Medical Implications of Hypothermia in Threatened Loggerhead (Caretta caretta) and Endangered Kemp's Ridley (Lepidochelys kempi) and Green (Chelonia mydas) Sea Turtles
IAAAM 2000
Beth S. Turnbull, DVM, PhD; Cynthia R. Smith, DVM; M. Andrew Stamper, DVM, DACZM
Departments of Veterinary Services and Rescue and Rehabilitation, New England Aquarium, Boston, MA, USA

Abstract

Hypothermia

Hypothermia results in cellular and tissue necrosis and potentially death due to the slowing of metabolic processes, particularly in the brain and medullary centers. Hypothermia is known to damage tissues in two ways. First, the direct effects are mediated by the crystallization of intra- and extracellular water and the resultant high salt concentrations. Second, indirect effects are exerted by circulatory changes.4 With a slow drop in temperature, vasoconstriction and increased permeability result in edematous changes. However, a sudden drop in temperature leads to vasoconstriction and increased viscosity of the blood with ischemic injury and degenerative changes in peripheral nerves. During the period of ischemia, hypoxic changes and infarction necrosis of the affected tissues may develop. When the temperature begins to return to normal, the vascular injury and increased permeability with exudation become evident.4 Other detrimental physiologic changes include dermal injury, immune function compromise, decreased threshold for myocardial arrhythmias, bradycardia, electrolyte imbalances and acid base disturbances.1,3

Hypothermia in Sea Turtles

Hypothermia, or cold stunning, in sea turtles is considered a rare winter phenomenon in which the water temperature quickly drops below 50°F (10°C).5,9 At this cold temperature, turtles lose their ability to swim and dive, become buoyant, and float to the surface.5,7 This phenomenon is most commonly reported in juvenile sea turtles. Cold stunning has been recognized from the Gulf of Mexico to New England, as well as in Western Europe.5 The physiology of the cold stunning response is not understood, however it is thought to involve disruption of metabolic pathways.8 Indeed, cold stunned turtles have been shown to have decreased salt gland function resulting in abnormal blood levels of sodium, potassium, chloride, calcium, magnesium, and phosphorus.5 In addition, cold stunned Kemp's ridley (Lepidochelys kempi) sea turtles have been shown to have increased creatine kinase (CK) and decreased blood urea nitrogen (BUN).3

Previous accounts of cold stunning events along the East Coast of the United States have typically only involved one turtle to several dozen turtles. However, four large hypothermic events have occurred in the Indian River in Florida. During the winter of 1894, Wilcox described a hypothermic event involving hundreds of green turtles.9 Similarly, in 1977, 1981, and 1985, 136 to 163 hypothermic turtles were collected in the Indian River in Florida.9 In 1924, Latham reported 103 turtles on a 3-mile stretch of beach in Long Island, New York.2 However, a massive cold stunning event has not previously been reported in the New England region despite the fact that these waters have been shown to be a critically important habitat for juvenile Kemp's ridley sea turtles.6

1999 Cape Cod Bay Cold-Stunning Event

From 8 November 1999 to 7 January 2000, 277 turtles including 218 Kemp's ridleys, 54 loggerheads (Caretta caretta), and 5 greens (Chelonia mydas) stranded along Cape Cod Bay. The Massachusetts Audubon Society's Wellfleet Bay Wildlife Sanctuary collected the turtles. Of the 277 turtles, 123 Kemp's ridleys, 17 loggerheads, and 4 greens were found alive. These 144 sea turtles were transported to the New England Aquarium. Table 1 documents the ranges of straight carapace length and body weights of the turtles upon arrival. The ranges in body size and weight were significant and not all stranded turtles were in the juvenile class size.

Upon arrival, only 127 were alive. These turtles were severely hypothermic with body temperatures ranging from 40-60°F. Initial examinations revealed traumatic wounds, moderate to extreme dehydration, corneal ulcerations, and dermal, carapace, and plastron lesions secondary to hypothermia. Heart rates and respiratory rates were determined for each turtle and emergency procedures [oxygen, tracheal intubation, atropine sulfate at 0.04 mg/kg (Elkins-Sinn, Cherry Hill, NJ), doxapram HCl at 5 mg/kg (Dopram®-V, Fort Dodge, Fort Dodge, IA), dexamethasone sodium phosphate at 0.15 mg/kg (American Regent Laboratories, Shirley, NY)] were initiated on any turtle with bradycardia and/or apnea. The turtles were then carefully cleaned, their eyes were flushed with sterile isotonic buffered eye irrigating solution, their superficial wounds were debrided and treated with topical antibiotics and/or antimycotics, their bodies were lubricated with sterile water soluble/bacteriostatic lubricating jelly, and they were placed in an incubator or a temperature controlled room at 3-5°F above their arrival body temperature. Their body temperatures were then gradually increased approximately 5°F per day until they reached 75°F. Beginning at 48 hr post-arrival, the turtles were slowly introduced to fresh water equilibrated to their current body temperature. To prevent further dehydration, they were cautiously graduated from fresh to brackish and finally to seawater within 2 wk of arrival.

