Skip to main content

Advertisement

Log in

Increase in Antimicrobial Resistance in Bacteria Isolated from Stranded Marine Mammals of the Northwest Atlantic

  • Original Contribution
  • Published:
EcoHealth Aims and scope Submit manuscript

Abstract

Studies on marine mammals can inform our understanding of the environmental health of the ocean. To evaluate the potential for changes in antimicrobial resistance, we analyzed a database spanning 2004–2010 that consisted of bacterial isolate identity and antimicrobial sensitivity for stranded pinnipeds in the Northwest Atlantic. Samples (n = 170) from treated animals yielded 310 bacterial isolates representing 24 taxa. We evaluated changes in antimicrobial class resistance from 2004 to 2010 for eight taxa. Escherichia coli displayed a significant increase in resistance to several antimicrobial classes. Other taxa displayed significant increases in resistance to aminoglycosides, and/or fluoroquinolones. In addition, we observed a significant increase in multiple antimicrobial resistance in cultures from untreated animals. These results demonstrate an increase in resistance among common bacterial pathogens of marine mammals over a time span of 6 years.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Figure 1

Similar content being viewed by others

References

  • Allen HK, Donato J, Wang HH, Cloud-Hansen KA, Davies J, Handelsman J (2010) Call of the wild: antibiotic resistance genes in natural environments. Nature Reviews Microbiology 8:251-259

    Article  PubMed  CAS  Google Scholar 

  • Baker-Austin C, Wright MS, Stepanauskas R, McArthur JV (2006) Co-selection of antibiotic and metal resistance. Trends in Microbiology 14:176-182

    Article  PubMed  CAS  Google Scholar 

  • Bartram J, Rees G (2000) Monitoring bathing waters—a practical guide to the design and implementation of assessments and monitoring programmes. World Health Organization ISBN 0-419-24390-1

  • Bauer SAW, Kirby WM, Sherris JC, Turck M (1966) Antibiotic susceptibility testing by standardized single disc method. American Journal of Clinical Pathology 45:493-498.

    PubMed  CAS  Google Scholar 

  • Bogomolni AL, Gast RJ, Ellis JC, Dennett M, Pugliares KR, Lentell, BJ, et al. (2008) Victims of vectors: a survey of marine vertebrate zoonoses from coastal waters of the Northwest Atlantic. Diseases of Aquatic Organisms 81:13-38

    Article  PubMed  Google Scholar 

  • Chitanand MP, Kadam TA, Gyananath G, Totewad ND, Balhal DK (2010) Multiple antibiotic resistance indexing of coliforms to identify high risk contamination sites in aquatic environment. Indian Journal of Microbiology 50:216-220

    Article  PubMed  CAS  Google Scholar 

  • Clinical and Laboratory Standards Institute (2009) Performance standards for antimicrobial disk susceptibility tests; approved standard. Wayne, PA

  • Diaz RJ, Rosenberg R (2008) Spreading dead zones and consequences for marine ecosystems. Science 321:926-929

    Article  PubMed  CAS  Google Scholar 

  • Durante-Mangoni E, Grammatikos A, Utili R, Falagas ME (2009) Do we still need the aminoglycosides? International Journal of Antimicrobial Agents 33:201-205

    Article  PubMed  CAS  Google Scholar 

  • Falagas ME, Grammatikos AP, Michalopoulos A (2008) Potential of old-generation antibiotics to address current need for new antibiotics. Expert Review of Anti-Infective Therapy 6:593-600

    Article  PubMed  Google Scholar 

  • Foti M, Giacopello C, Bottari T, Fisichella V, Rinaldo D, Mammina C (2009) Antibiotic resistance of gram negatives isolates from loggerhead sea turtles (Caretta caretta) in the central Mediterranean Sea. Marine Pollution Bulletin 58:1363-1366

    Article  PubMed  CAS  Google Scholar 

  • Gullberg E, Cao S, Berg OG, Ilbäck C, Sandegren L, Hughes D, et al. (2011) Selection of resistant bacteria and very low antibiotic concentrations. PLoS Pathogens 7:e1002158

    Article  PubMed  CAS  Google Scholar 

  • Johnson SP, Nolan S, Gulland FM (1998) Antimicrobial susceptibility of bacteria isolated from pinnipeds stranded in central and northern California. Journal of Zoo and Wildlife Medicine 29:288-294

