Blood-based indicators of insulin resistance and metabolic syndrome in bottlenose dolphins (Tursiops truncatus)

Frontiers in Endocrinology

Volumn 4, Issue OCT, 2013, Pages

  Venn Watson, Stephanie ^a   Smith, Cynthia Rowe ^a   Stevenson, Sacha ^a   Parry, Celeste ^a   Daniels, Risa ^a   Jensen, Eric ^b   Cendejas, Veronica ^a   Balmer, Brian ^c   Janech, Michael ^d   Neely, Benjamin A ^d   Wells, Randall ^c  

^a NATIONAL MARINE MAMMAL FOUNDATION   (United States)

^b LAC+USC Medical Center   (United States)

^c MOTE MARINE LABORATORY   (United States)

^d MEDICAL UNIVERSITY OF SOUTH CAROLINA   (United States)

Author keywords

Adiponectin; Bottlenose dolphin; Diabetes; Insulin resistance; Iron; Metabolic syndrome

Indexed keywords

ADIPONECTIN; ALANINE AMINOTRANSFERASE; ASPARTATE AMINOTRANSFERASE; CHOLESTEROL; CREATININE; GAMMA GLUTAMYLTRANSFERASE; HAPTOGLOBIN; HIGH DENSITY LIPOPROTEIN CHOLESTEROL; INSULIN; IRON; LACTATE DEHYDROGENASE; TRANSFERRIN; TRIACYLGLYCEROL; URIC ACID; VERY LOW DENSITY LIPOPROTEIN;

ARTICLE; BODY MASS; BOTTLENOSE DOLPHIN; ERYTHROCYTE SEDIMENTATION RATE; FEMALE; GLUCOSE BLOOD LEVEL; INSULIN RESISTANCE; LEUKOCYTE COUNT; MALE; METABOLIC SYNDROME X; NONHUMAN; RISK FACTOR;

EID: 84885397907     PISSN: None     EISSN: 16642392     Source Type: Journal    
DOI: 10.3389/fendo.2013.00136     Document Type: Article

References (50)