Complete blood counts and chemistry profiles were performed as often as every 12 hr. Abnormalities such as hypoglycemia and hyperglycemia, decreased BUN, decreased phosphorus, hypocalcemia, decreased total protein, hypokalemia, increased CK, and heterophilic leukocytoses were common initial findings in all three species (Table 2). In addition, sodium and chloride levels were elevated in the Kemp's ridley sea turtles (Table 2). All electrolyte and acid base abnormalities were treated immediately with 50% dextrose at 1-2 ml i.v. or intracoelomic (i.c.) (Abbott Labs, North Chicago, IL), calcium gluconate at 100 mg/kg i.m. or i.c. (Abbott Labs, North Chicago, IL), and Potassium chloride at 15-30 mEq/L of fluid i.c. (Abbott Labs, North Chicago, IL). In addition, all turtles were given 1% body weight reptile ringers (1 part Lactated Ringers, 2 parts 2.5% dextrose and 0.45% sodium chloride) s.i.d, i.c. or s.c. for the first 3-5 days and then decreasing amounts of 0.9% sodium chloride e.o.d. until the turtles were actively eating. When the turtles reached 60-65°F they were placed on a prophylactic antibiotic and antifungal regime including ceftazidime at 22 mg/kg i.m., e.t.d. (Fortaz®; Glaxo Wellcome, Research Triangle Park, NC), clindamycin at 5 mg/kg i.m., s.i.d. (Cleocin®; Upjohn, Kalamazoo, MI), and fluconazole at 0.75 mg/kg s.c., e.o.d. (Diflucan®; Pfizer, New York, NY). Once actively eating, fluconazole was discontinued and in some turtles itraconazole at 5 mg/kg p.o., s.i.d. (Sporanox®; Janssen Pharmaceuticals, Beerse, Belgium) was begun. In addition, all turtles were given injectable vitamins i.m. or s.c. including Iron Hydrogenated Dextran at 12 mg/kg (Phoenix Labs, St. Joseph, MO), vitamin B complex at 0.1 ml/kg (Butler, Columbus, OH), vitamin K1 (phytonadione) at 0.5 mg/kg (Amvet, Yaphank, NY), vitamin C at 10 mg/kg (Butler, Columbus, OH), and vitamins A and D3 at 0.02 mg/kg (Phoenix Labs, St. Joseph, MO) until they began actively eating and were then switched to generic oral multi-vitamins including A, D, E, B1, B2, B6, niacin, C, folic acid, B12, pantothenic acid, and calcium.

After being slowly warmed to 75°F, hematocrit and chemistry profiles were performed as often as once daily and as infrequently as every 2 wk depending upon the health status of the individual turtle. Complete blood counts were performed every 2 wk. During the first couple of weeks of rehabilitation, the hypoglycemias, hypocalcemias, and hypokalemias became more pronounced. Furthermore, while some of the leukocytoses became extremely elevated, others developed into leukopenias. Monocytoses became a frequent finding. Radiographs revealed pneumonia and coelomic taps demonstrated coelomitis in the majority of animals. Cultures indicated localized and systemic bacterial and fungal infections. Approximately one-fourth of the animals continued to have buoyancy disorders due to trapped air in the coelomic cavity and/or excessive gas in the gastrointestinal tract. At least three turtles (two Kemp's ridleys and one loggerhead) suffered from functional ileus. Five Kemp's ridley turtles developed a non-regenerative anemia that was not responsive to repeated whole blood transfusions from a healthy adult Kemp's ridley sea turtle or Hemoglobin Glutamer-200 (bovine) (Oxyglobin®; Biopure Corporation, Cambridge, MA) transfusions. Three of these five turtles were found to have systemic mycoses with positive cultures for Beauveria bassiana. Eventually, most turtles developed frostbite type dermal lesions, which included flipper tip necrosis. Radiographs, bone scintigraphy, and computed tomography confirmed that osteolysis with or without osteomyelitis coincided with a large proportion of the traumatic wounds and flipper tip necrosis lesions.

