FREE SHIPPING over $40
OVER 10000 FIVE-STAR REVIEWS
5% OFF ALL SUBSCRIPTIONS
100% HAPPINESS GUARANTEE
Analyze Diet
0
PloS one2014; 9(7); e102044; doi: 10.1371/journal.pone.0102044

Enhanced or reduced fetal growth induced by embryo transfer into smaller or larger breeds alters post-natal growth and metabolism in pre-weaning horses.

Abstract: In equids, placentation is diffuse and nutrient supply to the fetus is determined by uterine size. This correlates with maternal size and affects intra-uterine development and subsequent post-natal growth, as well as insulin sensitivity in the newborn. Long-term effects remain to be described. In this study, fetal growth was enhanced or restricted through ET using pony (P), saddlebred (S) and draft (D) horses. Control P-P (n = 21) and S-S (n = 28) pregnancies were obtained by AI. Enhanced and restricted pregnancies were obtained by transferring P or S embryos into D mares (P-D, n = 6 and S-D, n = 8) or S embryos into P mares (S-P, n = 6), respectively. Control and experimental foals were raised by their dams and recipient mothers, respectively. Weight gain, growth hormones and glucose homeostasis were investigated in the foals from birth to weaning. Fetal growth was enhanced in P-D and these foals remained consistently heavier, with reduced T3 concentrations until weaning compared to P-P. P-D had lower fasting glucose from days 30 to 200 and higher insulin secretion than P-P after IVGTT on day 3. Euglycemic clamps in the immediate post-weaning period revealed no difference in insulin sensitivity between P-D and P-P. Fetal growth was restricted in S-P and these foals remained consistently lighter until weaning compared to S-D, with elevated T3 concentrations in the newborn compared to S-S. S-P exhibited higher fasting glycemia than S-S and S-D from days 30 to 200. They had higher maximum increment in plasma glucose than S-D after IVGTT on day 3 and clamps on day 200 demonstrated higher insulin sensitivity compared to S-D. Neither the restricted nor the enhanced fetal environment affected IGF-1 concentrations. Thus, enhanced and restricted fetal and post-natal environments had combined effects that persisted until weaning. They induced different adaptive responses in post-natal glucose metabolism: an early insulin-resistance was induced in enhanced P-D, while S-P developed increased insulin sensitivity.
Get Full Text
Publication Date: 2014-07-09 PubMed ID: 25006665PubMed Central: PMC4090198DOI: 10.1371/journal.pone.0102044Google Scholar: Lookup
The Equine Research Bank provides access to a large database of publicly available scientific literature. Inclusion in the Research Bank does not imply endorsement of study methods or findings by Mad Barn.
LinkedInCopy
  • Journal Article
  • Research Support
  • Non-U.S. Gov't

Summary

This research summary has been generated with artificial intelligence and may contain errors and omissions. Refer to the original study to confirm details provided. Submit correction.

The research investigates how the alteration of fetal growth, by transferring an embryo onto a larger or smaller breed, affects the post-birth growth and metabolism of pre-weaning horses. The study concludes that both enhanced and restricted fetal environments have effects that last until weaning, inducing different responses in post-birth glucose metabolism.

Methodology

  • The study was conducted on three different types of horses: pony (P), saddlebred (S) and draft (D).
  • Control pregnancies were obtained through artificial insemination in ponies (P-P) and saddlebred horses (S-S). Enhanced and restricted pregnancies were created by transferring pony or saddlebred embryos into a draft mare (P-D and S-D), or by transferring a saddlebred embryo into a pony mare (S-P).
  • The foals were monitored from birth to weaning, assessing their weight gain, growth hormone levels, and glucose metabolism.

Observations

  • Pony embryos transferred to draft mares (P-D) resulted in enhanced fetal growth and the foals remained heavier than control ponies (P-P) up to weaning.
  • These P-D foals showed reduced T3 hormone concentrations and lower fasting glucose levels compared to P-P. They also showed higher insulin secretion after an intravenous glucose tolerance test performed on day 3.
  • Saddlebred embryos transferred into a pony mare (S-P) resulted in restricted fetal growth, and these foals remained lighter until weaning compared to those where saddlebred embryos were transferred to draft mares (S-D).
  • The S-P foals also exhibited higher fasting glycemia, a higher maximum increase in plasma glucose after the 3rd day IVGTT, and higher insulin sensitivity compared to S-D.
  • The Insulin-like growth factor 1 (IGF-1) concentrations remained unaffected in both enhanced and restricted fetal environments.