1. Danaei G, Finucane MM, Lu Y, Singh GM, Cowan MJ, Paciorek CJ, et al. National, regional, and global trends in fasting plasma glucose and diabetes prevalence since 1980:systematic analysis of health examination surveys and epidemiological studies with 370 country-years and 2.7 million participants. Lancet (2011) 378:31-40. doi:10.1016/S0140-6736(11)60679-X.
2. Shaw JE, Sicree RA, Zimmet PZ. Global estimates of the prevalence of diabetes for 2010 and 2030. Diabetes Res Clin Pract (2010) 87:4-14. doi:10.1016/j.diabres.2009.10.007.
3. Patterson CC, Dahlquist GG, Gyurus E, Green A, Soltesz G, EURODIAB Study Group. Incidence trends for childhood type 1 diabetes in Europe during 1989-2003 and predicted new cases 2005-2020:a multicentre prospective registration study. Lancet (2009) 373:2027-33. doi:10.1016/S0140-6736(09)60568-7.
4. Cefalu WT. Animal models of type 2 diabetes:clinical presentation and pathophysiological relevance to the human condition. ILAR J (2006) 47:186-98. doi:10.1093/ilar.47.3.186.
5. Kaplan JR, Wagner JD. Type 2 diabetes-an introduction to the development and use of animal models. ILAR J (2006) 47:181-5. doi:10.1093/ilar.47.3.181.
6. Ridgway SH, Simpson JG, Patton GS, Gilmartin WG. Hematologic findings in certain small cetaceans. J Am Vet Med Assoc (1970) 157:566-75.
7. Venn-Watson S, Carlin K, Ridgway S. Dolphins as animal models for type 2 diabetes:sustained, postprandial hyperglycemia and hyperinsulinemia. Gen Comp Endocrinol (2012) 170:193-9. doi:10.1016/j.ygcen.2010.10.005.
8. Patton GS. Metabolic Studies on Marine Mammals:Characterization of Alpha- and Beta-Cell Function [Ph.D. Dissertation]. Los Angeles:University of Southern California Graduate School (1975).
9. Johnson SP, Venn-Watson S, Cassle SE, Jensen ED, Smith CR, Ridgway SH. Use of phlebotomy treatment in Atlantic bottlenose dolphins with iron overload. J Am Vet Med Assoc (2009) 235:194-200. doi:10.2460/javma.235.2.194.
10. Venn-Watson S, Benham C, Carlin K, St Leger J. Hemochromatosis and fatty change:building evidence for insulin resistance in bottlenose dolphins (Tursiops truncatus). J Zoo Wildl Med (2012) 43:S35-47. doi:10.1638/2011-0146.1.
11. Venn-Watson S, Smith CR, Daniels R, Townsend F. Clinical relevance of urate nephrolithiasis in bottlenose dolphins (Tursiops truncatus). Dis Aquat Organ (2010) 89:167-77. doi:10.3354/dao02187.
12. Venn-Watson S, Smith CR, Gomez F, Jensen ED. Physiology of aging among healthy, older bottlenose dolphins (Tursiops truncatus):comparisons with aging humans. J Comp Physiol B (2011) 181:667-80. doi:10.1007/s00360-011-0549-3.
13. Haffner SM. Epidemiology of type 2 diabetes:risk factors. Diabetes Care (1998) 21:C3-6.
14. Harris MI, Eastman RC, Cowie CC, Flegal KM, Eberhardt MS. Racial and ethnic differences in glycemic control of adults with type 2 diabetes. Diabetes Care (1999) 22:403-8. doi:10.2337/diacare.22.3.403.
15. Kaufman FR. Type 2 diabetes mellitus in children and youth:a new epidemic. J Pediatr Endocrinol Metab (2002) 15:737-44. doi:10.1515/JPEM.2002.15.S2.737.
16. Pan A, Schernhammer ES, Sun Q, Hu FB. Rotating night shift work and risk of type 2 diabetes:two prospective cohort studies in women. PLoS Med (2011) 8:e1001141. doi:10.1371/journal.pmed.1001141.
17. Scott LJ, Mohlke KL, Bonnycastle LL, Willer CJ, Li Y, Duren WL, et al. A genome-wide association study of type 2 diabetes in Finns detects multiple susceptibility variants. Science (2007) 316:1341-5. doi:10.1126/science.1142382.
18. Mazzaro LM, Johnson SP, Fair PA, Bossart G, Carlin KP, Jensen ED, et al. Iron indices among bottlenose dolphins (Tursiops truncatus):identifying populations at risk for iron overload. Comp Med (2012) 62:508-15.
19. Houser DS, Finneran JJ, Ridgway SH. Research with Navy marine mammals benefits animal care, conservation, and biology. Int J Comp Psychol (2010) 23:249-68.
20. Wells RS. Learning from nature:bottlenose dolphin care and husbandry. Zoo Biol (2009) 28:1-17. doi:10.1002/zoo.20252.
21. Wells RS. Dolphin social complexity:lessons from long-term study and life history. In:de Waal FBM, Tyack PL editors. Cambridge, MA:Harvard University Press (2003). p. 32-56.
22. Wells RS, McHugh KA, Douglas DC, Shippee S, McCabe EB, Barros NB, et al. Evaluation of potential protective factors against metabolic syndrome in bottlenose dolphins:feeding and activity patterns of dolphins in Sarasota Bay, Florida. Front Endocrinol (2013) 4:139. doi:10.3389/fendo.2013.00139.
23. Neely BA, Carlin KP, Arthur JM, McFee WE, Janech MG. Radiometric measurements of adiponectin by mass spectrometry in bottlenose dolphins (Tursiops truncatus) with iron overload reveal an association with insulin resistance and glucagon. Front Endocrinol (2013) 4:132. doi:10.3389/fendo.2013.00132.
24. Smith JE, Chavey PS, Andrews GA. Semiautomatic and robotic methods for determining serum haptoglobin levels. Vet Clin Pathol (1998) 27:11-4. doi:10.1111/j.1939-165X.1998.tb01073.x.
25. Alberti KGM, Zimmet P, Shaw J, IDF Epidemiology Task Force Consensus Group. The metabolic syndrome-a new worldwide definition. Lancet (2005) 366:1059-62. doi:10.1016/S0140-6736(05)67402-8.
26. Grundy SM. Hypertriglyceridemia, insulin resistance, and the metabolic syndrome. Am J Cardiol (1999) 83:25-9. doi:10.1016/S0002-9149(99)00211-8.
