Maternal obesity increases insulin resistance, low-grade inflammation and osteochondrosis lesions in foals and yearlings until 18 months of age.
- Journal Article
- Research Support
- Non-U.S. Gov't
Summary
The research explores how maternal obesity in horses impacts the mother’s metabolism, inflammation, and the offspring’s growth, metabolism, inflammation, osteochondrotic lesions, and testicular maturation up to 18 months of age. It was shown that obesity in mother horses lead to increased insulin resistance and low-grade inflammation in their offspring and a higher risk of osteochondrosis.
Research Participants
- The study involved two groups of mares separated by their Body Condition Score (BCS) at the time of insemination. One group, referred to as Normal (N), included 10 mares with BCS less or equal to 4. The second group, Obese (O), consisted of 14 mares with BCS equal or greater than 4.25.
- These BCS and other health and metabolic indicators were monitored throughout gestation and later compared to evaluate the impact of maternal obesity.
Methods and Monitoring
- Researchers checked BCS and various serum and plasma concentrations throughout the pregnancy of mares, including glucose, insulin, triglyceride, urea, non-esterified fatty acid, serum amyloid A (SAA), leptin, and adiponectin.
- The Frequently Sampled Intravenous Glucose Tolerance Test (FSIGT) was administered at 300 days of gestation.
- Postpartum, researchers observed and measured offspring’s weight and size until they turned 18 months old, measuring different plasma light indicators at regular intervals.
- FSIGT and osteoarticular examinations were performed when the offspring became 6, 12, and 18 months old.
- Male foals were castrated at one year and genes associated with testicular maturation were analyzed.
Results
- The mares in the Obese group remained more obese throughout the study than those in the Normal group. During pregnancy, the Obese mares had lower levels of plasma urea and adiponectin, but higher levels of SAA and leptin. They were also more resistant to insulin, showing higher glucose effectiveness.
- Postpartum, offspring from Obese mares displayed higher plasma SAA concentrations until they were 6 months old, suggesting protracted inflammation and higher glucose effectiveness, indicating increased insulin resistance.
- By the time they were 12 months old, these offspring were significantly more affected by osteochondrosis than their counterparts from the Normal group.
Conclusion
This study’s results show that maternal obesity in horses leads to metabolic alterations and increased low-grade inflammation in both mothers and offspring. Furthermore, offspring born to obese mares have a higher risk of developing osteochondrosis by the time they are 12 months old.
Cite This Article
Publication
Researcher Affiliations
- UMR BDR, INRA, ENVA, Université Paris Saclay, Jouy en Josas, France.
- UMR BDR, INRA, ENVA, Université Paris Saclay, Jouy en Josas, France.
- Normandie Univ, UNICAEN, EA2608, OeReCa, USC-INRA, Caen, France.
- Clinique Equine, Faculté de Médecine Vétérinaire, Université de Liège, Liège, Belgium.
- IFCE, Station Expérimentale de la Valade, Chamberet, France.
- UMR BDR, INRA, ENVA, Université Paris Saclay, Jouy en Josas, France.
- UMR BDR, INRA, ENVA, Université Paris Saclay, Jouy en Josas, France.
- UMR BDR, INRA, ENVA, Université Paris Saclay, Jouy en Josas, France.
- Clinique Equine, Faculté de Médecine Vétérinaire, Université de Liège, Liège, Belgium.
- Clinique Equine, Faculté de Médecine Vétérinaire, Université de Liège, Liège, Belgium.
- Normandie Univ, UNICAEN, EA2608, OeReCa, USC-INRA, Caen, France.
- INRA, UMR Toxalim, Research Center in Food Toxicology, Toulouse, France.
- IFCE, Station Expérimentale de la Valade, Chamberet, France.
- Normandie Univ, UNICAEN, EA2608, OeReCa, USC-INRA, Caen, France.
- Clinique Equine, Faculté de Médecine Vétérinaire, Université de Liège, Liège, Belgium.
- UMR BDR, INRA, ENVA, Université Paris Saclay, Jouy en Josas, France.
- UMR BDR, INRA, ENVA, Université Paris Saclay, Jouy en Josas, France.