Conclusion

  • The findings suggest that the manipulation of fetal growth through embryo transfer in horses can significantly impact their postnatal growth and glucose metabolism.
  • Enhanced growth (as in the P-D foals) seemed to induce a form of early insulin resistance, while restricted growth (S-P foals) led to increased insulin sensitivity.
  • The findings could have significant implications for understanding how intrauterine environments could influence the health and metabolic adaptations in newborn animals.

Cite This Article

APA
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. (2014). 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, 9(7), e102044. https://doi.org/10.1371/journal.pone.0102044

Publication

PloS one
ISSN: 1932-6203
NlmUniqueID: 101285081
Country: United States
Language: English
Volume: 9
Issue: 7
Pages: e102044

Researcher Affiliations

Peugnet, Pauline
  • INRA, UMR1198 Biologie du Développement et Reproduction, Jouy en Josas, France; ENVA, Maisons Alfort, France.
Wimel, Laurence
  • IFCE, Station Expérimentale de la Valade, Chamberet, France.
Duchamp, Guy
  • INRA, UE1293, Nouzilly, France.
Sandersen, Charlotte
  • Clinique équine, Faculté de Médecine Vétérinaire, CORD, Université de Liège, Liège, Belgique.
Camous, Sylvaine
  • INRA, UMR1198 Biologie du Développement et Reproduction, Jouy en Josas, France; ENVA, Maisons Alfort, France.
Guillaume, Daniel
  • INRA, UMR85, Physiologie de la Reproduction et Comportements, Nouzilly, France; CNRS, UMR7247, Nouzilly, France; Université François Rabelais de Tours, Tours, France; IFCE, Nouzilly, France.
Dahirel, Michèle
  • INRA, UMR1198 Biologie du Développement et Reproduction, Jouy en Josas, France; ENVA, Maisons Alfort, France.
Dubois, Cédric
  • IFCE, Station Expérimentale de la Valade, Chamberet, France.
Jouneau, Luc
  • INRA, UMR1198 Biologie du Développement et Reproduction, Jouy en Josas, France; ENVA, Maisons Alfort, France.
Reigner, Fabrice
  • INRA, UE1293, Nouzilly, France.
Berthelot, Valérie
  • INRA, UMR791 Modélisation Systémique Appliquée aux Ruminants, Paris, France; AgroParis Tech, Paris, France.
Chaffaux, Stéphane
  • INRA, UMR1198 Biologie du Développement et Reproduction, Jouy en Josas, France; ENVA, Maisons Alfort, France.
Tarrade, Anne
  • INRA, UMR1198 Biologie du Développement et Reproduction, Jouy en Josas, France; ENVA, Maisons Alfort, France.
Serteyn, Didier
  • Clinique équine, Faculté de Médecine Vétérinaire, CORD, Université de Liège, Liège, Belgique.
Chavatte-Palmer, Pascale
  • INRA, UMR1198 Biologie du Développement et Reproduction, Jouy en Josas, France; ENVA, Maisons Alfort, France.

MeSH Terms

  • Animals
  • Animals, Newborn / growth & development
  • Animals, Newborn / metabolism
  • Blood Glucose / metabolism
  • Breeding
  • Embryo Transfer / veterinary
  • Female
  • Fetal Development
  • Growth Hormone / metabolism
  • Horses / growth & development
  • Horses / metabolism
  • Insulin Resistance
  • Male
  • Pregnancy
  • Weaning
  • Weight Gain

Conflict of Interest Statement

Competing Interests: Co-author Pascale Chavatte-Palmer is a PLOS ONE Editorial Board member. This does not alter the authors\' adherence to all the PLOS ONE policies on sharing data and materials.