Necropsies and histopathology of the non-surviving turtles revealed pneumonia, splenitis, pancreatitis, centrilobular liver necrosis, hepatocellular swelling and fatty change, red blood cell casts with renal tubular dilation, steatitis, esophagitis, ulcerative gastritis, enteritis, colitis, intestinal parasitism, subcutaneous and intramuscular edema, myofiber degeneration, bone marrow hypocellularity, erythrophagocytosis, and systemic bacterial and fungal infections. Our laboratory is currently comparing clinical findings with pathologic observations in each animal's case, which will enable us to better characterize these pathophysiologic processes.

Due to space limitations at the New England Aquarium, eight transports were made from 19 November 1999 to 28 January 2000 to deliver 85 Kemp's ridley and 11 loggerhead sea turtles to the following facilities for continued rehabilitation: The Turtle Hospital, Marathon Key, FL; Mote Marine Lab, Sarasota, FL; Epcot's Living Seas, Orlando, FL; Clearwater Marine Aquarium, Clearwater, FL; Marine Life Center, Juno Beach, FL; Woods Hole Oceanographic Institute, MA; Mystic Aquarium, Mystic, CT; Florida Aquarium, Tampa, FL; Topsail Sea Turtle Hospital, NC; Virginia Marine Science Museum, VA; The Riverhead Foundation, Long Island, NY; Marine Biological Laboratory, Woods Hole, MA; Columbus Zoo, OH.

Of the 127 turtles transported alive to the New England Aquarium, 84% (107) were successfully rehabilitated or transported to another facility. These included 89 Kemp's ridley, 16 loggerhead, and 2 green sea turtles. After transport to other facilities, six Kemp's ridleys did not survive bringing the overall survivorship rate to 79% for all facilities involved. Despite an extensive list of electrolyte, organ, and tissue abnormalities seen as a direct result from the hypothermic cold stunning, we attribute the high success rate of rehabilitation to the following; slow increases in body temperatures, gradual reintroduction to sea water from fresh and brackish water, prophylactic antibiotic and antimycotic therapy, vitamin therapy, and finally repeated blood analyses with immediate correction of any electrolyte or acid base abnormalities.

Table 1. Straight carapace length and body weight ranges for the 1999 Cape Cod Bay stranded turtles.

Kemp's ridley

Loggerhead

Green

Straight carapace length (cm)

21.0-37.2

42.2-89.6

20.5-67.0

Body weight (kg)

1.2-6.7

10.7-89.0

1.0-39.9

Table 2. Preliminarya range and mean--standard deviation of arrival and release (non-fasting) blood values for 1999 Kemp's ridley (n = 15) and loggerhead (n = 10) stranded sea turtles.

 

Kemp's Ridley

Kemp's Ridley

Loggerhead

Loggerhead

Arrival

Release

Arrival

Release

Glucose(mg/dl)

Range

32.0-226.0

88.0-134.0

71.0-304.0

100.0-152.0

Mean ± std

123.9 ± 55.4

111.9 ± 13.3

166.2 ± 74.3

123.7 ± 15.9

BUN (mg/dl)

Range

14.0-167.0

94.0-190.0

21.0-178.0

136.0-274.0

Mean ± std

38.9 ± 38.3

149.6 ± 31.1

62.7 ± 60.1

191.2 ± 43.3

Phosphorus (mg/dl)

Range

5.2-10.2

7.6-12.0

5.5-9.2

6.7-13.4

Mean ± std

6.9 ± 1.4

9.7 ± 1.5

6.5 ± 1.2

10.1 ± 1.8

Calcium (mg/dl)

Range

5.3-7.6

5.7-8.6

4.6-9.4

7.3-8.4

Mean ± std

6.3 ± 0.7

6.8 ± 0.8

6.5 ± 1.4

7.9 ± 0.4

Total Protein (g/dl)

Range

2.1-3.3

3.3-4.8

2.0-4.0

3.9-6.0

Mean ± std

2.7 ± 0.3

3.9 ± 0.4

3.3 ± 0.6

4.8 ± 0.7

Sodium (mEq/L)

