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

Volumn 9, Issue , 2011, Pages

  Salazar Ortiz, Juan ^a,b,c   Camous, Sylvaine ^d,e   Briant, Christine ^a,b,c   Lardic, Lionel ^a,b,c   Chesneau, Didier ^a,b,c   Guillaume, Daniel ^a,b,c  

^a UMR85 PHYSIOLOGIE DE LA REPRODUCTION ET DES COMPORTEMENTS   (France)

^b UNIVERSITÉ DE TOURS   (France)

^c IFCE   (France)

^d INRA Institut National de la Recherche Agronomique   (France)

^e ECOLE NATIONALE VÉTÉRINAIRE D ALFORT   (France)

Author keywords

[No Author keywords available]

Indexed keywords

GLUCOSE; GROWTH HORMONE; INSULIN; LEPTIN; MELATONIN; SOMATOMEDIN C;

ARTICLE; BLOOD SAMPLING; BODY CONSTITUTION; CONTROLLED STUDY; DIET RESTRICTION; FEMALE; METABOLIC BALANCE; NONHUMAN; OVARY FUNCTION; OVULATION INHIBITION; PASTURELAND; PHYSIOLOGICAL PROCESS; REPRODUCTION; SEASONAL VARIATION; ABDOMINAL SUBCUTANEOUS FAT; ANIMAL; ANIMAL DISEASE; ANOVULATION; BLOOD; BODY WEIGHT; CALORIC RESTRICTION; CIRCADIAN RHYTHM; CLINICAL TRIAL; COMPARATIVE STUDY; CONTROLLED CLINICAL TRIAL; FRANCE; GLUCOSE BLOOD LEVEL; HORSE; OBESITY; OVULATION; PATHOLOGY; PATHOPHYSIOLOGY; PHOTOPERIODICITY; PHYSIOLOGY; RADIATION EXPOSURE; RANDOMIZED CONTROLLED TRIAL; SEASON; TIME;

EQUIDAE; EQUUS CABALLUS;

ADIPOSITY; ANIMALS; ANOVULATION; BLOOD GLUCOSE; BODY WEIGHT; CALORIC RESTRICTION; CIRCADIAN RHYTHM; FEMALE; FRANCE; GROWTH HORMONE; HORSES; INSULIN; INSULIN-LIKE GROWTH FACTOR I; LEPTIN; MELATONIN; OVULATION; PHOTOPERIOD; SEASONS; SUBCUTANEOUS FAT, ABDOMINAL; TIME FACTORS;

EID: 80053173471     PISSN: None     EISSN: 14777827     Source Type: Journal    
DOI: 10.1186/1477-7827-9-130     Document Type: Article

References (95)