References

This article includes 83 references
  1. Barker DJ, Winter PD, Osmond C, Margetts B, Simmonds SJ. Weight in infancy and death from ischaemic heart disease.. The Lancet 1989 2: 577–580.
    pubmed: 2570282
  2. Barker DJ, Gluckman PD, Godfrey KM, Harding JE, Owens JA. Fetal nutrition and cardiovascular disease in adult life.. Lancet 1993 341: 938–941.
    pubmed: 8096277
  3. Barker DJ, Hales CN, Fall CH, Osmond C, Phipps K. Type 2 (non-insulin-dependent) diabetes mellitus, hypertension and hyperlipidaemia (syndrome X): relation to reduced fetal growth.. Diabetologia 1993 36: 62–67.
    pubmed: 8436255
  4. Ravelli ACJ, van der Meulen JHP, Michels RPJ, Osmond C, Barker DJP. Glucose tolerance in adults after prenatal exposure to famine.. The Lancet 1998 351: 173–177.
    pubmed: 9449872
  5. Ravelli AC, van Der Meulen JH, Osmond C, Barker DJ, Bleker OP. Obesity at the age of 50 y in men and women exposed to famine prenatally.. Am J Clin Nutr 1999 70: 811–816.
    pubmed: 10539740
  6. Roseboom TJ, van der Meulen JH, Ravelli AC, Osmond C, Barker DJ. Effects of prenatal exposure to the Dutch famine on adult disease in later life: an overview.. Mol Cell Endocrinol 2001 185: 93–98.
    pubmed: 11738798
  7. Stettler N, Zemel BS, Kumanyika S, Stallings VA. Infant Weight Gain and Childhood Overweight Status in a Multicenter, Cohort Study.. Pediatrics 2002 109: 194–199.
    pubmed: 11826195
  8. McMullen S, Mostyn A. Animal models for the study of the developmental origins of health and disease.. Proc Nutr Soc 2009 68: 306–320.
    pubmed: 19490740
  9. Poore KR, Fowden AL. The effect of birth weight on glucose tolerance in pigs at 3 and 12 months of age.. Diabetologia 2002 45.
    pubmed: 12242457
  10. Gatford KL, Mohammad SNB, Harland ML, De Blasio MJ, Fowden AL. Impaired beta-cell function and inadequate compensatory increases in beta-cell mass after intrauterine growth restriction in sheep.. Endocrinology 2008 149: 5118–5127.
    pubmed: 18535100
  11. Forhead AJ, Broughton Pipkin F, Fowden AL. Effect of cortisol on blood pressure and the renin-angiotensin system in fetal sheep during late gestation.. J Physiol 2000 526 Pt 1: 167–176.
    pmc: PMC2269992pubmed: 10878109
  12. Poore KR, Fowden A. The effect of birth weight on hypothalamo–pituitary–adrenal axis function in juvenile and adult pigs.. J Physiol 2003 547: 107–116.
    pmc: PMC2342625pubmed: 12562947
  13. Levin BE. Metabolic imprinting: critical impact of the perinatal environment on the regulation of energy homeostasis.. Phil Trans R Soc B 2006 361: 1107–1121.
    pmc: PMC1642705pubmed: 16815795
  14. Clifton VL. Review: Sex and the Human Placenta: Mediating Differential Strategies of Fetal Growth and Survival.. Placenta 2010 31: S33–S39.
    pubmed: 20004469
  15. Fowden A, Giusani DA, Forhead AJ. Intrauterine programming of physiological systems: causes and consequences.. Phyiology 2006 21: 29–37.
    pubmed: 16443820
  16. Symonds ME, Sebert SP, Budge H. Nutritional regulation of fetal growth and implications for productive life in ruminants.. Animal 2010 4: 1075–1083.
    pubmed: 22444610
  17. Wu G, Bazer FW, Wallace JM, Spencer TE. Intrauterine growth retardation: Implications for the animal sciences.. Journal of Animal Science 2006 84: 2316–2337.
    pubmed: 16908634
  18. Rossdale PD, Ousey JC. Fetal programming for athletic performance in the horse: potential effects of IUGR.. Equine Veterinary Education 2002 14: 98–111.
  19. Ansari T, Beech D, Sibbons PD, Rossdale PD, Ousey JC. Pilot investigations into microanatomical defects associated with IUGR in the horse and other domestic animals.. 1998 Sydney, Australia. The Dorothy Havermeyer Foundation. pp. 15.
  20. Van der Heyden L, Lejeune JP, Caudron I, Detilleux J, Sandersen C. Association of breeding conditions with prevalence of osteochondrosis in foals.. Vet Rec 2013 172: 68.
    pubmed: 23118049
  21. Geor R, Frank N. Metabolic syndrome-From human organ disease to laminar failure in equids.. Vet Immunol Immunopathol 2009 129: 151–154.
    pubmed: 19110319
