Effects of diet-induced weight gain on insulin sensitivity and plasma hormone and lipid concentrations in horses

Rebecca A. Carter Department of Animal and Poultry Sciences, College of Agricultural and Life Sciences, Virginia Polytechnic Institute and State University, Blacksburg, VA 24061.

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L. Jill McCutcheon Department of Biomedical Sciences and Pathobiology, Virginia-Maryland Regional College of Veterinary Medicine, Virginia Polytechnic Institute and State University, Blacksburg, VA 24061.

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Lindsey A. George Department of Animal and Poultry Sciences, College of Agricultural and Life Sciences, Virginia Polytechnic Institute and State University, Blacksburg, VA 24061.

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Tracy L. Smith Department of Animal and Poultry Sciences, College of Agricultural and Life Sciences, Virginia Polytechnic Institute and State University, Blacksburg, VA 24061.

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Nicholas Frank Department of Large Animal Clinical Sciences, College of Veterinary Medicine, University of Tennessee, Knoxville, TN 37996.

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Raymond J. Geor Department of Animal and Poultry Sciences, College of Agricultural and Life Sciences, Virginia Polytechnic Institute and State University, Blacksburg, VA 24061.

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 BVSc, PhD

Abstract

Objective—To determine the effects of diet-induced weight gain on glucose and insulin dynamics and plasma hormone and lipid concentrations in horses.

Animals—13 adult geldings.

Procedures—Horses were fed 200% of their digestible energy requirements for maintenance for 16 weeks to induce weight gain. Frequently sampled IV glucose tolerance tests were performed before and after weight gain to evaluate glucose and insulin dynamics. Adiposity (assessed via condition scoring, morphometric measurements, and subcutaneous fat depth) and plasma concentrations of insulin, glucose, nonesterified fatty acids, triglycerides, and leptin were measured on a weekly or biweekly basis.

Results—Mean ± SD body weight increased by 20% from 440 ± 44 kg to 526 ± 53 kg, and body condition score (scale, 1 to 9) increased from 6 ± 1to8 ± 1. Plasma glucose, triglyceride, and nonesterified fatty acid concentrations were similar before and after weight gain. Leptin and insulin concentrations increased with weight gain. Mean ± SD insulin sensitivity decreased by 71 ± 28%, accompanied by a 408 ± 201% increase in acute insulin response to glucose, which resulted in similar disposition index before and after weight gain.

Conclusions and Clinical Relevance—Diet-induced weight gain in horses occurred concurrently with decreased insulin sensitivity that was effectively compensated for by an increase in insulin secretory response. Obesity resulted in hyperinsulinemia and hyperleptinemia, compared with baseline values, but no changes in lipid concentrations were apparent. Preventing obesity is a potential strategy to help avoid insulin resistance, hyperinsulinemia, and hyperleptinemia in horses.

Abstract

Objective—To determine the effects of diet-induced weight gain on glucose and insulin dynamics and plasma hormone and lipid concentrations in horses.

Animals—13 adult geldings.

Procedures—Horses were fed 200% of their digestible energy requirements for maintenance for 16 weeks to induce weight gain. Frequently sampled IV glucose tolerance tests were performed before and after weight gain to evaluate glucose and insulin dynamics. Adiposity (assessed via condition scoring, morphometric measurements, and subcutaneous fat depth) and plasma concentrations of insulin, glucose, nonesterified fatty acids, triglycerides, and leptin were measured on a weekly or biweekly basis.

Results—Mean ± SD body weight increased by 20% from 440 ± 44 kg to 526 ± 53 kg, and body condition score (scale, 1 to 9) increased from 6 ± 1to8 ± 1. Plasma glucose, triglyceride, and nonesterified fatty acid concentrations were similar before and after weight gain. Leptin and insulin concentrations increased with weight gain. Mean ± SD insulin sensitivity decreased by 71 ± 28%, accompanied by a 408 ± 201% increase in acute insulin response to glucose, which resulted in similar disposition index before and after weight gain.