    PubMed  CAS  Google Scholar 

  • Kahn LH, Kaplan B, Steele JH (2007) Confronting zoonoses through closer collaboration between medicine and veterinary medicine (as ‘One Medicine’). Veterinaria Italiana 43:5-19

    PubMed  Google Scholar 

  • Kelsey RH, Scott GI, Porter DE, Thompson B, Webster L (2003) Using multiple antibiotic resistance and land use characteristics to determine sources of fecal coliform bacterial pollution. Environmental Monitoring and Assessment 81:337-348

    Article  PubMed  Google Scholar 

  • Kemper N (2008) Veterinary antibiotics in the aquatic and terrestrial environment. Ecological Indicators 8: 1-13

    Article  CAS  Google Scholar 

  • Knapp CW, Dolfing J, Ehlert PA, Graham DW (2010) Evidence of increasing antibiotic resistance gene abundances in archived soils since 1940. Environmental Science & Technology 44:580-587

    Article  PubMed  CAS  Google Scholar 

  • Krumperman PH (1983) Multiple antibiotic resistance indexing of Escherichia coli to identify high-risk sources of fecal contamination of food. Applied and Environmental Microbiology 46:165-170

    PubMed  CAS  Google Scholar 

  • Lautenbach E, Larosa LA, Kasbekar N, Peng HP, Maniglia RJ, Fishman NO (2003) Fluoroquinolone utilization in the emergency departments of academic medical centers. Archives of Internal Medicine 163:601-605

    Article  PubMed  Google Scholar 

  • Linder JA, Huang ES, Steinman MA, Gonzales R, Stafford RS (2005) Fluoroquinolone prescribing in the United States: 1995 to 2002. The American Journal of Medicine 118:259-268

    Article  PubMed  Google Scholar 

  • Lockwood SK, Chovan JL, Gaydos JK (2006) Aerobic bacterial isolations from harbor seals (Phoca vitulina) stranded in Washington: 1992–2003. Journal of Zoo and Wildlife Medicine 37:281-291

    Article  PubMed  Google Scholar 

  • Martinez JL (2008) Antibiotics and antibiotic resistance genes in natural environments. Science 321:365-367

    Article  PubMed  CAS  Google Scholar 

  • Martinez JL (2009) Environmental pollution by antibiotics and by antibiotic resistance determinants. Environmental Pollution 157:2893-2902

    Article  PubMed  CAS  Google Scholar 

  • Nikaido H (1989) Outer membrane barrier as a mechanism of antimicrobial resistance. Antimicrobial Agents and Chemotherapy 33:1831-1836

    Article  PubMed  CAS  Google Scholar 

  • Poole, N (2001) Multidrug efflux pumps and antimicrobial resistance in Pseudomonas aeruginosa and related organisms. Journal of Molecular Microbiology and Biotechnology 3:255-264

    PubMed  CAS  Google Scholar 

  • Rabalais NN, Diaz RJ, Levin LA, Turner RE, Gilbert D, Zhang J (2010) Dynamics and distribution of natural and human-caused hypoxia. Biogeosciences 7: 585–619

    Article  CAS  Google Scholar 

  • Reddy ML, Dierauf LA, Gulland FMD (2001) Marine mammals as sentinels of ocean health. In: Marine Mammal Medicine, ed. Dierauf L and Gulland F, pp. 3-13. CRC Press, Boca Raton, FL

    Chapter  Google Scholar 

  • Rose JM, Gast RJ, Bogomolni A, Ellis JC, Lentell BJ, Touhey K, et al. (2009) Occurrence and patterns of antibiotic resistance in vertebrates off the Northeastern United States coast. FEMS Microbiology Ecology 76:421-431

    Article  Google Scholar 

  • Schaefer AM, Goldstein JD, Reif JS, Fair PA, Bossart GD (2009) Antibiotic-resistant organisms cultured from Atlantic bottlenose dolphins (Tursiops truncatus) inhabiting estuarine waters of Charleston, SC and Indian River Lagoon, FL. Ecohealth 6:33-41

    Article  PubMed  Google Scholar 

  • Schaible B, Taylor CT, Schaffer K (2012) Hypoxia increases antibiotic resistance in Pseudomonas aeruginosa through altering the composition of multidrug efflux pumps. Antimicrobial Agents and Chemotherapy 56:2114-2118

