• 1. Márquez-Millan R, Burchfield PM, Díaz-Flores J, et al. Status of the Kemp's ridley turtle, Lepidochelys kempii. Chelonian Conserv Biol 2005; 4: 761766.

    • Search Google Scholar
    • Export Citation
  • 2. Morreale SJ, Standora EA. Western North Atlantic waters: crucial developmental habitat for Kemp's ridley and loggerhead sea turtles. Chelonian Conserv Biol 2005; 4: 872882.

    • Search Google Scholar
    • Export Citation
  • 3. Morreale SJ, Meylan AB, Sadove SS, et al. Annual occurrence and winter mortality of marine turtles in New York waters. J Herpetol 1992; 26: 301308.

  • 4. Still BM, Griffin CR, Prescott R. Climatic and oceanographic factors affecting daily patterns of juvenile sea turtle cold-stunning in Cape Cod Bay, Massachusetts. Chelonian Conserv Biol 2005; 4: 883890.

    • Search Google Scholar
    • Export Citation
  • 5. Witherington BE, Ehrhart LM. Hypothermic stunning and mortality of marine turtles in the Indian River lagoon system, Florida. Copeia 1989; 696703.

    • Search Google Scholar
    • Export Citation
  • 6. Bentivegnal F, Breber P, Hochscheid S. Cold stunned loggerhead turtles in the south Adriatic Sea. Mar Turtle Newsl 2000; 97: 13.

  • 7. Gerle E, DiGiovanni R, Pisciotta R. A fifteen year review of cold-stunned sea turtles in New York waters, in Proceedings. 18th Int Sea Turtle Symp 2000; 222224.

    • Search Google Scholar
    • Export Citation
  • 8. Wyneken J, Mader DR, Weber ES, et al. Medical care of seaturtles. In: Mader D, ed. Reptile medicine and surgery. 2nd ed. St Louis: Elsevier, 2006; 9721007.

    • Search Google Scholar
    • Export Citation
  • 9. Turnbull BS, Smith CR, Stamper MA. Medical implications of hypothermia in threatened loggerhead (Caretta caretta) and endangered Kemp's ridley (Lepidochelys kempii) and green (Chelonia mydas) sea turtles, in Proceedings. Joint Conf Am Assoc Zoo Vet Int Assoc Aquat Anim Med 2000; 3135.

    • Search Google Scholar
    • Export Citation
  • 10. Stacy NI, Innis CJ, Hernandez JA. Development and evaluation of three mortality prediction indices for cold-stunned Kemp's ridley sea turtles (Lepidochelys kempii). Cons Physiol [serial online]. 2013; 1. Available at: conphys.oxfordjournals.org/content/1/1/cot003.short?rss=1. Accessed Nov 3, 2013.

    • Search Google Scholar
    • Export Citation
  • 11. Keller KA, Innis CJ, Tlusty MF, et al. Metabolic and respiratory derangements associated with death in cold-stunned Kemp's ridley turtles (Lepidochelys kempii): 32 cases (2005)2009). J Am Vet Med Assoc 2012; 240: 317323.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 12. Stockman J, Innis CJ, Solano M, et al. Prevalence, distribution, and progression of radiographic abnormalities in the lungs of cold-stunned Kemp's ridley sea turtles (Lepidochelys kempii): 89 cases (2002)2005). J Am Vet Med Assoc 2013; 242: 675681.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 13. Manire CA, Rhinehart HL, Sutton DA, et al. Disseminated mycotic infection caused by Colletotrichum acutatum in a Kemp's ridley sea turtle (Lepidochelys kempii). J Clin Microbiol 2002; 40: 42734280.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 14. Pare JA, Sigler L, Rosenthal, et al. Microbiology: fungal and bacterial diseases of reptiles. In: Mader D, ed. Reptile medicine and surgery. 2nd ed. St Louis: Elsevier, 2006; 217238.

    • Search Google Scholar
    • Export Citation
  • 15. Cervera C, Almela M, Martínez-Martínez JA, et al. Risk factors and management of gram-positive bacteraemia. Int J Antimicrob Agents 2009; 34 (suppl 4):S26S30.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 16. Orsini JA, Snooks-Parsons C, Stine L, et al. Vancomycin for the treatment of methicillin-resistant staphylococcal and enterococcal infections in 15 horses. Can J Vet Res 2005; 69: 278286.

    • Search Google Scholar
    • Export Citation
  • 17. Devriese LA, Chiers K, De Herd P, et al. Enterococcus hirae infections in psittacine birds: epidemiological, pathological and bacteriological observations. Avian Pathol 1995; 24: 523531.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 18. Mundt JO. Occurrence of enterococci in animals in a wild environment. Appl Microbiol 1963; 11: 136140.

  • 19. Sheridan BS, Wilson GR, Weldon PJ. Aerobic bacteria from the skin of the rattlesnake, Crotalus atrox. J Herpetol 1989; 23: 200202.