27. Younossi ZM, Gramlich T, Matteoni CA, Boparai N, McCollough AJ. Nonalcoholic fatty liver disease in patients with type 2 diabetes. Clin Gastroenterol Hepatol (2004) 2:262-5. doi:10.1016/S1542-3565(04)00014-X.
28. Venn-Watson S, Jensen ED, Ridgway S. Population health indicators of the Navy Marine Mammal Program bottlenose dolphin (Tursiops truncatus) population, 1988-2007. J Am Vet Med Assoc (2011) 238:356-60. doi:10.2460/javma.238.3.356.
29. Venn-Watson S, Smith CR, Jensen ED, Rowles T. Assessing the potential health impacts of the 2003 and 2007 firestorms on bottlenose dolphins (Tursiops truncatus) in San Diego Bay. Inhal Toxicol (2013) 25:481-91. doi:10.3109/08958378.2013.804611.
30. St. Aubin DJ, Ridgway SH, Wells RS, Rhinehart H. Dolphin thyroid and adrenal hormones:circulating levels of wild and semidomesticated Tursiops truncatus, and influence of sex, age, and season. Mar Mamm Sci (1996) 12:1-13. doi:10.1111/j.1748-7692.1996.tb00301.x.
31. Spencer GSG. Relationship between plasma somatomedin activity and levels of cortisol and free fatty acids following stress in pigs. J Endocrinol (1980) 84:109-14. doi:10.1677/joe.0.0840109.
32. Zivkovic AM, German JB, Sanyal AJ. Comparative review of diet for the metabolic syndrome:implications for nonalcoholic fatty liver disease. Am J Clin Nutr (2007) 86:285-300.
33. Slifka KA, Wells RS, Ardente AJ, Crissey S. Comparative diet analysis of fish species commonly consumed by managed and free-ranging bottlenose dolphins (Tursiops truncatus). Internet J Vet Med (2013) 10:1.
34. Nanri A, Mizoue T, Noda M, Takahashi Y, Matsushita Y, Poudel-Tandukar K, et al. Fish intake and type 2 diabetes in Japanese men and women:the Japan Public Health Center-based Prospective Study. Am J Clin Nutr (2011) 94:884-91. doi:10.3945/ajcn.111.012252.
35. Patel PS, Sharp SJ, Luben RN, Khaw KT, Bingham SA, Wareham NJ, et al. Association between type of dietary fish and seafood intake and incident type 2 diabetes:the European prospective investigation of cancer (EPIC)-Norfolk cohort study. Diabetes Care (2009) 32:1857-63. doi:10.2337/dc09-0116.
36. Sigal RJ, Kenny GP, Wasserman DH, Castaneda-Sceppa C, White RD. Physical activity/exercise and type 2 diabetes:a consensus statement from the American Diabetes Association. Diabetes (2006) 29:1433-8.
37. Shippee S, Townsend F, Deckert F, Knowles K. Monitoring Swimming, Diving, and Forestomach Temperature Changes on Instrumented Wild Dolphins to Determine Post-Release Foraging Effort and Success. (2006). Final Technical Report, Harbor Branch Oceanographic Institution Contract No. PWD2003-11. Fort Pierce:Florida Atlantic University. 46 p.
38. Howard BV. Insulin resistance and lipid metabolism. Am J Cardiol (1999) 84:28-32. doi:10.1016/S0002-9149(99)00355-0.
39. Chahil TJ, Ginsberg HN. Diabetic dyslipidemia. Endocrinol Metab Clin North Am (2006) 35:491-510. doi:10.1016/j.ecl.2006.06.002.
40. Wieckowska A, Feldstein AE. Diagnosis of nonalcoholic fatty liver disease:invasive versus noninvasive. Semin Liver Dis (2008) 28:386-95. doi:10.1055/s-0028-1091983.
41. Kadowaki T, Yamauchi T, Kubota N, Hara K, Ueki K, Tobe K. Adiponectin and adiponectin receptors in insulin resistance, diabetes, and the metabolic syndrome. J Clin Invest (2006) 116:1784-92. doi:10.1172/JCI29126.
42. Spranger J, Kroke A, Mohlig M, Bergmann MM, Ristow M, Boeing H, et al. Adiponectin and protection against type 2 diabetes. Lancet (2003) 361:226-8. doi:10.1016/S0140-6736(03)12255-6.
43. Wang Y, Lam KS, Chan L, Chan KW, Lam JB, Lam MC, et al. Post-translational modifications of the four conserved lysine residues within the collagenous domain of adiponectin are required for the formation of its high molecular weight oligomeric complex. J Biol Chem (2006) 281:16391-400. doi:10.1074/jbc.M513907200.
44. Wang Y, Lam KS, Yau MH, Xu A. Post-translational modifications of adiponectin:mechanisms and functional implications. Biochem J (2008) 409:623-33. doi:10.1042/BJ20071492.
45. Almeda-Valdes P, Cuevas-Ramos D, Mehta R, Gomez-Perez FJ, Cruz-Bautista I, Arellano-Campos O, et al. Total and high molecular weight adiponectin have similar utility for the identification of insulin resistance. Cardiovasc Diabetol (2010) 9:26. doi:10.1186/1475-2840-9-26.
46. Zhu N, Pankow JS, Ballantyne CM, Couper D, Hoogeveen RC, Pereira M, et al. High-molecular-weight adiponectin and the risk of type 2 diabetes in the ARIC study. J Clin Endocrinol Metab (2010) 95:5097-104. doi:10.1210/jc.2010-0716.
47. Daimon M, Oizumi T, Saitoh T, Kameda W, Hirata A, Yamaguchi H, et al. Decreased serum levels of adiponectin are a risk factor for the progression to type 2 diabetes in the Japanese population:the Funagata study. Diabetes Care (2003) 26:2015-20. doi:10.2337/diacare.26.7.2015.
48. Lindsay RS, Funahashi T, Hanson RL, Matsuzawa Y, Tanaka S, Tataranni PA, et al. Adiponectin and development of type 2 diabetes in the Pima Indian population. Lancet (2002) 360:57-8. doi:10.1016/S0140-6736(02)09335-2.
49. Mendler MH, Turlin B, Moirand R, Jouanolle AM, Sapey T, Guyader D, et al. Insulin resistance-associated hepatic iron overload. Gastroenterology (1999) 117:1155-63. doi:10.1016/S0016-5085(99)70401-4.
50. Wrede CE, Buettner R, Bollheimer LC, Scholmerich J, Palitzsch KD, Hellerbrand C. Association between serum ferritin and the insulin resistance syndrome in a representative population. Eur J Endocrinol (2006) 154:333-40. doi:10.1530/eje.1.02083.