaculture 133: 175-184.
28. Herwig RP, Gray JP, Weston DP, (1997) Antibacterial resistant bacteria in superficial sediments near salmon net-cage farms in Puget Sound, Washington. Aquaculture 149: 163-283.
29. Coyne R, Smith P, Moriarty C, (2001) The fate of oxytetracycline in the marine environment of a salmon cage farm. Mar Environ Health 3: 1-24.
30. Holten Lützhøft H-C, Halling-Sørensen B, Jørgensen SE, (1999) Algal toxicity of antibacterial agents applied in Danish fish farming. Arch Environ Contam Toxicol 436: 1171-1175.
31. DePaola A, Peeler JT, Rodrick GE, (1995) Effect of oxytetracycline-medicated feed on antibiotic resistance of gram-negative bacteria in catfish ponds. Appl Environ Microbiol 61: 2335-2340.
32. Cattoir V, Poirel L, Aubert C, Soussy CJ, Nordmann P, (2008) Unexpected occurrence of plasmid-mediated quinolone resistance determinants in environmental Aeromonas spp. Emerg Infect Dis 14: 231-237.
33. Cattoir V, Poirel L, Mazel D, Soussy CJ, Nordmann P, (2007) Vibrio splendidus as the source of plasmid-mediated QnrS-like quinolone resistance determinants. Antimicrob Agents Chemother 51: 2650-2651.
34. Pan JC, Ye R, Wang HQ, Xiang HQ, Zhang W, et al. (2008) Vibrio cholerae O139 multiple-drug resistance mediated by Yersinia pestis pIP1202-like conjugative plasmids. Antimicrob Agents Chemother 52: 3829-3836.
35. Rhodes G, Huys G, Swings J, McGann P, Hiney M, et al. (2000) Distribution of oxytetracycline resistance plasmids between aeromonads in hospital and aquaculture environments: implication of Tn1721 in dissemination of the tetracycline resistance determinant Tet A. Appl Environ Microbiol 66: 3883-3890.
36. Welch TJ, Fricke WF, McDermott PF, White DG, Rosso ML, et al. (2007) Multiple antimicrobial resistance in plague: an emerging public health risk. PLoS One 2: e309.
37. Baquero F, Martinez JL, Canton R, (2008) Antibiotics and antibiotic resistance in water environments. Curr Opin Biotechnol 19: 260-265.
38. Schmidt AS, Bruun MS, Dalsgaard I, Pedersen K, Larsen JL, (2000) Occurrence of antimicrobial resistance in fish-pathogenic and environmental bacteria associated with four Danish rainbow trout farms. Appl Environ Microbiol 66: 4908-4915.
39. Saga T, Kaku M, Onodera Y, Yamachika S, Sato K, et al. (2005) Vibrio parahaemolyticus chromosomal qnr homologue VPA0095: demonstration by transformation with a mutated gene of its potential to reduce quinolone susceptibility in Escherichia coli. Antimicrob Agents Chemother 49: 2144-2145.
40. Strahilevitz J, Jacoby GA, Hooper DC, Robicsek A, (2009) Plasmid-mediated quinolone resistance: a multifaceted threat. Clin Microbiol Rev 22: 664-689.
41. Jacobs L, Chenia HY, (2007) Characterization of integrons and tetracycline resistance determinants in Aeromonas spp. isolated from South African aquaculture systems. Int J Food Microbiol 114: 295-306.
42. Rosewarne CP, Pettigrove V, Stokes HW, Parsons YM, (2010) Class 1 integrons in benthic bacterial communities: abundance, association with Tn402-like transposition modules and evidence for coselection with heavy-metal resistance. FEMS Microbiol Ecol 72: 35-46.
43. 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.
44. Sørum H, L'Abee-Lund TM, Solberg A, Wold A, (2003) Integron-containing IncU R plasmids pRAS1 and pAr-32 from the fish pathogen Aeromonas salmonicida. Antimicrob Agents Chemother 47: 1285-1290.
45. Xu H, Davies J, Miao V, (2007) Molecular characterization of class 3 integrons from Delftia spp. J Bacteriol 189: 6276-6283.
46. Miranda CD, Zemelman R, (2001) Antibiotic resistant bacteria in fish from the Concepcion Bay, Chile. Mar Pollut Bull 42: 1096-1102.
47. Silva J, Zemelman R, Mandoca MA, Henriquez M, Merino C, et al. (1987) Antibiotic-resistant gram negative bacilli isolated from sea water and shellfish. Possible epidemiological implications. Rev Latinoam Microbiol 29: 165-169.
48. Bissett A, Bowman J, Burke C, (2006) Bacterial diversity in organically-enriched fish farm sediments. FEMS Microbiol Ecol 55: 48-56.