Conclusions and Clinical Relevance—Diet-induced weight gain in horses occurred concurrently with decreased insulin sensitivity that was effectively compensated for by an increase in insulin secretory response. Obesity resulted in hyperinsulinemia and hyperleptinemia, compared with baseline values, but no changes in lipid concentrations were apparent. Preventing obesity is a potential strategy to help avoid insulin resistance, hyperinsulinemia, and hyperleptinemia in horses.

Contributor Notes

Dr. Carter's present address is Department of Clinical Studies, New Bolton Center, School of Veterinary Medicine, University of Pennsylvania, Kennett Square, PA 19348.

Dr. McCutcheon's present address is Department of Pathobiology and Diagnostic Investigation, College of Veterinary Medicine, Michigan State University, East Lansing, MI 48824.

Dr. Geor's present address is Department of Large Animal Clinical Sciences, College of Veterinary Medicine, Michigan State University, East Lansing, MI 48824.

Supported by a grant from the Patricia Bonsall Stuart Fund and the John Lee Pratt Graduate Fellowship Program in Animal Nutrition at Virginia Tech.

Presented in part at the American College of Veterinary Internal Medicine Forum, San Antonio, Tex, July 2008.

Address correspondence to Dr. Carter (Carterre@vet.upenn.edu).
  • 1.

    Frank N, Elliott SB, Brandt LE, et al. Physical characteristics, blood hormone concentrations, and plasma lipid concentrations in obese horses with insulin resistance. J Am Vet Med Assoc 2006;228:13831390.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 2.

    Treiber KH, Kronfeld DS, Hess TM, et al. Evaluation of genetic and metabolic predispositions and nutritional risk factors for pasture-associated laminitis in ponies. J Am Vet Med Assoc 2006;228:15381545.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 3.

    Hoffman RM, Boston RC, Stefanovski D, et al. Obesity and diet affect glucose dynamics and insulin sensitivity in Thoroughbred geldings. J Anim Sci 2003;81:23332342.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 4.

    Vick MM, Adams AA, Murphy BA, et al. Relationships among inflammatory cytokines, obesity, and insulin sensitivity in the horse. J Anim Sci 2007;85:11441155.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 5.

    Jeffcott LB, Field JR, McLean JG, et al. Glucose tolerance and insulin sensitivity in ponies and Standardbred horses. Equine Vet J 1986;18:97101.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 6.

    Vick MM, Sessions DR, Murphy BA, et al. Obesity is associated with altered metabolic and reproductive activity in the mare: effects of metformin on insulin sensitivity and reproductive cyclicity. Reprod Fertil Dev 2006;18:609617.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 7.

    Johnson PJ. The equine metabolic syndrome peripheral Cushing's syndrome. Vet Clin North Am Equine Pract 2002;18:271293.

  • 8.

    Carter RA, Treiber KH, Geor RJ, et al. Prediction of incipient pasture-associated laminitis from hyperinsulinaemia, hyperleptinaemia and generalised and localised obesity in a cohort of ponies. Equine Vet J 2009;41:171178.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 9.

    Buff PR, Dodds AC, Morrison CD, et al. Leptin in horses: tissue localization and relationship between peripheral concentrations of leptin and body condition. J Anim Sci 2002;80:29422948.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 10.

    Carter RA, Geor RJ, Staniar WB, et al. Apparent adiposity assessed by standardised scoring systems and morphometric measurements in horses and ponies. Vet J 2009;179:204210.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 11.

    Donaldson MT, McDonnell SM, Schanbacher BJ, et al. Variation in plasma adrenocorticotropic hormone concentration and dexamethasone suppression test results with season, age, and sex in healthy ponies and horses. J Vet Intern Med 2005;19:217222.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 12.

    Henneke DR, Potter GD, Kreider JL, et al. Relationship between condition score, physical measurements and body fat percentage in mares. Equine Vet J 1983;15:371372.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 13.

    Westervelt RG, Stouffer JR, Hintz HF, et al. Estimating fatness in horses and ponies. J Anim Sci 1976;43:781785.

  • 14.

    Freestone JF, Wolfsheimer KJ, Kamerling SG, et al. Exercise induced hormonal and metabolic changes in Thoroughbred horses: effects of conditioning and acepromazine. Equine Vet J 1991;23:219223.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 15.