  22. Johnson PJ. The equine metabolic syndrome peripheral Cushing's syndrome.. Vet Clin North Am Equine Pract 2002 18: 271–293.
    pubmed: 15635908
  23. Vick MM, Sessions DR, Murphy BA, Kennedy EL, Reedy SE. 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: 609–617.
    pubmed: 16930507
  24. Walton A, Hammond J. The maternal effects on growth and conformation in shire horse-shetland pony crosses.. Proc R Soc Lond B 1938 125: 311–335.
  25. Allen WR, Wilsher S, Turnbull C, Stewart F, Ousey J. Influence of maternal size on placental, fetal and postnatal growth in the horse. I. Development in utero.. Reproduction 2002 123: 445–453.
    pubmed: 11882022
  26. Giussani DA, Forhead AJ, Gardner DS, Fletcher AJW, Allen WR. Postnatal cardiovascular function after manipulation of fetal growth by embryo transfer in the horse.. J Physiol 2003 547: 67–76.
    pmc: PMC2342620pubmed: 12562940
  27. Forhead AJ, Ousey JC, Allen WR, Fowden AL. Postnatal insulin secretion and sensitivity after manipulation of fetal growth by embryo transfer in the horse.. Journal of Endocrinology 2004 181: 459–467.
    pubmed: 15171694
  28. Arnaud G. Notation de l'état corporel des chevaux de selle et de sport.. 2000 Paris, France: Institut de l'élevage, INRA, Institut Français du Cheval et de l'Equitation.
  29. Rijnen KE, van der Kolk JH. Determination of reference range values indicative of glucose metabolism and insulin resistance by use of glucose clamp techniques in horses and ponies.. Am J Vet Res 2003 64: 1260–1264.
    pubmed: 14596464
  30. Salazar-Ortiz J, Camous S, Briant C, Lardic L, Chesneau D. Effects of nutritional cues on the duration of the winter anovulatory phase and on associated hormone levels in adult female Welsh pony horses (Equus caballus).. Reproductive Biology and Endocrinology 2011 9.
    pmc: PMC3195710pubmed: 21958120
  31. Horhorn T, Hornik K, Van de Will MA, Zeileis A. A lego system for conditional inference.. The American Statistician 2006 60: 257–263.
  32. Noguchi K, Gel YR, Brunner E, Konietschke F. nparLD: An R software package for the non parametric analysis of longitudinal data in factorial experiments.. J Stat Software 2012 50: 1–23.
  33. Rossdale PD. A clinician's view of prematurity and dysmaturity in Thoroughbred foals.. Proc R Soc Med 1976 69: 631–632.
    pmc: PMC1864628pubmed: 981260
  34. Donjacour A, Liu X, Lin W, Simbulan R, Rinaudo P. In Vitro Fertilization Affects Growth and Glucose Metabolism in a Sex-Specific Manner in an Outbred Mouse Model.. Biol Reprod .
    pmc: PMC4076384pubmed: 24621920
  35. Watkins A, Lucas ES, Fleming T. Impact of the periconceptional environment on the programming of adult disease.. Journal of Developmental Origins of Health and Disease 2010 1: 1–9.
    pubmed: 25143062
  36. Market-Velker BA, Fernandes AD, Mann MR. Side-by-side comparison of five commercial media systems in a mouse model: suboptimal in vitro culture interferes with imprint maintenance.. Biol Reprod 2010 83: 938–950.
    pubmed: 20702853
  37. Watkins AJ, Platt D, Papenbrock T, Wilkins A, Eckert JJ. Mouse embryo culture induces changes in postnatal phenotype including raised systolic blood pressure.. Proc Natl Acad Sci U S A 2007 104: 5449–5454.
    pmc: PMC1838459pubmed: 17372207
  38. Hemkemeyer SA, Schwarzer C, Boiani M, Ehmcke J, Le Gac S. Effects of embryo culture media do not persist after implantation: a histological study in mice.. Hum Reprod 2014 29: 220–233.
    pubmed: 24324026
  39. Elliott C, Morton J, Chopin J. Factors affecting foal birth weight in Thoroughbred horses.. Theriogenology 2009 71: 683–689.
    pubmed: 18980778
  40. 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 2013 in press.
    pubmed: 24308928
  41. Jeffcott LB, Field JR, McLean JG, O'Dea K. Glucose tolerance and insulin sensitivity in ponies and Standardbred horses.. Equine Vet J 1986 18: 97–101.
    pubmed: 3516677
  42. Frank N, Geor RJ, Bailey SR, Durham AE, Johnson PJ. Equine metabolic syndrome.. J Vet Intern Med 2010 24: 467–475.
    pubmed: 20384947