49. Navarro N, Leakey RJG, Black KD, (2008) Effect of salmon cage aquaculture on the pelagic environment of temperate coastal waters: seasonal changes in nutrients and microbial community. Mar Ecol Prog Ser 361: 47-58.
50. Kerry J, Coyne R, Gilroy D, Hiney M, Smith P, (1996) Spatial distribution of oxytetracycline and elevated frequencies of oxytetracycline resistance in sediments beneath a marine salmon farm following oxytetracycline therapy. Aquaculture 145: 31-39.
51. Smith P, (1996) Is sediment deposition the dominant fate of oxytetracycline used in marine salmonid farms: a review of available evidence. Aquaculture 146: 157-169.
52. Weston DP (2000) Ecological effects of the use of chemicals in aquaculture. In: Arthur JR, Lavilla-Pitogo CR, Subasinghe RP, editors. Use of Chemicals in Aquaculture in Asia: Proceedings of the Meeting on the Use of Chemicals in Aquaculture in Asia 20-22 May 1996, Tigbauan, Iloilo, Philippines. Tigbauan, Iloilo, Philippines: Aquaculture Department, Southeast Asian Fisheries Development Center. 20-30.
53. Council NR (2010) The Prevention and Treatment of Missing Data in Clinical Trials. Washington, D.C.: National Academies Press. 162 p.
54. Pepe MS (2003) The Statistical Evaluation of Medical Tests for Classificaiton and Prediction. Oxford Statistical Science Series 28 Oxford University Press. 318 p.
55. Kapetanaki M, Kerry J, Hiney M, O'Brien C, Coyne R, et al. (1995) Emergence, in oxytetracycline-free marine mesocosms, of microorganisms capable of colony formation on oxytetracycline-containing media. Aquaculture 134: 227-236.
56. Smith P, Hiney MP, Samuelsen OB, (1994) Bacterial resistance to antimicrobial agents used in fish farming: A critical evaluation of method and meaning. Annu Rev Fish Dis 4: 273-313.
57. Smith P, (2008) Antimicrobial resistance in aquaculture. Rev Sci Tech 27: 243-264.
58. Akinbowale OL, Peng H, Grant P, Barton MD, (2007) Antibiotic and heavy metal resistance in motile aeromonads and pseudomonads from rainbow trout (Oncorhynchus mykiss) farms in Australia. Int J Antimicrob Agents 30: 177-182.
59. McIntosh D, Cunningham M, Ji B, Fekete FA, Parry EM, et al. (2008) Transferable, multiple antibiotic and mercury resistance in Atlantic Canadian isolates of Aeromonas salmonicida subsp. salmonicida is associated with carriage of an IncA/C plasmid similar to the Salmonella enterica plasmid pSN254. J Antimicrob Chemother 61: 1221-1228.
60. Björklund H, Bondestam J, Bylund G, (1990) Residues of oxytetracycline in wild fish and sediments from fish farms. Aquaculture 86: 359-367.
61. Samuelsen OB, Torsvik V, Ervik A, (1992) Long-range changes in oxytetracycline concentration and bacterial resistance toward oxytetracycline in a fish farm sediment after medication. Sci Total Environ 114: 25-36.
62. D'Costa VM, King CE, Kalan L, Morar M, Sung WW, et al. (2011) Antibiotic resistance is ancient. Nature 477: 457-461.
63. Robicsek A, Strahilevitz J, Jacoby GA, Macielag M, Abbanat D, et al. (2006) Fluoroquinolone-modifying enzyme: a new adaptation of a common aminoglycoside acetyltransferase. Nat Med 12: 83-88.
64. Chopra I, Roberts M, (2001) Tetracycline antibiotics: mode of action, applications, molecular biology, and epidemiology of bacterial resistance. Microbiol Mol Biol Rev 65: 232-260.
65. Miranda CD, Kehrenberg C, Ulep C, Schwarz S, Roberts MC, (2003) Diversity of tetracycline resistance genes in bacteria from Chilean salmon farms. Antimicrob Agents Chemother 47: 883-888.
66. Singer RS, Patterson SK, Meier AE, Gibson JK, Lee HL, et al. (2004) Relationship between phenotypic and genotypic florfenicol resistance in Escherichia coli. Antimicrob Agents Chemother 48: 4047-4049.
67. Canton R, (2009) Antibiotic resistance genes from the environment: a perspective through newly identified antibiotic resistance mechanisms in the clinical setting. Clin Microbiol Infect 15 (Suppl 1): 20-25.
68. Hastings PJ, Rosenberg SM, Slack A, (2004) Antibiotic-induced lateral transfer of antibiotic resistance. Trends Microbiol 12: 401-404.