1. Langlois B, Blouin C. Effect of a horse's month of birth on its future sport performance. I Effect on annual phenotypic indices. Ann Zootech 1997, 46:393-398.
2. Langlois B, Blouin C. Effect of a horse's month of birth on its future sport performance. II Effect on annual earning and annual earning per start. Ann Zootech 1998, 47:67-74.
3. Langlois B, Blouin C. Statistical analysis of some factors affecting the number of horse birth in France. Reprod Nut Dév 2004, 44:583-596.
4. Van Niekerk CH, Van Heerden JS. Nutrition and ovarian activity of mares early in the breeding season. J South Afr Vet Med Ass 1972, 43:351-360.
5. Ginther OJ. Occurrence of anestrous, estrus, diestrus, and ovulation over a twelve-month period in mares. Am J Vet Res 1974, 35:1173-1179.
6. McDaniel JB, Kreider JL, Thrasher DM. The influence of artificial light and a nutritional supplement on the onset of the breeding season in mares [abstract]. J Anim Sci 1979, 49(Suppl 1):54-55.
7. Henneke DR, Potter GD, Kreider JL. Body condition during pregnancy and lactation and reproductive efficiency of mares. Theriogenology 1984, 21:897-909.
8. Kubiak JR, Crawford BH, Squires EL, Wrigley RH, Ward GM. The influence of energy intake and percentage body fat on the reproductive performance of nonpregnant mare. Theriogenology 1987, 28:587-598. 10.1016/0093-691X(87)90275-5, 16726341.
9. Koskinen E, Katila T. Onset of luteal activity in non-foaling mares during the early breeding season in Finland. Acta Vet Scand 1991, 32:319-325.
10. Gentry LR, Thompson DL, Gentry GT, 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, 80:2695-703. a.
11. Driancourt MA, Palmer E. Seasonal and individual effects on ovarian and endocrine responses of mares to a synchronization treatment with progestagen-impregnated vaginal sponges. J Reprod Fertil 1982, 32(Suppl):283-291.
12. Palmer E, Driancourt MA. Some Interactions of Season of Foaling, Photoperiod and Ovarian Activity in the Equine. Livest Prod Sci 1983, (10):197-210.
13. Koskinen E, Kurki E, Katila T. Onset of luteal activity in foaling and seasonally anoestrous mares treated with artificial light. Acta Vet Scand 1991, 32:307-312.
14. Fitzgerald BP, McManus CJ. Photoperiodic versus metabolic signals as determinants of seasonal anestrus in the mare. Biol Reprod 2000, 63:335-340. 10.1095/biolreprod63.1.335, 10859276.
15. Crowe MA. Resumption of ovarian cyclicity in post-partum beef and dairy cows. Reprod Domest Anim 2008, 43:Suppl 5:20-28.
16. Crowe MA, Goulding D, Baguisi A, Boland MP, Roche JF. Induced ovulation of the first postpartum dominant follicle in beef suckler cows using a GnRH analogue. J Reprod Fertil 1993, 99:551-555. 10.1530/jrf.0.0990551, 8107039.
17. Armstrong JD, Britt JH. Nutritionally-induced anestrus in gilts: metabolic and endocrine changes associated with cessation and resumption of estrous cycles. J Anim Sci 1987, 65:508-523.
18. Gentry LR, Thompson DL, Gentry GT, Davis KA, Godke RA. High versus low body condition in mares: interactions with responses to somatotropin, GnRH analog, and dexamethasone. J Anim Sci 2002, 80:3277-3285. b.
19. Schneider JE, Friedenson DG, Hall AJ, Wade GN. Glucoprivation induces anestrus and lipoprivation may induce hibernation in Syrian hamsters. Am J Physiol 1993, 264:R573-R577.
20. Goubillon ML, Thalabard JC. Insulin-induced hypoglycemia decreases luteinizing hormone secretion in the castrated male rat: involvement of opiate peptides. Neuroendocrinology 1996, 64:49-56. 10.1159/000127097, 8811666.
21. Cagampang FRA, Cates PS, Sandhu S, Strutton PH, McGarvey C, Coen CW, O'Byrne KT. Hypoglycaemia-induced inhibition of pulsatile luteinizing hormone secretion in female rats: role of oestradiol, endogenous opioids and the adrenal medulla. J Neuroendocrinol 1997, 9:867-872.