MeSH Terms
- Adiponectin / blood
- Animals
- Animals, Newborn
- Blood Glucose / metabolism
- Female
- Glucose Tolerance Test
- Horse Diseases / pathology
- Horse Diseases / physiopathology
- Horses
- Inflammation / etiology
- Inflammation / veterinary
- Insulin / blood
- Insulin Resistance / physiology
- Leptin / blood
- Male
- Maternal-Fetal Exchange
- Obesity / complications
- Obesity / physiopathology
- Obesity / veterinary
- Osteochondrosis / etiology
- Osteochondrosis / veterinary
- Pregnancy
- Pregnancy Complications / pathology
- Pregnancy Complications / physiopathology
- Pregnancy Complications / veterinary
Conflict of Interest Statement
References
- Barker DJ. The origins of the developmental origins theory.. J Intern Med 2007 May;261(5):412-7.
- Hanson MA, Gluckman PD. Early developmental conditioning of later health and disease: physiology or pathophysiology?. Physiol Rev 2014 Oct;94(4):1027-76.
- Chavatte-Palmer P, Tarrade A, Kiefer H, Duranthon V, Jammes H. Breeding animals for quality products: not only genetics.. Reprod Fertil Dev 2016;28(1-2):94-111.
- McMullen S, Mostyn A. Animal models for the study of the developmental origins of health and disease.. Proc Nutr Soc 2009 Aug;68(3):306-20.
- Peugnet P, Robles M, Wimel L, Tarrade A, Chavatte-Palmer P. Management of the pregnant mare and long-term consequences on the offspring.. Theriogenology 2016 Jul 1;86(1):99-109.
- Arnaud G, Perret G, Dubroeucq H, Rivot D. Notation de l’état corporel des chevaux de selle et de sport—Guide pratique. Quae: Institut de l’élevage; 1997.
- Henneke D, Potter G, Kreider J. Body condition during pregnancy and lactation and reproductive efficiency of mares. Theriogenology 1984;21: 897‑909.
- Henneke DR, Potter GD, Kreider JL, Yeates BF. Relationship between condition score, physical measurements and body fat percentage in mares.. Equine Vet J 1983 Oct;15(4):371-2.
- Martin-Rosset W, Vernet J, Dubroeucq H, Arnaud G, Picard A, Vermorel M. Variation of fatness and energy content of the body with body condition score in sport horses and its prediction. In: Saastamoinen M, Martin-Rosset W, éditeurs. Nutrition of the Exercising Horse. Vilnius: Wageningen Academic Publishers; 2008. p. 167–176.
- Luna D, Vásquez R, Rojas M, Tadich T. Welfare Status of Working Horses and Owners′ Perceptions of Their Animals. Animals Multidisciplinary Digital Publishing Institute; 2017;7: 56.
- Giles SL, Rands SA, Nicol CJ, Harris PA. Obesity prevalence and associated risk factors in outdoor living domestic horses and ponies.. PeerJ 2014;2:e299.
- Potter SJ, Bamford NJ, Harris PA, Bailey SR. Prevalence of obesity and owners' perceptions of body condition in pleasure horses and ponies in south-eastern Australia.. Aust Vet J 2016 Nov;94(11):427-432.
- Jensen RB, Danielsen SH, Tauson AH. Body condition score, morphometric measurements and estimation of body weight in mature Icelandic horses in Denmark.. Acta Vet Scand 2016 Oct 20;58(Suppl 1):59.
- Wyse CA, McNie KA, Tannahill VJ, Murray JK, Love S. Prevalence of obesity in riding horses in Scotland.. Vet Rec 2008 May 3;162(18):590-1.
- Thatcher CD, Pleasant RS, Geor RJ, Elvinger F. Prevalence of overconditioning in mature horses in southwest Virginia during the summer.. J Vet Intern Med 2012 Nov-Dec;26(6):1413-8.
- Hansen A, Catalano D, Coleman R, Hathaway M, McCue M, Rendahl A. Demographics, body condition scores, and owner bodyweight estimations of adult draft and warmblood horse breeds. J Equine Vet Sci 2015;35: 389.
- Wood S, Allen E, Corr A, Lee M, Magee A. Ability of horse and pony owners to estimate body weight and assess body condition score. European Equine Health & Nutrition Congress; 8th Edition 2016. p. 124‑126.
- Harker I, Harris P, Barfoot C. The body condition score of leisure horses competing at an unaffiliated championship in the UK. J Equine Vet Sci 2011;31: 253‑254.
- Fernandes K, Rogers C, Gee E, Bolwell C, Thomas D. Body condition and morphometric measures of adiposity in a cohort of Pony Club horses and ponies in New Zealand. Proceedings of the New Zealand Society of Animal Production Dudenin; 2015. p. 195‑199.