  • 20. Innis C, Merigo C, Dodge K, et al. Health evaluation of leather-back turtles (Dermochelys coriacea) in the northwestern Atlantic during direct capture and fisheries gear disentanglement. Chelonian Conserv Biol 2010; 9: 205222.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 21. Schröter M, Heckers KO, Rüschoff B, et al. Severe case of spinal osteomyelitis due to Enterococcus sp. in a three-year old rhinoceros horned viper, Bitis nasicornis. J Herpetol Med Surg 2005; 15: 5356.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 22. Solano M, Innis C, Smith C, et al. Scintigraphic and radiographic evaluation of appendicular skeletal lesions in cold-stunned Kemp's ridley sea turtles. Vet Radiol Ultrasound 2008; 49: 388394.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 23. Johnson J. Enteritis in a pair of juvenile Aldabra tortoises, Geochelone gigantea, in Proceedings. Assoc Reptil Amphib Vet 8th Ann Conf 2001; 147152.

    • Search Google Scholar
    • Export Citation
  • 24. Anderson ET, Kennedy-Stoskopf S, Sandy JR, et al. Squamous cell carcinoma with vascular invasion in a diamondback rattlesnake (Crotalus adamanteus). J Zoo Wildl Med 2010; 41: 745748.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 25. Clinical and Laboratory Standards Institute. Performance standards for antimicrobial susceptibility testing; twentieth informational supplement. M100)S20. Wayne, Pa: Clinical and Laboratory Standards Institute, 2010.

    • Search Google Scholar
    • Export Citation
  • 26. Baden LR, Critchley IA, Sahm DF, et al. Molecular characterization of vancomycin-resistant enterococci repopulating the gastrointestinal tract following treatment with a novel glycolipodepsipeptide, ramoplanin. J Clin Microbiol 2002; 40: 11601163.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 27. Baden LR, Thiemke W, Skolnik A, et al. Prolonged colonization with vancomycin-resistant Enterococcus faecium in long-term care patients and the significance of “clearance.” Clin Infect Dis 2001; 33: 16541660.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 28. Innis C, Nyaoke A, Williams C III, et al. Pathologic and parasitologic findings of cold-stunned Kemp's ridley sea turtles (Lepidochelys kempii) stranded on Cape Cod, MA, 2001)2006. J Wildl Dis 2009; 45: 594610.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 29. Innis CJ, Ravich JB, Tlusty MF, et al. Hematologic and plasma biochemical findings in cold-stunned Kemp's ridley turtles: 176 cases (2001)2005). J Am Vet Med Assoc 2009; 235: 426432.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 30. Innis CJ, Ceresia ML, Merigo C, et al. Single-dose pharmacokinetics of ceftazidime and fluconazole during concurrent clinical use in cold-stunned Kemp's ridley turtles (Lepidochelys kempii). J Vet Pharmacol Ther 2012; 35: 8289.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 31. Jang HC, Lee S, Song KH, et al. Clinical features, risk factors and outcomes of bacteremia due to enterococci with high-level gentamicin resistance: comparison with bacteremia due to enterococci without high-level gentamicin resistance. J Korean Med Sci 2010; 25: 38.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 32. Hunt KE, Innis C, Rolland RM. Corticosterone and thyroxine in cold-stunned Kemp's ridley sea turtles (Lepidochelys kempii). J Zoo Wildl Med 2012; 43: 479493.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 33. Zimmerman LM, Vogel LA, Bowden RM. Understanding the vertebrate immune system: insights from the reptilian perspective. J Exp Biol 2010; 213: 661671.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 34. Mylniczenko ND, Harris B, Wilborn RE, et al. Blood culture results from healthy captive and free-ranging elasmobranchs. J Aquat Anim Health 2007; 19: 159167.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 35. Hanel R, Heard DJ, Ellis G, et al. Isolation of Clostridium spp from the blood of captive lizards: real or pseudobacteremia? Bull Assoc Reptil Amphib Vet 1999; 9 (2):48.

    • Search Google Scholar
    • Export Citation
  • 36. Gentry-Weeks C, Estay M, Loui C, et al. Intravenous mouse infection model for studying the pathology of Enterococcus faecalis infections. Infect Immun 2003; 71: 14341441.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 37. US Department of the Interior Fish and Wildlife Service. Standard permit conditions for care and maintenance of captive sea turtles. Available at: www.fws.gov/northflorida/seaturtles/Captive_Forms/20130213_revised%20_standard_permit_conditions_for_captive_sea_turtles.pdf. Accessed Nov 3, 2013.

    • Search Google Scholar
    • Export Citation
  • 38. Caputo GM, White S, Weitekamp MR. Infections due to antibiotic-resistant gram-positive cocci. J Gen Intern Med 1993; 8: 626634.