  43. 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 81: 2333–2342.
    pubmed: 12968709
  44. 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: 81–84.
    pubmed: 12405664
  45. Romagnoli U, Macchi E, Romano G, Motta M, Accornero P. Leptin concentration in plasma and in milk during the interpartum period in the mare.. Animal Reproduction Science 2007 97: 180–185.
    pubmed: 16524675
  46. Heidler B, Aurich JE, Pohl W, Aurich C. Body weight of mares and foals, estrous cycles and plasma glucose concentration in lactating and non-lactating Lipizzaner mares.. Theriogenology 2004 61: 883–893.
    pubmed: 14757474
  47. Buff PR, Dodds AC, Morrison CD, Whitley NC, McFadin EL. Leptin in horses: Tissue localization and relationship between peripheral concentrations of leptin and body condition.. J Anim Sci 2002 80: 2942–2948.
    pubmed: 12462262
  48. Radin MJ, Sharkey LC, Holycross BJ. Adipokines: a review of biological and analytical principles and an update in dogs, cats, and horses.. Vet Clin Pathol 2009 38: 136–156.
    pubmed: 19392760
  49. Berg EL, McNamara DL, Keisler DH. Endocrine profiles of periparturient mares and their foals.. J Anim Sci 2007 85: 1660–1668.
    pubmed: 17431046
  50. Ben X, Qin Y, Wu S, Zhang W, Cai W. Placental leptin correlates with intrauterine fetal growth and development.. Chin Med J (Engl) 2001 114: 636–639.
    pubmed: 11780443
  51. Jakimiuk AJ, Skalba P, Huterski D, Tarkowski R, Haczynski J. Leptin messenger ribonucleic acid (mRNA) content in the human placenta at term: relationship to levels of leptin in cord blood and placental weight.. Gynecol Endocrinol 2003 17: 311–316.
    pubmed: 14503975
  52. Kawai M, Yamaguchi M, Murakami T, Shima K, Murata Y. The placenta is not the main source of leptin production in pregnant rat: gestational profile of leptin in plasma and adipose tissues.. Biochem Biophys Res Commun 1997 240: 798–802.
    pubmed: 9398648
  53. Thomas L, Wallace JM, Aitken RP, Mercer JG, Trayhurn P. Circulating leptin during ovine pregnancy in relation to maternal nutrition, body composition and pregnancy outcome.. J Endocrinol 2001 169.
    pubmed: 11375117
  54. Wang C, Medan MS, Shimizu K, Kojima C, Itoh M. Secretion of leptin throughout pregnancy and early postpartum period in Japanese monkeys: placenta as another potential source of leptin.. Endocrine 2005 27: 75–81.
    pubmed: 16077175
  55. Thomas CR, Oon BB, Lowy C. Placental transfer of lactate, glucose and 2-deoxyglucose in control and diabetic Wistar rats.. Int J Exp Diabetes Res 2001 2: 113–120.
    pmc: PMC2478544pubmed: 12369714
  56. Allen WR, Wilsher S, Tiplady C, Butterfield RM. The influence of maternal size on pre- and postnatal growth in the horse: III Postnatal growth.. Reproduction 2004 127: 67–77.
    pubmed: 15056771
  57. Berends LM, Fernandez-Twinn DS, Martin-Gronert MS, Cripps RL, Ozanne SE. Catch-up growth following intra-uterine growth-restriction programmes an insulin-resistant phenotype in adipose tissue.. Int J Obes (Lond) 2013 37: 1051–1057.
    pmc: PMC3734734pubmed: 23229735
  58. Pardo CE, Kreuzer M, Bee G. Effect of average litter weight in pigs on growth performance, carcass characteristics and meat quality of the offspring as depending on birth weight.. Animal 2013 7: 1884–1892.
    pubmed: 23896082
  59. Gonzalez-Bulnes A, Ovilo C, Lopez-Bote CJ, Astiz S, Ayuso M. Gender-specific early postnatal catch-up growth after intrauterine growth retardation by food restriction in swine with obesity/leptin resistance.. Reproduction 2012 144: 269–278.
    pubmed: 22692087
  60. De Blasio MJ, Gatford KL, Robinson JS, Owens JA. Placental restriction of fetal growth reduces size at birth and alters postnatal growth, feeding activity, and adiposity in the young lamb.. Am J Physiol Regul Integr Comp Physiol 2007 292: R875–886.
    pubmed: 17023666
  61. Doreau M, Boulot S. Recent knowledge on mare milk production: a review.. Livestock Production Science 1989 22: 213–235.