- Ireland JL, Wylie CE, Collins SN, Verheyen KL, Newton JR. Preventive health care and owner-reported disease prevalence of horses and ponies in Great Britain.. Res Vet Sci 2013 Oct;95(2):418-24.
- Stephenson HM, Green MJ, Freeman SL. Prevalence of obesity in a population of horses in the UK.. Vet Rec 2011 Feb 5;168(5):131.
- Christie JL, Hewson CJ, Riley CB, McNiven MA, Dohoo IR, Bate LA. Management factors affecting stereotypies and body condition score in nonracing horses in Prince Edward Island.. Can Vet J 2006 Feb;47(2):136-43.
- Honoré E, Uhlinger C. Equine feeding practices in central north carolina: a preliminary survey. J equine Vet Sci 1994;14: 425‑429.
- Ireland JL, Clegg PD, McGowan CM, McKane SA, Chandler KJ, Pinchbeck GL. Comparison of owner-reported health problems with veterinary assessment of geriatric horses in the United Kingdom.. Equine Vet J 2012 Jan;44(1):94-100.
- Robin CA, Ireland JL, Wylie CE, Collins SN, Verheyen KL, Newton JR. Prevalence of and risk factors for equine obesity in Great Britain based on owner-reported body condition scores.. Equine Vet J 2015 Mar;47(2):196-201.
- Visser EK, Neijenhuis F, de Graaf-Roelfsema E, Wesselink HG, de Boer J, van Wijhe-Kiezebrink MC, Engel B, van Reenen CG. Risk factors associated with health disorders in sport and leisure horses in the Netherlands.. J Anim Sci 2014 Feb;92(2):844-55.
- Jensen R, Danielsen S, Tauson A-H. The prevalence of obesity in mature Icelandic horses in Denmark. Acta Vet Scand 2015;57: 2015.
- Morrison P, Harris P, Maltin C, Grove-white D, Argo C, Barfoot C. Perceptions of obesity in a UK leisure-based population of horse owners. Acta Vet Scand 2015;57: 2015.
- Arnold W, Ruf T, Kuntz R. Seasonal adjustment of energy budget in a large wild mammal, the Przewalski horse (Equus ferus przewalskii) II. Energy expenditure.. J Exp Biol 2006 Nov;209(Pt 22):4566-73.
- Dawson M, Hone J. Demography and dynamics of three wild horse populations in the australian alps. Austral Ecol 2012;37: 97‑109.
- Giles SL, Nicol CJ, Rands SA, Harris PA. Assessing the seasonal prevalence and risk factors for nuchal crest adiposity in domestic horses and ponies using the Cresty Neck Score.. BMC Vet Res 2015 Jan 31;11:13.
- Hitchens PL, Hultgren J, Frössling J, Emanuelson U, Keeling LJ. Prevalence and risk factors for overweight horses at premises in Sweden assessed using official animal welfare control data.. Acta Vet Scand 2016 Oct 20;58(Suppl 1):61.
- Giles S, Nicol C, Rands S, Harris P. Fat all year round—The welfare consequences of continuous equine obesity. Recent advances in animal welfare science—UFAW Animal Welfare Conference. Science in the Service of Animal Welfare 2012. p. 33.
- Bamford NJ, Potter SJ, Baskerville CL, Harris PA, Bailey SR. Effect of increased adiposity on insulin sensitivity and adipokine concentrations in different equine breeds adapted to cereal-rich or fat-rich meals.. Vet J 2016 Aug;214:14-20.
- Frank N, Elliott SB, Brandt LE, Keisler DH. Physical characteristics, blood hormone concentrations, and plasma lipid concentrations in obese horses with insulin resistance.. J Am Vet Med Assoc 2006 May 1;228(9):1383-90.
- Powell DM, Reedy SE, Sessions DR, Fitzgerald BP. Effect of short-term exercise training on insulin sensitivity in obese and lean mares.. Equine Vet J Suppl 2002 Sep;(34):81-4.
- Jansson A, Stéfansdóttir GJ, Ragnarsson S. Plasma insulin concentration increases linearly with body condition in Icelandic horses.. Acta Vet Scand 2016 Nov 9;58(1):76.
- Hoffman RM, Boston RC, Stefanovski D, Kronfeld DS, Harris PA. Obesity and diet affect glucose dynamics and insulin sensitivity in Thoroughbred geldings.. J Anim Sci 2003 Sep;81(9):2333-42.
- Vick MM, Adams AA, Murphy BA, Sessions DR, Horohov DW, Cook RF, Shelton BJ, Fitzgerald BP. Relationships among inflammatory cytokines, obesity, and insulin sensitivity in the horse.. J Anim Sci 2007 May;85(5):1144-55.