22. Downing JA, Scaramuzzi RJ. The effect of the infusion of insulin during the luteal phase of the estrous cycle on the ovulation rate and on plasma concentrations of LH, FSH and glucose in ewes. Theriogenology 1997, 47:747-759. 10.1016/S0093-691X(97)00031-9, 16728025.
23. Morton GJ, Cummings DE, Baskin DG, Barsh GS, Schwartz MW. Central nervous system control of food intake and body weight. Nature 2006, 443:289-295. 10.1038/nature05026, 16988703.
24. Buff PR, Dodds AC, Morrison CD, Whitley NC, McFadin EL, Daniel JA, Djiane J, Keisler DH. Leptin in horses: tissue localisation and relationship between peripheral concentrations of leptin and body condition. J Anim Sci 2002, 80:2943-2948.
25. Chen K, Li F, Li J, Cai H, Strom S, Bisello A, Kelley DE, Friedman-Einat M, Skibinski GA, McCrory MA, Szalai AJ. Zhao AZ: Induction of leptin resistance through direct interaction of C-reactive protein with leptin. Nat Med 2006, 12:425-432. 10.1038/nm1372, 16582918.
26. Adam CL, Finley PA, Miller DW. Blood-brain leptin transport and appetite and reproductive neuroendocrine responses to intracerebroventricular leptin injection in sheep: influence of photoperiod. Endocrinology 2006, 147:4589-4598. 10.1210/en.2006-0576, 16794008.
27. Henry BA, Goding JW, Tilbrooke AJ, Dunshea FR, Clarke IJ. Intracerebroventricular infusion of leptin elevates the secretion of luteinizing hormone without affecting food intake in long-term food restricted sheep, but increases growth hormone irrespective of body weight. J Endocrinol 2001, 168:67-77. 10.1677/joe.0.1680067, 11139771.
28. Polkowska J, Wojcik-Gladysz A, Wańkowska M. The effect of intracerebroventricular infusions of leptin on the immunoreactivity of neuropeptide Y and gonadotrophin releasing hormone neurons in the hypothalamus of prepubertal sheep in condition of fasting. J Chem Neuroanat 2006, 32:65-73. 10.1016/j.jchemneu.2006.05.001, 16765021.
29. Scacchi M, Pincelli AI, Cavagnini F. Nutritional status in the neuroendocrine control of growth hormone secretion: the model of anorexia nervosa. Front Neuroendocrin 2003, 24:200-224.
30. Hull KL, Harvey S. GH as a co-gonadotropin: the relevance of correlative changes in GH secretion to reproductive state. J Endocrinol 2002, (172):1-19.
31. Cingel-Ristic V, Van Neck JW, Frystyk J, Drop SL, Flyvbjerg. A administration of human insulin-like growth factor-binding protein-1 increases circulating levels of growth hormone in mice. Endocrinology 2004, 145:4401-4407. 10.1210/en.2003-1742, 15166120.
32. Popot MA, Bobin S, Bonnaire Y, Delahaut PH, Closset J. IGF-I plasma concentrations in non-treated horses and horses administered with methionyl equine somatotrophin. Res Vet Sci 2001, 71:167-173. 10.1053/rvsc.2001.0505, 11798290.
33. Ortavant R, Bocquier F, Pelletier J, Ravault JP, Thimonier J, Volland-Nail P. Seasonality of reproduction in sheep and its control by photoperiod. Aust J Biol Sci 1988, 41:69-85.
34. Chemineau P, Pelletier J, Guerin Y, Colas G, Ravault JP, Toure G, Almeida G, Thimonier J, Ortavant R. Photoperiodic and melatonin treatments for the control of seasonal reproduction in sheep and goats. Reprod Nut Dév 1988, 28:409-422.
35. Lincoln GA, Short RV. Seasonal breeding: nature's contraceptive. Rec Prog Horm Res 1980, 36:1-52.
36. Freedman LJ, Garcia MC, Ginther OJ. Influence of photoperiod and ovaries on seasonal reproductive activity in mares. Biol Reprod 1979, 20:567-574. 10.1095/biolreprod20.3.567, 572238.
37. Palmer E. Reproductive management of mares without detection of oestrus. J Reprod Fertil 1979, 27(Suppl):263-270.
38. Miller KF, Berg SL, Sharp DC, Ginther OJ. Concentrations of Circulating Gonadotropins During Various Reproductive States in Mares. Biol Reprod 1980, 22:744-750. 10.1095/biolreprod22.4.744, 6772244.