Range

146.0-170.0

151.0-159.0

147.0-165.0

148.0-158.0

Mean ± std

156.9 ± 6.4

154.3 ± 2.9

152.1 ± 5.0

154.6 ± 3.0

Chloride (mEq/L)

Range

105.0-133.0

110.0-123.0

102.0-118.0

110.0-120.0

Mean ± std

117.7 ± 8.8

115.2 ± 3.5

111.4 ± 5.3

114.5 ± 3.3

Potassium (mEq/L)

Range

2.3-4.8

2.7-4.0

1.7-3.4

2.9-4.3

Mean ± std

3.2 ± 0.7

3.4 ± 0.5

2.6 ± 0.6

3.7 ± 0.4

CK (U/L)

Range

3958.0-107688.0

256.0-2905.0

1932.0-494038.0

523.0-13503.0

Mean ± std

22508.8 ± 27944.3

1225.2 ± 920.5

71750.4 ± 159077.5

3738.3 ± 4728.2

Total WBC (10 x 3/μl)

Range

3.3-24.7

5.7-9.5

4.9-30.0

2.3-5.1

Mean ± std

10.4 ± 6.2

7.6 ± 1.3

12.1 ± 7.5

3.8 ± 0.9

Hematocrit (%)

Range

26.0-44.0

27.0-37.0

22.0-41.0

29.0-40.0

Mean ± std

35.5 ± 5.7

33.7 ± 3.3

32.2± 6.0

35.8 ± 4.1

a. As of April 2000, only 25 of the 101 surviving turtles were considered "healthy" for release. The arrival and release blood values of these 25 animals are compared in this table.

Acknowledgments

This project would not have been possible without Connie Merigo, Belinda Rubinstein, Jim Rice, Kristen Patchett, Melissa Hodge, Kristen Dubé, Dr. Sonia Mumford, Robert Cooper, Casey Sugarman, Deana Edmunds, Katarina Peterson, Susan Goodridge, John Dayton, and volunteers of the New England Aquarium. We also thank the Massachusetts Audubon Society's Wellfleet Bay Wildlife Sanctuary for their beach rescue of the turtles. Finally, we thank all of the facilities that generously accepted the turtles, provided for their excellent care, and supplied blood for the support of this and other projects.

References

1.  Ackerman L. 1999. Anesthesia. In: The Biology, Husbandry and Health Care of Reptiles, Volume III. TFH Publications, Neptune, New Jersey, Pp. 848-850.

2.  Burke VJ, EA Standora, SJ Morreale. 1991. Factors affecting strandings of cold-stunned juvenile Kemp's ridley and loggerhead sea turtles in Long Island, New York. Copeia 4: 1136-1138.

3.  Carminati CE, E Gerle, LL Kiehn, RP Pisciotta. 1994. Blood chemistry comparison of healthy vs hypothermic juvenile Kemp's ridley sea turtles (Lepidochelys kempi) in New York Bright. In: Proceedings of the Fourteenth Annual Symposium on Sea Turtle Biology and Conservation. NOAA Technical Memorandum NMFS-SEFSC-351, Pp. 203-207.

4.  Cotran RS, V Kumar, SL Robbins. 1994. Environmental and nutritional diseases. In: Pathologic Basis of Disease. W.B. Saunders Company, Philadelphia, Pennsylvania, Pp. 400-401.

5.  George RH. 1997. Health problems and diseases of sea turtles. In: The Biology of Sea Turtles. CRC Press, Inc., Boca Raton, Florida, Pp. 377-378.

6.  Lazell JD. 1980. New England waters: critical habitat for marine turtles. Copeia 2:290-295.

7.  Lutz PL. 1997. Salt, water, and pH balance in the sea turtle. In: The Biology of Sea Turtles. CRC Press, Inc., Boca Raton, Florida, Pp. 355-357.

8.  Spotila JR, MP O'Connor, FV Paladino. 1997. Thermal biology. In: The Biology of Sea Turtles. CRC Press, Inc., Boca Raton, Florida, Pp. 308.

9.  Witherington BE, LM Ehrhart. 1989. Hypothermic stunning and mortality of marine turtles in the Indian River Lagoon system, Florida. Copeia 3: 696-703.

Speaker Information
(click the speaker's name to view other papers and abstracts submitted by this speaker)

Beth S. Turnbull, DVM, PhD
Department of Pathology, University of Texas Medical Branch
Galveston, TX, USA
Texas Marine Mammal Stranding Network


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