- Suagee JK, Corl BA, Crisman MV, Pleasant RS, Thatcher CD, Geor RJ. Relationships between body condition score and plasma inflammatory cytokines, insulin, and lipids in a mixed population of light-breed horses.. J Vet Intern Med 2013 Jan-Feb;27(1):157-63.
- Frank N, Geor R, Bailey S, Durham A, Johnson P. Equine metabolic syndrome. J Vet Intern Med 2010;19: 1‑13.
- Menzies-Gow NJ, Stevens K, Barr A, Camm I, Pfeiffer D, Marr CM. Severity and outcome of equine pasture-associated laminitis managed in first opinion practice in the UK.. Vet Rec 2010 Sep 4;167(10):364-9.
- Kearns CF, McKeever KH, Kumagai K, Abe T. Fat-free mass is related to one-mile race performance in elite standardbred horses.. Vet J 2002 May;163(3):260-6.
- Lawrence L, Jackson S, Kline K, Moser L, Powell D, Biel M. Observations in body weight and condition of horses in a 150-mile endurance ride. Equine Vet Sci 1992;12: 320‑324.
- Fitzgerald BP, McManus CJ. Photoperiodic versus metabolic signals as determinants of seasonal anestrus in the mare.. Biol Reprod 2000 Jul;63(1):335-40.
- Morley S, Murray J-A. Effects of Body Condition Score on the Reproductive Physiology of the Broodmare: A Review. J Equine Vet Sci Elsevier Ltd; 2014;34: 842‑853.
- Kubiak J, Evans J, Potter G, Harms P, Jenkins W. Parturition in the multiparous mare fed to obesity. Equine Vet Sci 1988;8: 135‑140.
- Kubiak JRR, Evans JWW, Potter GDD, Harms PGG, Jenkins WLL. Milk yield composition in the multiparous mare fed to obesity. Equine Vet Sci 1991;11: 158‑162.
- Martin-Rosset W. Nutrition et alimentation des chevaux: Nouvelles recommandations alimentaires de l’Inra. Versailles: Éditions Quæ; 2012.
- Bergman RN. Lilly lecture 1989. Toward physiological understanding of glucose tolerance. Minimal-model approach.. Diabetes 1989 Dec;38(12):1512-27.
- Robles M, Gautier C, Mendoza L, Peugnet P, Dubois C, Dahirel M, Lejeune JP, Caudron I, Guenon I, Camous S, Tarrade A, Wimel L, Serteyn D, Bouraima-Lelong H, Chavatte-Palmer P. Maternal Nutrition during Pregnancy Affects Testicular and Bone Development, Glucose Metabolism and Response to Overnutrition in Weaned Horses Up to Two Years.. PLoS One 2017;12(1):e0169295.
- Bergman RN, Phillips LS, Cobelli C. Physiologic evaluation of factors controlling glucose tolerance in man: measurement of insulin sensitivity and beta-cell glucose sensitivity from the response to intravenous glucose.. J Clin Invest 1981 Dec;68(6):1456-67.
- Bergman RN. Minimal model: perspective from 2005.. Horm Res 2005;64 Suppl 3:8-15.
- Boston RC, Stefanovski D, Moate PJ, Sumner AE, Watanabe RM, Bergman RN. 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(6):1003-15.
- Almeida J, Conley AJ, Mathewson L, Ball BA. Expression of steroidogenic enzymes during equine testicular development.. Reproduction 2011 Jun;141(6):841-8.
- Rode K, Sieme H, Richterich P, Brehm R. Characterization of the equine blood-testis barrier during tubular development in normal and cryptorchid stallions.. Theriogenology 2015 Sep 15;84(5):763-72.
- Almeida J, Conley AJ, Mathewson L, Ball BA. Expression of anti-Müllerian hormone, cyclin-dependent kinase inhibitor (CDKN1B), androgen receptor, and connexin 43 in equine testes during puberty.. Theriogenology 2012 Mar 15;77(5):847-57.
- Ball BA. Oxidative stress, osmotic stress and apoptosis: impacts on sperm function and preservation in the horse.. Anim Reprod Sci 2008 Sep;107(3-4):257-67.
- Vander Heyden L, Lejeune JP, Caudron I, Detilleux J, Sandersen C, Chavatte P, Paris J, Deliège B, Serteyn D. Association of breeding conditions with prevalence of osteochondrosis in foals.. Vet Rec 2013 Jan 19;172(3):68.