    Article  PubMed  CAS  Google Scholar 

  • Shah SQA, Colquhoun DJ, Nikuli HL, Sorum H (2012) Prevalence of antibiotic resistance genes in the bacterial flora of integrated fish farming environments of Pakistan and Tanzania. Environmental Science and Technology 46:8672-8679

    Article  PubMed  CAS  Google Scholar 

  • Sokal RR, Rohlf FJ (2012) Biometry, 4th edn. W.H. Freeman and Company. New York, NY

    Google Scholar 

  • Stock I & Wiedemann B (1998) Identification of natural antibiotic susceptibility of Morganella morganii. Diagnostic Microbiology and Infectious Diseases 30:153-165

    Article  CAS  Google Scholar 

  • Stock I & Wiedemann B (1999) Natural antibiotic susceptibility of Escherichia coli, Shigella, E. vulneris and E. hermannii strains. Diagnostic Microbiology and Infectious Diseases 33:187-199

    Article  CAS  Google Scholar 

  • Stock I & Wiedemann B (2001) Natural antibiotic susceptibility of Klebsiella pneumonia, K. oxytoca, K. planticola, K. ornithinolytica and K. terrigena strains. Journal of Medical Microbiology 50:396-406

    PubMed  CAS  Google Scholar 

  • Stock I & Wiedemann B (2002) Natural antibiotic susceptibility of Enterobacter amnigenus, Enterobacter cancerogenus, Enterobacter gergoviae and Enterobacter sakazakii strains. Clinical Microbiology and Infections 8:564-578

    Article  CAS  Google Scholar 

  • Stoddard RA, Atwill ER, Conrad PA, Byrne BA, Jang S, Lawrence J, McCowan B, Gulland FMD (2009) The effect of rehabilitation of Northern Elephant Seals (Mirounga angustirostris) on antimicrobial resistance of commensal Escherichia coli. Veterinary Microbiology 13:264-271

    Article  Google Scholar 

  • Taylor NGH, Verner-Jeffreys DW, Baker-Austin C (2011) Aquatic systems: maintaining, mixing and mobilizing antimicrobial resistance? Trends in Ecology & Evolution 26: 278-284

    Article  Google Scholar 

  • Thornton SM, Nolan S, Gulland FM (1998) Bacterial isolates from California sea lions (Zalophus californianus), harbor seals (Phoca vitulina), and northern elephant seals (Mirounga angustirostris) admitted to a rehabilitation center along the central California coast, 1994–1995. Journal of Zoo and Wildlife Medicine 29:171-176

    PubMed  CAS  Google Scholar 

  • van der Donk CF, Beisser PS, Hoogkamp-Korstanje JA, Bruggeman CA, Stobberingh EE, Antibiotic Resistance Surveillance Group (2011) A 12 year 1998–2009 antibiotic resistance surveillance of Klebsiella pneumoniae collected from intensive care and urology patients in 14 Dutch hospitals. The Journal of Antimicrobial Chemotherapy 66:855–858

    Article  PubMed  Google Scholar 

  • Zhang XX, Zhang T, Fang HHP (2009) Antibiotic resistance genes in water environment. Applied Microbiology and Biotechnology 82:397-414

    Article  PubMed  CAS  Google Scholar 

Download references

Acknowledgments

We thank the volunteers, interns, and staff at UNE’s Marine Animal Rehabilitation Center for their years of sample collection, record keeping, and marine animal care. The Maine Department of Marine Resources, College of the Atlantic/Allied Whale, New England Aquarium and International Fund for Animal Welfare Marine Mammal Rescue and Research were essential to the collection and transportation of stranded animals. A. Simpson, S. Prendiville, E. Mercker, K. Patchett, and R. Gibson provided valuable assistance concerning animal records, treatments, sensitivity testing, and evaluation. Three anonymous reviewers provided constructive comments that significantly improved the manuscript. Funding support for this study was provided by NOAA/NMFS (John H. Prescott Marine Mammal Rescue Assistance Grant Program to MARC # NA08NMF4390562), the Elmina B. Sewall Foundation and the University of New England. This is contribution #51 from the University of New England’s Marine Science Center.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Anna L. Bass.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Wallace, C.C., Yund, P.O., Ford, T.E. et al. Increase in Antimicrobial Resistance in Bacteria Isolated from Stranded Marine Mammals of the Northwest Atlantic. EcoHealth 10, 201–210 (2013). https://doi.org/10.1007/s10393-013-0842-6

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10393-013-0842-6

Keywords

Navigation