39. Kooistra LH, Ginther OJ. Effect of photoperiod on reproductive activity and hair in mares. Am J Vet Res 1975, 36:1413-1419.
40. Guillaume D, Palmer E. Effect of oral melatonin on the date of the first ovulation after ovarian inactivity in mares under artificial photoperiod. J Reprod Fertil 1991, 44(Suppl):249-257.
41. Guillaume D, Arnaud G, Camillo F, Duchamp G, Palmer E. Effect of melatonin implants on reproductive status of mares. 'Equine Reproduction VI'. Biol Reprod 1995, 1:435-442. Monograph Series.
42. McManus CJ, Fitzgerald BP. Effect of daily clenbuterol and exogenous melatonin treatment on body fat, serum leptin and the expression of seasonal anoestrus in the mare. Anim Reprod Sci 2003, 76:217-230. 10.1016/S0378-4320(02)00246-4, 12586494.
43. Peltier MR, Robinson G, Sharp DC. Effects of melatonin implants in pony mares. 2. Long-term effects. Theriogenology 1998, 49:1125-1142. 10.1016/S0093-691X(98)00061-2, 10732051.
44. Sharp DC, Vernon MW, Zavy MT. Alteration of seasonal reproductive patterns in mares following superior cervical ganglionectomy. J Reprod Fertil 1979, 27(Suppl):1-7.
45. Grubaugh WR, Sharp DC, Berglund LA, McDowell KJ, Kilmer DM, Peck LS, Seamans KW. Effects of pinealectomy in pony mares. J Reprod Fertil 1982, 32(Suppl):293-295.
46. Palmer E, Driancourt MA, Ortavant R. Photoperiodic stimulation of the mare during winter anoestrus. J Reprod Fertil 1982, 32:275-282.
47. Scraba ST, Ginther OJ. Effects of lighting programs on onset of the ovulatory season in mares. Theriogenology 1985, 24:667-679.
48. Guillaume D, Duchamp G, Nagy P, Palmer E. Determination of minimum light treatment required for photostimulation of winter anoestrus mares. J Reprod Fertil 2000, 56(suppl 1):205-216.
49. Karsch FJ, Robinson JE, Woodfill CJI, Brown MB. Circannual cycles of luteinizing hormone and prolactin secretion in ewes during prolonged exposure to a fixed photoperiod: Evidence for an endogenous reproductive rhythm. Biol Reprod 1989, 41:1034-1046. 10.1095/biolreprod41.6.1034, 2624864.
50. H N, I E. INRA Notation de l'état corporel des chevaux de selle et de sport. Guide pratique 1997, Eds Institut Elevage Publishing 149 rue de Bercy 75595 Paris, France, INRA.
51. Henneke DR, Potter GD, Krieder JL, Yeates BF. Relationship between body condition score, physical measurements and body fat percentage in mares. Equine Vet J 1983, 15:371-372. 10.1111/j.2042-3306.1983.tb01826.x, 6641685.
52. Vermorel M, Garrige R, Martin-Rosset W. Métabolisme et besoin énergétiques du cheval, le système des UFC. INRA. 13eme Journée du Grenier de Theix 1981, 239-276. Eds INRA Publishing Versailles, France, Clermont-ferrand.
53. Martin-Rosset W, Vermorel M, Doreau M, Tisserand V, Andrieu J. The French horse feed evaluation systems and recommended allowances for energy and protein. Livest Prod Sci 1994, 40:37-56.
54. Vermorel M, Vernet J, Martin-Rosset W. Digestive and energy utilisation of two diets by ponies and horses. Livest Prod Sci 1997, 51:13-19.
55. Terqui M, Thimonier J. New rapid radioimmunologic method for estimation of plasma progesterone. Application to early diagnosis of gestation in the ewe and goat. C R Acad Sci 1974, 279:1109-1112.
56. Tillet Y, Ravault JP, Selve C, Evin G, Castro B, Dubois MP. Condition d'utilisation d'anticorps spécifiques pour la visualisation immunohistochimique de la sérotonine et de la mélatonine dans la glande pinéale du mouton. C R Acad Sci 1986, 303:77-82.
57. Kadish AH, Little RL, Sternberg JC. A New and rapid method for the determination of glucose by measurement of oxygen consumption rate. Clin Chem 1968, 14:144-116.
58. Guillaume D, Chavatte-Palmer P, Combarnous Y, Duchamp G, Martinat M, Nagy P, Daels PF. Induced lactation with a dopamine antagonist in mares: different responses between ovariectomised and intact mares. Reprod Domest Anim 2003, 38:394-400. 10.1046/j.1439-0531.2003.00454.x, 12950692.