- Vander Heyden L, Lejeune JP, Caudron I, Detilleux J, Sandersen C, Chavatte P, Paris J, Deliège B, Serteyn D. Association of breeding conditions with prevalence of osteochondrosis in foals.. Vet Rec 2013 Jan 19;172(3):68.
- van Weeren P. Etiology, Diagnosis, and Treatment of OC(D). Clin Tech Equine Pract 2006;5: 248‑258.
- Denoix J. Sémiologie radiographique générale des articulations. Prat Vétérinaire Equine 1990;22: 14‑27.
- Fox J, Weisberg S. An {R} Companion to Applied Regression, Second Edition. Sage; 2011.
- Pinheiro J, Bates D, DebRoy S, Sarkar D, Core Team R. nlme: Linear and Nonlinear Mixed Effects Models. [Internet]. R package version 2.1–131. 2017. Consulté: https://cran.r-project.org/package=nlme.
- Lenth R V. Least-Squares Means: The R Package lsmeans. J Stat Softw 2016;69: 1‑33.
- Lê S, Josse J, Husson F. FactoMineR: An R Package for Multivariate Analysis. J Stat Softw 2008;25: 1‑18.
- Gentry LR, Thompson DL Jr, Gentry GT Jr, Davis KA, Godke RA, Cartmill JA. The relationship between body condition, leptin, and reproductive and hormonal characteristics of mares during the seasonal anovulatory period.. J Anim Sci 2002 Oct;80(10):2695-703.
- Kearns CF, McKeever KH, Roegner V, Brady SM, Malinowski K. Adiponectin and leptin are related to fat mass in horses.. Vet J 2006 Nov;172(3):460-5.
- Buff PR, Dodds AC, Morrison CD, Whitley NC, McFadin EL, Daniel JA, Djiane J, Keisler DH. Leptin in horses: tissue localization and relationship between peripheral concentrations of leptin and body condition.. J Anim Sci 2002 Nov;80(11):2942-8.
- Bamford NJ, Potter SJ, Harris PA, Bailey SR. Effect of increased adiposity on insulin sensitivity and adipokine concentrations in horses and ponies fed a high fat diet, with or without a once daily high glycaemic meal.. Equine Vet J 2016 May;48(3):368-73.
- Cartmill JA, Thompson DL Jr, Storer WA, Gentry LR, Huff NK. Endocrine responses in mares and geldings with high body condition scores grouped by high vs. low resting leptin concentrations.. J Anim Sci 2003 Sep;81(9):2311-21.
- Wu X, Motoshima H, Mahadev K, Stalker TJ, Scalia R, Goldstein BJ. Involvement of AMP-activated protein kinase in glucose uptake stimulated by the globular domain of adiponectin in primary rat adipocytes.. Diabetes 2003 Jun;52(6):1355-63.
- Yamauchi T, Kamon J, Minokoshi Y, Ito Y, Waki H, Uchida S, Yamashita S, Noda M, Kita S, Ueki K, Eto K, Akanuma Y, Froguel P, Foufelle F, Ferre P, Carling D, Kimura S, Nagai R, Kahn BB, Kadowaki T. Adiponectin stimulates glucose utilization and fatty-acid oxidation by activating AMP-activated protein kinase.. Nat Med 2002 Nov;8(11):1288-95.
- Yokota T, Oritani K, Takahashi I, Ishikawa J, Matsuyama A, Ouchi N, Kihara S, Funahashi T, Tenner AJ, Tomiyama Y, Matsuzawa Y. Adiponectin, a new member of the family of soluble defense collagens, negatively regulates the growth of myelomonocytic progenitors and the functions of macrophages.. Blood 2000 Sep 1;96(5):1723-32.
- Wolf AM, Wolf D, Rumpold H, Enrich B, Tilg H. Adiponectin induces the anti-inflammatory cytokines IL-10 and IL-1RA in human leukocytes.. Biochem Biophys Res Commun 2004 Oct 15;323(2):630-5.
- Tsatsanis C, Zacharioudaki V, Androulidaki A, Dermitzaki E, Charalampopoulos I, Minas V, Gravanis A, Margioris AN. Adiponectin induces TNF-alpha and IL-6 in macrophages and promotes tolerance to itself and other pro-inflammatory stimuli.. Biochem Biophys Res Commun 2005 Oct 7;335(4):1254-63.