Advertisement

Diagnosis and management of Enterococcus spp infections during rehabilitation of cold-stunned Kemp's ridley turtles (Lepidochelys kempii): 50 cases (2006–2012)

View More View Less
  • 1 Department of Animal Health, New England Aquarium, 1 Central Wharf, Boston, MA 02110.
  • | 2 Hospital for Animals, College of Veterinary Medicine, Cornell University, Ithaca, NY 14853.
  • | 3 Department of Animal Health, New England Aquarium, 1 Central Wharf, Boston, MA 02110.
  • | 4 Pharmacy Practice, School of Pharmacy, MCPHS University, Boston, MA 02115.
  • | 5 Brigham and Women's Hospital, 75 Francis St, Boston, MA 02115.
  • | 6 Whitehead Institute, 9 Cambridge Center, Cambridge, MA 02142.
  • | 7 Connecticut Veterinary Medical Diagnostic Laboratory, Department of Pathobiology and Veterinary Science, College of Agriculture and Natural Resources, University of Connecticut, Storrs, CT 06269.
  • | 8 Department of Animal Health, New England Aquarium, 1 Central Wharf, Boston, MA 02110.
  • | 9 Department of Animal Health, New England Aquarium, 1 Central Wharf, Boston, MA 02110.
  • | 10 Office of Protected Resources, National Oceanic and Atmospheric Administration, 1315 East-West Hwy, Gainesville, FL 32611.
  • | 11 Department of Rescue and Rehabilitation, New England Aquarium, 1 Central Wharf, Boston, MA 02110.

Abstract

Objective—To evaluate clinical data for cold-stunned Kemp's ridley turtles (Lepidochelys kempii) with Enterococcus spp infections during rehabilitation.

Design—Retrospective case series.

Animals—50 stranded cold-stunned Kemp's ridley turtles hospitalized between 2006 and 2012.

Procedures—Medical records for turtles from which Enterococcus spp were isolated were reviewed retrospectively, and clinical data, including morphometric data, body temperature at admission, physical examination findings, antimicrobial medication history, history of medications administered IV, environmental data, day of diagnosis, clinical signs at diagnosis, microbiological testing results, sources of positive culture results, hematologic and plasma biochemical data, cytologic and histopathologic results, radiographic findings, antimicrobial treatments, time to first negative culture result, treatment duration, results of subsequent cultures, and case outcome, were collated and analyzed.

ResultsEnterococcus spp were isolated from bacteriologic cultures of blood, bone, joint, and respiratory tract samples and a skin lesion, with supporting evidence of infection provided by histopathologic, cytologic, and radiographic data. Positive culture results were associated with clinical problems such as lethargy, anorexia, and lameness. Most (34/43 [79%]) turtles for which an antemortem diagnosis was made survived with treatment and were released into the wild.

Conclusions and Clinical Relevance—Cold-stunned Kemp's ridley turtles may be affected by serious Enterococcus spp infections during rehabilitation. Recognition and treatment of these infections are important for successful rehabilitation.

Abstract

Objective—To evaluate clinical data for cold-stunned Kemp's ridley turtles (Lepidochelys kempii) with Enterococcus spp infections during rehabilitation.

Design—Retrospective case series.

Animals—50 stranded cold-stunned Kemp's ridley turtles hospitalized between 2006 and 2012.

Procedures—Medical records for turtles from which Enterococcus spp were isolated were reviewed retrospectively, and clinical data, including morphometric data, body temperature at admission, physical examination findings, antimicrobial medication history, history of medications administered IV, environmental data, day of diagnosis, clinical signs at diagnosis, microbiological testing results, sources of positive culture results, hematologic and plasma biochemical data, cytologic and histopathologic results, radiographic findings, antimicrobial treatments, time to first negative culture result, treatment duration, results of subsequent cultures, and case outcome, were collated and analyzed.

ResultsEnterococcus spp were isolated from bacteriologic cultures of blood, bone, joint, and respiratory tract samples and a skin lesion, with supporting evidence of infection provided by histopathologic, cytologic, and radiographic data. Positive culture results were associated with clinical problems such as lethargy, anorexia, and lameness. Most (34/43 [79%]) turtles for which an antemortem diagnosis was made survived with treatment and were released into the wild.

Conclusions and Clinical Relevance—Cold-stunned Kemp's ridley turtles may be affected by serious Enterococcus spp infections during rehabilitation. Recognition and treatment of these infections are important for successful rehabilitation.

Contributor Notes

Dr. Kuhn's present address is Cambridge Health Alliance, 1493 Cambridge St, Cambridge, MA 02139.

Dr. Hirokawa's present address is Miami Seaquarium, 4400 Rickenbacker Causeway, Miami, FL 33149.

Dr. Weber's present address is American Association for Advancement of Science, 1200 New York Ave, Washington, DC 20001.

Dr. Braverman was a third-year veterinary student at the time of the study.

Financial support for Dr. Braverman was provided by the International Association of Aquatic Animal Medicine Medway Scholarship. Histologic services were partially funded by the US Department of Commerce National Marine Fisheries Service.

Presented in part at the 17th Annual Conference of the Association of Reptilian and Amphibian Veterinarians, South Padre Island, Tex, October 2010, and the 44th Annual Conference of the International Association of Aquatic Animal Medicine, Sausalito, Calif, April 2013.

The authors thank Dr. Leigh Clayton, Dr. Catherine Hadfield, Dr. Lara Croft, Dr. Michelle Davis, Dr. Sea Rogers Williams, Dr. Michelle Sims, Dr. Howard Gold, Dr. George Eliopoulos, and Kristen Patchett for contributions.

Address correspondence to Dr. Innis (cinnis@neaq.org).