59. Delavaud C, Bocquier F, Chilliard Y, Keisler DH, Gertler A, Kann G. Plasma leptin determination in ruminants: effect of nutritional status and body fatness on plasma leptin concentration assessed by a specific RIA in sheep. J Endocrinol 2000, 165:519-526. 10.1677/joe.0.1650519, 10810316.
60. Agresti A. Categorical data analysis 1990, John Willey and Sons Press New-York.
61. Freeman GH, Halton JH. Note on an exact treatment of contingency, goodness of fit and other problems of significance. Biometrika 1951, 38:141-149.
62. Gibbons JD. Nonparametric statistical inference. 1985, Dekker Press New-York, 2.
63. Little RC, Henry PR, Ammerman CB. Statistical analysis of repeated measures data using SAS procedures. J Anim Sci 1998, 76:1216-1231.
64. Bossis I, Wettemann RP, Welty SD, Vizcarra J, Spicer LJ. Nutritionally induced anovulation in beef heifers: ovarian and endocrine function during realimentation and resumption of ovulation. Biol Reprod 2000, 62:1436-1444. 10.1095/biolreprod62.5.1436, 10775198.
65. Tanaka T, Yamaguchi T, Kamomae H, Kaneda Y. Nutritionally induced body weight loss and ovarian quiescence in Shiba goats. J Reprod Dev 2003, 49:113-119. 10.1262/jrd.49.113, 14967956.
66. Zarazaga LA, Guzman JL, Dominguez C, Perez MC, Prieto R. Effect of plan of nutrition on seasonality of reproduction in Spanish Payoya goats. Anim Reprod Sci 2005, 87:253-267. 10.1016/j.anireprosci.2004.11.004, 15911175.
67. Miller KK, Grinspoon S, Gleysteen S, Grieco KA, Ciampa J, Breu J, Herzog DB, Klibanski A. Preservation of neuroendocrine control of reproductive function despite severe undernutrition. J Clin Endocrinol Metab 2004, 89:4434-4438. 10.1210/jc.2004-0720, 15356043.
68. Miller DW, Harrison JL, Bennett EJ, Findlay PA, Adam CL. Nutritional influences on reproductive neuroendocrine output: insulin, leptin, and orexigenic neuropeptide signaling in the ovine hypothalamus. Endocrinology 2007, 148:5313-22. 10.1210/en.2007-0534, 17702844.
69. Allen WR. Endogenous hormonal control of the mare's oestrus cycle. Proceedings of the Bain-Fallon Memorial 1987, Lectures 2-13.
70. Carnevale EM, Ginther OJ. Age and pasture effects on vernal transition in mares. Theriogenology 1997, 47:1009-1018. 10.1016/S0093-691X(97)00058-7, 16728051.
71. Van Niekerk FE, Van Niekerk CH. The effect of dietary protein on reproduction in the mare. III. ovarian and uterine changes during the anovulatory, transitional and ovulatory periods in the non-pregnant mare. J South Afr Vet Med Ass 1997, 68:86-92.
72. Rhind SM, McNeilly AS. Effects of level of food intake on ovarian follicle number, size and steroidogenic capacity in the ewe. Anim Reprod Sci 1998, 52:131-138. 10.1016/S0378-4320(98)00097-9, 9776486.
73. Nagy P, Huszenicza G, Juhasz J, Solti L, Kulcsar M. Diagnostic problems associated with ovarian activity in barren and postpartum mares early in the breeding season. Reproduction in Domestic Animals 1998, 33:187-192.
74. Martin GB, Hötzel MJ, Blache D, Walkden-Brown SW, Blackberry MA, Boukhliq RC, Fisher JS, Miller DW. Determinants of the annual pattern of reproduction in mature male Merino and Suffolk sheep: modification of responses to photoperiod by an annual cycle in food supply. Reprod Fertil Dev 2002, 14:165-75. 10.1071/RD02010, 12219938.
75. Gu J, Orr N, Park SD, Katz LM, Sulimova G, MacHugh DE, Hill EW. A Genome Scan for Positive Selection in Thoroughbred Horses. PLoS ONE 2009, (4 e5767):1-17.
76. Jousse C, Parry L, Lambert-Langlais S, Maurin AC, Averous J, Bruhat A, Carraro V, Tost J, Letteron P, Chen P, Jockers R, Launay JM, Mallet J, Fafournoux P. Perinatal undernutrition affects the methylation and expression of the leptin gene in adults: implication for the understanding of metabolic syndrome. The FASEB Journal 2011, 25:3271-3278. 10.1096/fj.11-181792, 21670064.