- Engeli S, Feldpausch M, Gorzelniak K, Hartwig F, Heintze U, Janke J, Möhlig M, Pfeiffer AF, Luft FC, Sharma AM. Association between adiponectin and mediators of inflammation in obese women.. Diabetes 2003 Apr;52(4):942-7.
- Ouchi N, Kihara S, Funahashi T, Nakamura T, Nishida M, Kumada M, Okamoto Y, Ohashi K, Nagaretani H, Kishida K, Nishizawa H, Maeda N, Kobayashi H, Hiraoka H, Matsuzawa Y. Reciprocal association of C-reactive protein with adiponectin in blood stream and adipose tissue.. Circulation 2003 Feb 11;107(5):671-4.
- Klop B, Elte JW, Cabezas MC. Dyslipidemia in obesity: mechanisms and potential targets.. Nutrients 2013 Apr 12;5(4):1218-40.
- Smith S, Marr CM, Dunnett C, Menzies-Gow NJ. The effect of mare obesity and endocrine function on foal birthweight in Thoroughbreds.. Equine Vet J 2017 Jul;49(4):461-466.
- Pleasant RS, Suagee JK, Thatcher CD, Elvinger F, Geor RJ. Adiposity, plasma insulin, leptin, lipids, and oxidative stress in mature light breed horses.. J Vet Intern Med 2013 May-Jun;27(3):576-82.
- Barber T, Viña JR, Viña J, Cabo J. Decreased urea synthesis in cafeteria-diet-induced obesity in the rat.. Biochem J 1985 Sep 15;230(3):675-81.
- He Q, Ren P, Kong X, Wu Y, Wu G, Li P, Hao F, Tang H, Blachier F, Yin Y. Comparison of serum metabolite compositions between obese and lean growing pigs using an NMR-based metabonomic approach.. J Nutr Biochem 2012 Feb;23(2):133-9.
- Wijekoon EP, Skinner C, Brosnan ME, Brosnan JT. Amino acid metabolism in the Zucker diabetic fatty rat: effects of insulin resistance and of type 2 diabetes.. Can J Physiol Pharmacol 2004 Jul;82(7):506-14.
- Carter RA, McCutcheon LJ, Valle E, Meilahn EN, Geor RJ. Effects of exercise training on adiposity, insulin sensitivity, and plasma hormone and lipid concentrations in overweight or obese, insulin-resistant horses.. Am J Vet Res 2010 Mar;71(3):314-21.
- Peugnet P, Wimel L, Duchamp G, Sandersen C, Camous S, Guillaume D, Dahirel M, Dubois C, Jouneau L, Reigner F, Berthelot V, Chaffaux S, Tarrade A, Serteyn D, Chavatte-Palmer P. Enhanced or reduced fetal growth induced by embryo transfer into smaller or larger breeds alters post-natal growth and metabolism in pre-weaning horses.. PLoS One 2014;9(7):e102044.
- Irvine CH, Evans MJ. Postnatal changes in total and free thyroxine and triiodothyronine in foal serum.. J Reprod Fertil Suppl 1975 Oct;(23):709-15.
- Malinowski K, Christensen RA, Hafs HD, Scanes CG. Age and breed differences in thyroid hormones, insulin-like growth factor (IGF)-I and IGF binding proteins in female horses.. J Anim Sci 1996 Aug;74(8):1936-42.
- Murray MJ, Luba NK. Plasma gastrin and somatostatin, and serum thyroxine (T4), triiodothyronine (T3), reverse triiodothyronine (rT3) and cortisol concentrations in foals from birth to 28 days of age.. Equine Vet J 1993 May;25(3):237-9.
- Furr MO, Murray MJ, Ferguson DC. The effects of stress on gastric ulceration, T3, T4, reverse T3 and cortisol in neonatal foals.. Equine Vet J 1992 Jan;24(1):37-40.
- Rossdale PD. A clinician's view of prematurity and dysmaturity in thoroughbred foals.. Proc R Soc Med 1976 Sep;69(9):631-2.
- Frank N, Sojka JE, Patterson BW, Wood KV, Bonham CC, Latour MA. Effect of hypothyroidism on kinetics of metabolism of very-low-density lipoprotein in mares.. Am J Vet Res 2003 Aug;64(8):1052-8.
- Wagner MS, Wajner SM, Maia AL. The role of thyroid hormone in testicular development and function.. J Endocrinol 2008 Dec;199(3):351-65.