  62. Slebodzinski AB, Brzezinska-Slebodzinska E, Nowak J, Kowalska K. Triiodothyronine (T3), insulin and characteristics of 5′-monodeiodinase (5′-MD) in mare's milk from parturition to 21 days post-partum.. Reprod Nutr Dev 1998 38: 235–244.
    pubmed: 9698274
  63. Salimei E, Varisco G, Rosi F. Major constituents, leptin, and non-protein nitrogen compounds in mares' colostrum and milk.. Reprod Nutr Dev 2002 42: 65–72.
    pubmed: 12199377
  64. Hess-Dudan F, Vacher PY, Bruckmaier RM, Weishaupt MA, Burger D. Immunoreactive insulin-like growth factor I and insulin in blood plasma and milk of mares and in blood plasma of foals.. Equine vet J 1994 26: 134–139.
    pubmed: 8575376
  65. Fowden AL, Silver M, Ellis L, Ousey J, Rossdale PD. Studies on equine prematurity 3: Insulin secretion in the foal during the perinatal period.. Equine Vet J 1984 16: 286–291.
    pubmed: 6383810
  66. De Blasio MJ, Gatford KL, Harland ML, Robinson JS, Owens JA. Placental Restriction Reduces Insulin Sensitivity and Expression of Insulin Signaling and Glucose Transporter Genes in Skeletal Muscle, But Not Liver, in Young Sheep.. Endocrinology 2012 153: 2142–2151.
    pubmed: 22434080
  67. De Blasio MJ, Gatford KL, McMillen IC, Robinson JS, Owens JA. Placental restriction of fetal growth increases insulin action, growth, and adiposity in the young lamb.. Endocrinology 2007 148: 1350–1358.
    pubmed: 17110432
  68. Lim K, Armitage JA, Stefanidis A, Oldfield BJ, Black MJ. IUGR in the absence of postnatal “catch-up” growth leads to improved whole body insulin sensitivity in rat offspring.. Pediatr Res 2011 70: 339–344.
    pubmed: 21885936
  69. Owens JA, Thavaneswaran P, De Blasio MJ, McMillen IC, Robinson JS. Sex-specific effects of placental restriction on components of the metabolic syndrome in young adult sheep.. Am J Physiol Endocrinol Metab 2007 292: E1879–1889.
    pubmed: 17327366
  70. Firshman AM, Valberg SJ. Factors affecting clinical assessment of insulin sensitivity in horses.. Equine Vet J 2007 39: 567–575.
    pubmed: 18065318
  71. 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.. Domestic Animal Endocrinology 1996 13: 197–209.
    pubmed: 8738861
  72. Panzani S, Comin A, Galeati G, Romano G, Villani M. How type of parturition and health status influence hormonal and metabolic profiles in newborn foals.. Theriogenology 2012 77: 1167–1177.
    pubmed: 22153270
  73. Ohkawa N, Shoji H, Kitamura T, Suganuma H, Yoshikawa N. IGF-I, leptin and active ghrelin levels in very low birth weight infants during the first 8 weeks of life.. Acta Paediatr 2010 99: 37–41.
    pubmed: 19785636
  74. Ogilvy-Stuart AL. Neonatal thyroid disorders.. Arch Dis Child Fetal Neonatal Ed 2002 87: F165–171.
    pmc: PMC1721489pubmed: 12390984
  75. 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 74: 1936–1942.
    pubmed: 8856448
  76. Irvine CH, Evans MJ. Postnatal changes in total and free thyroxine and triiodothyronine in foal serum.. J Reprod Fertil Suppl 1975: 709–715.
    pubmed: 1060870
  77. Kim B. Thyroid hormone as a determinant of energy expenditure and the basal metabolic rate.. Thyroid 2008 18: 141–144.
    pubmed: 18279014
  78. Silver M, Fowden AL, Knox J, Ousey JC, Cash R. Relationship between circulating tri-iodothyronine and cortisol in the perinatal period in the foal.. J Reprod Fert Suppl 1991 44: 619–626.
    pubmed: 1665521
  79. Sainsbury A, Zhang L. Role of the hypothalamus in the neuroendocrine regulation of body weight and composition during energy deficit.. Obes Rev 2012 13: 234–257.
    pubmed: 22070225
  80. Klein I, Ojamaa K. Thyroid hormone and the cardiovascular system.. N Engl J Med 2001 344: 501–509.
    pubmed: 11172193
  81. Larsen PR, Davies TF, Hay ID. The Thyroid Gland.. Williams Textbook of Endocrinology 1998 Philadelphia: W.B. Saunders. pp. 389–515.
  82. Hanson M, Gluckman P. Developmental origins of noncommunicable disease: population and public health implications.. American Journal of Clinical Nutrition 2011 94: 1754S–1758S.
    pubmed: 21525196
  83. Frank N, Tadros EM. Insulin dysregulation.. Equine Vet J 2014 46: 103–112.
    pubmed: 24033478