69. Baquero F, (2009) Environmental stress and evolvability in microbial systems. Clin Microbiol Infect 15 (Suppl 1): 5-10.
70. Dorr T, Lewis K, Vulic M, (2009) SOS response induces persistence to fluoroquinolones in Escherichia coli. PLoS Genet 5: e1000760.
71. Fortt ZA, Cabello CF, Buschmann RA, (2007) Residues of tetracycline and quinolones in wild fish living around a salmon aquaculture center in Chile. Rev Chilena Infectol 24: 14-18.
72. Samuelsen OB, Lunestad BT, Husevåg B, Hølleland T, Ervik A, (1992) Residues of oxolinic acid in wild fauna following medication in fish farms. Dis Aq Org 12: 111-119.
73. Cabello FC, (2006) Heavy use of prophylactic antibiotics in aquaculture: a growing problem for human and animal health and for the environment. Environ Microbiol 8: 1137-1144.
74. Carroll ML, Cochrane S, Fieler R, Velvin R, White P, (2003) Organic enrichment of sediments from salmon farming in Norway: environmental factors, management practices, and monitoring techniques. Aquaculture 226: 165-180.
75. Soto D, Norambuena F, (2004) Evaluation of salmon farming effects on marine systems in the inner seas of southern Chile: a large-scale mensurative experiment. J Appl Ichthyol 20: 493-501.
76. Pouliquen H, Gouelo D, Larhantec M, Pilet N, Pinault L, (1997) Rapid and simple determination of oxolinic acid and oxytetracycline in the shell of the blue mussel (Mytilus edulis) by high-performance liquid chromatography. J Chromatogr B Biomed Sci Appl 702: 157-162.
77. Sørensen LK, Hansen H, (2001) Determination of oxolinic acid in marine sediment by HPLC with fluorescence detection. J Liq Chromat Rel Tech 24: 2469-2476.
78. Cavaco LM, Hasman H, Xia S, Aarestrup FM, (2009) qnrD, a novel gene conferring transferable quinolone resistance in Salmonella enterica serovar Kentucky and Bovismorbificans strains of human origin. Antimicrob Agents Chemother 53: 603-608.
79. Robicsek A, Strahilevitz J, Sahm DF, Jacoby GA, Hooper DC, (2006) qnr prevalence in ceftazidime-resistant Enterobacteriaceae isolates from the United States. Antimicrob Agents Chemother 50: 2872-2874.
80. Wang M, Guo Q, Xu X, Wang X, Ye X, et al. (2009) New plasmid-mediated quinolone resistance gene, qnrC, found in a clinical isolate of Proteus mirabilis. Antimicrob Agents Chemother 53: 1892-1897.
81. Kim HB, Wang M, Park CH, Kim EC, Jacoby GA, et al. (2009) oqxAB encoding a multidrug efflux pump in human clinical isolates of Enterobacteriaceae. Antimicrob Agents Chemother 53: 3582-3584.
82. Minarini LA, Poirel L, Cattoir V, Darini AL, Nordmann P, (2008) Plasmid-mediated quinolone resistance determinants among enterobacterial isolates from outpatients in Brazil. J Antimicrob Chemother 62: 474-478.
83. Ng LK, Martin I, Alfa M, Mulvey M, (2001) Multiplex PCR for the detection of tetracycline resistant genes. Mol Cell Probes 15: 209-215.
84. Bolton LF, Kelley LC, Lee MD, Fedorka-Cray PJ, Maurer JJ, (1999) Detection of multidrug-resistant Salmonella enterica serotype Typhimurium DT104 based on a gene which confers cross-resistance to florfenicol and chloramphenicol. J Clin Microbiol 37: 1348-1351.
85. Bey BS, Fichot EB, Dayama G, Decho AW, Norman RS, (2010) Extraction of high molecular weight DNA from microbial mats. Biotechniques 49: 631-640.
86. Miller DN, Bryant JE, Madsen EL, Ghiorse WC, (1999) Evaluation and optimization of DNA extraction and purification procedures for soil and sediment samples. Appl Environ Microbiol 65: 4715-4724.
87. Griffen AL, Beall CJ, Firestone ND, Gross EL, Difranco JM, et al. (2011) CORE: a phylogenetically-curated 16S rDNA database of the core oral microbiome. PLoS One 6: e19051.
88. Weisburg WG, Barns SM, Pelletier DA, Lane DJ, (1991) 16S ribosomal DNA amplification for phylogenetic study. J Bacteriol 173: 697-703.
89. Conover WJ, Iman RL, (1981) Rank transformations as a bridge between parametric and nonparametric statistics. Am Stat 35: 124-133.