- Pitetti JL, Calvel P, Zimmermann C, Conne B, Papaioannou MD, Aubry F, Cederroth CR, Urner F, Fumel B, Crausaz M, Docquier M, Herrera PL, Pralong F, Germond M, Guillou F, Jégou B, Nef S. An essential role for insulin and IGF1 receptors in regulating sertoli cell proliferation, testis size, and FSH action in mice.. Mol Endocrinol 2013 May;27(5):814-27.
- Cymbaluk NF, Laarveld B. The ontogeny of serum insulin-like growth factor-I concentration in foals: effects of dam parity, diet, and age at weaning.. Domest Anim Endocrinol 1996 May;13(3):197-209.
- Kędzierski W, Kusy R, Kowalik S. Plasma leptin level in hyperlipidemic mares and their newborn foals.. Reprod Domest Anim 2011 Apr;46(2):275-80.
- Cavinder C, Burns S, Coverdale J, Hammer C, Holub G, Hinrichs K. Late gestational nutrition of the mare and potential effects on endocrine profiles and adrenal function of the offspring. Prof Anim Sci Elsevier Masson SAS; 2012;28: 344‑350.
- Bilbo SD, Tsang V. Enduring consequences of maternal obesity for brain inflammation and behavior of offspring.. FASEB J 2010 Jun;24(6):2104-15.
- Deardorff J, Smith LH, Petito L, Kim H, Abrams BF. Maternal Prepregnancy Weight and Children's Behavioral and Emotional Outcomes.. Am J Prev Med 2017 Oct;53(4):432-440.
- Peugnet P, Robles M, Mendoza L, Wimel L, Dubois C, Dahirel M, Guillaume D, Camous S, Berthelot V, Toquet MP, Richard E, Sandersen C, Chaffaux S, Lejeune JP, Tarrade A, Serteyn D, Chavatte-Palmer P. Effects of moderate amounts of barley in late pregnancy on growth, glucose metabolism and osteoarticular status of pre-weaning horses.. PLoS One 2015;10(4):e0122596.
- Mendoza L, Lejeune JP, Caudron I, Detilleux J, Sandersen C, Deliège B, Serteyn D. Impact of feeding and housing on the development of osteochondrosis in foals-A longitudinal study.. Prev Vet Med 2016 May 1;127:10-4.
- Ralston S. Postprandial hyperglycemica/hyperinsulinemia in young horses with osteochondritis dissecans lesions. Pferdeheilkunde 1996; 320‑322.
- Pagan JD, Geor RJ, Caddel SE, Pryor PB, Hoekstra KE. The Relationship Between Glycemic Response and the Incidence of OCD in Thoroughbred Weanlings: A Field Study. Proceedings of the 47th AAEP Annual Convention 2001. p. 322‑325. Consulté: http://citeseerx.ist.psu.edu/viewdoc/download?doi=10.1.1.459.5459&rep=rep1&type=pdf.
- Fulzele K, Riddle RC, DiGirolamo DJ, Cao X, Wan C, Chen D, Faugere MC, Aja S, Hussain MA, Brüning JC, Clemens TL. Insulin receptor signaling in osteoblasts regulates postnatal bone acquisition and body composition.. Cell 2010 Jul 23;142(2):309-19.
- Yang J, Zhang X, Wang W, Liu J. Insulin stimulates osteoblast proliferation and differentiation through ERK and PI3K in MG-63 cells.. Cell Biochem Funct 2010 Jun;28(4):334-41.
- Pramojanee SN, Phimphilai M, Kumphune S, Chattipakorn N, Chattipakorn SC. Decreased jaw bone density and osteoblastic insulin signaling in a model of obesity.. J Dent Res 2013 Jun;92(6):560-5.
- Pramojanee SN, Phimphilai M, Chattipakorn N, Chattipakorn SC. Possible roles of insulin signaling in osteoblasts.. Endocr Res 2014;39(4):144-51.
- Phornphutkul C, Wu KY, Gruppuso PA. The role of insulin in chondrogenesis.. Mol Cell Endocrinol 2006 Apr 25;249(1-2):107-15.
- Henson FM, Davenport C, Butler L, Moran I, Shingleton WD, Jeffcott LB, Schofield PN. Effects of insulin and insulin-like growth factors I and II on the growth of equine fetal and neonatal chondrocytes.. Equine Vet J 1997 Nov;29(6):441-7.
- Maor G, Silbermann M, von der Mark K, Heingard D, Laron Z. Insulin enhances the growth of cartilage in organ and tissue cultures of mouse neonatal mandibular condyle.. Calcif Tissue Int 1993 Apr;52(4):291-9.