Citations

This article has been cited 8 times.
  1. Robles M, Rousseau-Ralliard D, Dubois C, Josse T, Nouveau É, Dahirel M, Wimel L, Couturier-Tarrade A, Chavatte-Palmer P. Obesity during Pregnancy in the Horse: Effect on Term Placental Structure and Gene Expression, as Well as Colostrum and Milk Fatty Acid Concentration. Vet Sci 2023 Dec 4;10(12).
    doi: 10.3390/vetsci10120691pubmed: 38133242google scholar: lookup
  2. Meinecke B, Meinecke-Tillmann S. Lab partners: oocytes, embryos and company. A personal view on aspects of oocyte maturation and the development of monozygotic twins. Anim Reprod 2023;20(2):e20230049.
    doi: 10.1590/1984-3143-AR2023-0049pubmed: 37547564google scholar: lookup
  3. 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.
    doi: 10.3389/fvets.2023.1180622pubmed: 37152686google scholar: lookup
  4. Weatherall EL, Avilkina V, Cortes-Araya Y, Dan-Jumbo S, Stenhouse C, Donadeu FX, Esteves CL. Differentiation Potential of Mesenchymal Stem/Stromal Cells Is Altered by Intrauterine Growth Restriction. Front Vet Sci 2020;7:558905.
    doi: 10.3389/fvets.2020.558905pubmed: 33251256google scholar: lookup
  5. Yates DT, Petersen JL, Schmidt TB, Cadaret CN, Barnes TL, Posont RJ, Beede KA. ASAS-SSR Triennnial Reproduction Symposium: Looking Back and Moving Forward-How Reproductive Physiology has Evolved: Fetal origins of impaired muscle growth and metabolic dysfunction: Lessons from the heat-stressed pregnant ewe. J Anim Sci 2018 Jun 29;96(7):2987-3002.
    doi: 10.1093/jas/sky164pubmed: 29701769google scholar: lookup
  6. Robles M, Nouveau E, Gautier C, Mendoza L, Dubois C, Dahirel M, Lagofun B, Aubrière MC, Lejeune JP, Caudron I, Guenon I, Viguié C, Wimel L, Bouraima-Lelong H, Serteyn D, Couturier-Tarrade A, Chavatte-Palmer P. Maternal obesity increases insulin resistance, low-grade inflammation and osteochondrosis lesions in foals and yearlings until 18 months of age. PLoS One 2018;13(1):e0190309.
    doi: 10.1371/journal.pone.0190309pubmed: 29373573google scholar: lookup
  7. 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.
    doi: 10.1371/journal.pone.0169295pubmed: 28081146google scholar: lookup
  8. 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.
    doi: 10.1371/journal.pone.0122596pubmed: 25875166google scholar: lookup
Subscribe to our newsletter
Join 106,180 horse owners like you who receive our email updates on horse health and nutrition.