77. Sharp DC, Grubaugh W, Zavy MT, Vernon MW. Seasonal variation in melatonin secretory patterns in mares [abstract]. J Anim Sci 1980, 51(Suppl 1):327-328.
78. Guerin MV, Deed JR, Kennaway DJ, Matthews CD. Plasma melatonin in the horse: measurements in natural photoperiod and in acutely extended darkness throughout the year. J Pineal Res 1995, 19:7-15. 10.1111/j.1600-079X.1995.tb00165.x, 8609596.
79. Guillaume D, Rio N, Toutain PL. Kinetic studies and production rate of melatonin in pony mares. Am J Physiol 1995, 268:R1236-R1241.
80. Fitzgerald BP, Schmidt MJ. Absence of an association between melatonin and reproductive activity in mares during the nonbreeding season. Biol Reprod Monograph 1995, 1:425-434.
81. Diekman MA, Braun W, Peter D, Cook D. Seasonal serum concentrations of melatonin in cycling and noncycling mares. J Animl Sci 2002, 80:2949-2952.
82. Sticker LS, Thompson DL, Bunting LD, Fernandez JM, DePew CL. Dietary protein and or energy restriction in mares: plasma glucose, insulin, nonesterified fatty acid, and urea nitrogen responses to feeding, glucose and epinephrine. J Animl Sci 1995, 73:136-144.
83. Short RE, Adams C. Nutritional and Hormonal Interrelationships in Beef Cattle Reproduction. Can J Anim Sci 1988, 68:29-39.
84. Daniel JA, Thomas MG, Hale CS, JM Simmons JM, Keisler DH. Effect of cerebroventricular infusion of insulin and or glucose on hypothalamic expression of leptin receptor and pituitary secretion of LH in diet-restricted ewes. Domest Anim Endocrin 2000, 18:177-185.
85. Wettemann RP, Lents CA, Ciccioli NH, White FJ, Rubio I. Nutritional and suckling-mediated anovulation in beef cows. J Anim Sci 2003, 81:E48-E59.
86. Randel RD. Nutrition and postpartum rebreeding in cattle. J Anim Sci 1990, 68:853-862.
87. Dhuyvetter DV, Caton JS. Manipulation of reproduction and lactation with supplementation in beef cattle. Am Soc Anim Sci 1996, 47(Suppl 1):83-93. Proc 3rd Grazing Livest. Nutr. Conf., MB Judkins, McCollum FT, III, ed. Proc West Sec.
88. Archer ZA, Rhind SM, Findlay PA, Kyle CE, Barber MC, Adam CL. Hypothalamic responses to peripheral glucose infusion in food-restricted sheep are influenced by photoperiod. J Endocrinol 2005, 184:515-525. 10.1677/joe.1.06013, 15749810.
89. Unger JW, Moss AM, Livingston JN. Immunohistochemical localization of insulin receptors and phosphotyrosine in the brainstem of the adult rat. Neuroscience 1991, 42:853-861. 10.1016/0306-4522(91)90049-T, 1720228.
90. Miller DW, Blache D, Martin GB. The role of intracerebral insulin in the effect of nutrition on gonadotrophin secretion in mature male sheep. J Endocrinol 1995, 147:321-329. 10.1677/joe.0.1470321, 7490562.
91. McManus CJ, Davison LA, Fitzgerald BP. Effect of 2-deoxy-D-glucose on gonadotropins, prolactin and serum glucose concentrations in the mare. Anim Reprod Sci 2002, 71:217-228. 10.1016/S0378-4320(02)00030-1, 12047930.
92. Deichsel K, Hoppen HO, Bruckmaier RM, Kolm G, Aurich C. Acute-insulin-induced hypoglycaemia does not alter IGF-I and LH release in cyclic mares. Reprod Domest Anim 2005, 40:117-122. 10.1111/j.1439-0531.2005.00564.x, 15819959.
93. Butler ST, Marr AL, Pelton SH, Radcliff RP, Lucy MC, Butler WR. Insulin restores GH responsiveness during lactation-induced negative energy balance in dairy cattle: effects on expression of IGF-I and GH receptor 1A. J Endocrinol 2003, 176:205-217. 10.1677/joe.0.1760205, 12553869.
94. Breier BH. Regulation of protein and energy metabolism by the somatotropic axis. Domest Anim Endocrin 1999, 17:209-218.
95. Piccione G, Bertolucci C, Foà A, Caola G. Influence of fasting and exercise on the daily rhythm of serum leptin in the horse. Chronobiol Int 2004, 21:405-417. 10.1081/CBI-120038609, 15332446.