- Kaneshiro S, Ebina K, Shi K, Higuchi C, Hirao M, Okamoto M, Koizumi K, Morimoto T, Yoshikawa H, Hashimoto J. IL-6 negatively regulates osteoblast differentiation through the SHP2/MEK2 and SHP2/Akt2 pathways in vitro.. J Bone Miner Metab 2014 Jul;32(4):378-92.
- Hughes CK, Xie MM, McCoski SR, Ealy AD. Activities for leptin in bovine trophoblast cells.. Domest Anim Endocrinol 2017 Jan;58:84-89.
- Mera P, Laue K, Ferron M, Confavreux C, Wei J, Galán-Díez M, Lacampagne A, Mitchell SJ, Mattison JA, Chen Y, Bacchetta J, Szulc P, Kitsis RN, de Cabo R, Friedman RA, Torsitano C, McGraw TE, Puchowicz M, Kurland I, Karsenty G. Osteocalcin Signaling in Myofibers Is Necessary and Sufficient for Optimum Adaptation to Exercise.. Cell Metab 2016 Jun 14;23(6):1078-1092.
- Parameswaran N, Patial S. Tumor necrosis factor-α signaling in macrophages.. Crit Rev Eukaryot Gene Expr 2010;20(2):87-103.
- Serteyn D, Piquemal D, Vanderheyden L, Lejeune JP, Verwilghen D, Sandersen C. Gene expression profiling from leukocytes of horses affected by osteochondrosis.. J Orthop Res 2010 Jul;28(7):965-70.
- Hines K, Hodge S, Kreider J, Potter G, Harms P. Relationship between body condition and levels of serum luteinizing hormone in postpartum mares. Theriogenology 1987;28: 815‑825.
- Sutton E, Bowland J, Ratcliff W. Influence of level of energy and nutrient intake by Mares on Reproductive Performance and on Blood Serum Composition of the Mares and Foals. Can J Anim Sci 1977;57: 551‑558.
- Wilsher S, Allen WR. Effects of a Streptococcus equi infection--mediated nutritional insult during mid-gestation in primiparous Thoroughbred fillies. Part 1: placental and fetal development.. Equine Vet J 2006 Nov;38(6):549-57.
- Bamford NJ, Potter SJ, Harris PA, Bailey SR. Breed differences in insulin sensitivity and insulinemic responses to oral glucose in horses and ponies of moderate body condition score.. Domest Anim Endocrinol 2014 Apr;47:101-7.
- Treiber KH, Kronfeld DS, Hess TM, Byrd BM, Splan RK, Staniar WB. Evaluation of genetic and metabolic predispositions and nutritional risk factors for pasture-associated laminitis in ponies.. J Am Vet Med Assoc 2006 May 15;228(10):1538-45.
Citations
This article has been cited 6 times.- Hallman I, Karikoski N, Kareskoski M. The effects of obesity and insulin dysregulation on mare reproduction, pregnancy, and foal health: a review.. Front Vet Sci 2023;10:1180622.
- Smieszek A, Marcinkowska K, Pielok A, Sikora M, Valihrach L, Carnevale E, Marycz K. Obesity Affects the Proliferative Potential of Equine Endometrial Progenitor Cells and Modulates Their Molecular Phenotype Associated with Mitochondrial Metabolism.. Cells 2022 Apr 24;11(9).
- Ahmadi F, Mirshahi A, Mohri M, Sardari K, Sharifi K. Osteochondrosis dissecans (OCD) in horses: hormonal and biochemical study (19 cases).. Vet Res Forum 2021;12(3):325-331.
- D' Fonseca NMM, Gibson CME, van Doorn DA, Roelfsema E, de Ruijter-Villani M, Stout TAE. Effect of Overfeeding Shetland Pony Mares on Embryonic Glucose and Lipid Accumulation, and Expression of Imprinted Genes.. Animals (Basel) 2021 Aug 26;11(9).
- Robles M, Couturier-Tarrade A, Derisoud E, Geeverding A, Dubois C, Dahirel M, Aioun J, Prezelin A, Calvez J, Richard C, Wimel L, Chavatte-Palmer P. Effects of dietary arginine supplementation in pregnant mares on maternal metabolism, placental structure and function and foal growth.. Sci Rep 2019 Apr 23;9(1):6461.
- Durham AE, Frank N, McGowan CM, Menzies-Gow NJ, Roelfsema E, Vervuert I, Feige K, Fey K. ECEIM consensus statement on equine metabolic syndrome.. J Vet Intern Med 2019 Mar;33(2):335-349.