    McManus CJ, Fitzgerald BP. Effects of a single day of feed restriction on changes in serum leptin, gonadotropins, prolactin, and metabolites in aged and young mares. Domest Anim Endocrinol 2000;19:113.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 16.

    Boston RC, Stefanovski D, Moate PJ, et al. MINMOD Millennium: a computer program to calculate glucose effectiveness and insulin sensitivity from the frequently sampled intravenous glucose tolerance test. Diabetes Technol Ther 2003;5:10031015.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 17.

    Treiber KH, Boston RC, Kronfeld DS, et al. Insulin resistance and compensation in Thoroughbred weanlings adapted to highglycemic meals. J Anim Sci 2005;83:23572364.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 18.

    Surwit RS, Kuhn CM, Cochrane C, et al. Diet-induced type II diabetes in C57BL/6J mice. Diabetes 1988;37:11631167.

  • 19.

    Erdmann J, Kallabis B, Oppel U, et al. Development of hyperinsulinemia and insulin resistance during the early stage of weight gain. Am J Physiol Endocrinol Metab 2008;294:E568E575.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 20.

    Gayet C, Leray V, Saito M, et al. The effects of obesity-associated insulin resistance on mRNA expression of peroxisome proliferator-activated receptor-gamma target genes, in dogs. Br J Nutr 2007;98:497503.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 21.

    Zhao S, Chu Y, Zhang C, et al. Diet-induced central obesity and insulin resistance in rabbits. J Anim Physiol Anim Nutr (Berl) 2008;92:105111.

    • Search Google Scholar
    • Export Citation
  • 22.

    Gayet C, Bailhache E, Dumon H, et al. Insulin resistance and changes in plasma concentration of TNFalpha, IGF1, and NEFA in dogs during weight gain and obesity. J Anim Physiol Anim Nutr (Berl) 2004;88:157165.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 23.

    Chen H. Cellular inflammatory responses: novel insights for obesity and insulin resistance. Pharmacol Res 2006;53:469477.

  • 24.

    Delarue J, Magnan C. Free fatty acids and insulin resistance. Curr Opin Clin Nutr Metab Care 2007;10:142148.

  • 25.

    Bailey SR, Menzies-Gow NJ, Harris PA, et al. Effect of dietary fructans and dexamethasone administration on the insulin response of ponies predisposed to laminitis. J Am Vet Med Assoc 2007;231:13651373.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 26.

    Kasuga M. Insulin resistance and pancreatic beta cell failure. J Clin Invest 2006;116:17561760.

  • 27.

    Kearns CF, McKeever KH, Roegner V, et al. Adiponectin and leptin are related to fat mass in horses. Vet J 2006;172:460465.

  • 28.

    Cartmill JA, Thompson DL Jr, Storer WA, et al. Effect of dexamethasone, feeding time, and insulin infusion on leptin concentrations in stallions. J Anim Sci 2005;83:18751881.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 29.

    Cartmill JA, Thompson DL Jr, Storer WA, et al. Endocrine responses in mares and geldings with high body condition scores grouped by high vs. low resting leptin concentrations. J Anim Sci 2003;81:23112321.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 30.

    Weyenberg SV, Hesta M, Buyse J, et al. Short-term effects of energy changes on plasma leptin concentrations and glucose tolerance in healthy ponies. Vet J 2008;178:233237.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 31.

    Treiber KH, Hess TM, Kronfeld DS, et al. Insulin resistance and compensation in laminitis-predisposed ponies characterized by the minimal model. Pferdeheilkunde 2007;23:237240.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 32.

    Coffman JR, Colles CM. Insulin tolerance in laminitic ponies. Can J Comp Med 1983;47:347351.

  • 33.

    Bailey SR, Habershon-Butcher JL, Ransom KJ, et al. Hypertension and insulin resistance in a mixed-breed population of ponies predisposed to laminitis. Am J Vet Res 2008;69:122129.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 34.

    Asplin KE, Sillence MN, Pollitt CC, et al. Induction of laminitis by prolonged hyperinsulinaemia in clinically normal ponies. Vet J 2007;174:530535.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 35.

    Bailey SR, Marr CM, Elliott J. Current research and theories on the pathogenesis of acute laminitis in the horse. Vet J 2004;167:129142.

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