Overview on Reproductive Endocrine Aspects in Buffalo

Giuseppina Maria Terzano; Vittoria Lucia Barile; Antonio Borghese

doi:10.6000/1927-520X.2012.01.02.01

Authors

Giuseppina Maria Terzano Agricultural Research Council-Animal Production Research Centre (CRA-PCM) Monterotondo, Rome, Italy
Vittoria Lucia Barile Agricultural Research Council-Animal Production Research Centre (CRA-PCM) Monterotondo, Rome, Italy
Antonio Borghese General Secretary International Buffalo Federation (IBF); Coordinator FAO-ESCORENA Buffalo Network Monterotondo, Rome, Italy

DOI:

https://doi.org/10.6000/1927-520X.2012.01.02.01

Keywords:

Melatonin, Pituitary gonadotrophin, Gonadal steroid hormone, Inhibin, PAG, Leptin

Abstract

Buffalo is an important worldwide species in terms of milk and meat production as well as draft. The major constraints to full exploitation of the productive potential of buffalo are its inherent low reproductive efficiency due to delayed puberty, higher age at first calving, long post partum anoestrus period, long intercalving period, silent heat coupled with poor expression of oestrus, seasonality in breeding and low conception rate. Reproductive cycles in buffalo are regulated by endocrine-neuroendocrine interactions between hypothalamic, gonadotropic, gonadal and other hormones. To improve the buffalo reproductive efficiency, the investigation on endocrine aspects is useful to gain a better knowledge of buffalo reproduction. This review is focused on the information available on various basic hormones (Melatonin, Progesterone (P4), Estradiol 17B (E2), Follicle stimulating hormone (FSH), Luteinizing hormone (LH)) and on new hormones (Inhibin, Glycoproteins associated with pregnancy (PAGs), Leptin) related to reproductive function.

References

Seren E, Parmeggiani A, Mongiorgi S, et al. Modificazioni endocrine durante il ciclo estrale nella bufala. Agric Ricerca 1994; 16: 17-24.

Jainudeen MR, Hafez ESE. Cattle and Buffalo. In: Reproduction in Farm Animals, Hafez B, Hafez ESE, Eds. 7th ed. Lippincott Williams and Wilkins, Maryland, USA 2000; pp. 167-70. DOI: https://doi.org/10.1002/9781119265306.ch11

Perera BMAO. Reproductive cycles of buffalo. Anim Reprod Sci 2008; 124(3-4): 194-99. http://dx.doi.org/10.1016/j.anireprosci.2010.08.022 DOI: https://doi.org/10.1016/j.anireprosci.2010.08.022

Chemineau P, Malpaux B, Delgadillo JA, et al. Control of sheep and goat reproduction: use of light and melatonin. Anim Reprod Sci 1992; 30: 157-84. http://dx.doi.org/10.1016/0378-4320(92)90010-B DOI: https://doi.org/10.1016/0378-4320(92)90010-B

Malpaux B, Viguié C, Skinner DC, Thiéry JC, Pelletier J, Chemineau P. Seasonal breeding in sheep: mechanism of action of melatonin. Anim Reprod Sci 1996; 42: 109. http://dx.doi.org/10.1016/0378-4320(96)01505-9 DOI: https://doi.org/10.1016/0378-4320(96)01505-9

Rosa HJD, Bryant MJ. Seasonality of reproduction in sheep. Small Ruminant Res 2003; 48: 155-71. http://dx.doi.org/10.1016/S0921-4488(03)00038-5 DOI: https://doi.org/10.1016/S0921-4488(03)00038-5

Barile VL. Reproductive efficiency in female buffaloes. In Borghese A. editor. Buffalo Production and Research, REU Technical Series FAO Rome 2005; 67: 77-107.

Parmeggiani A, Seren E, Esposito L, Borghese A, Di Palo R, Terzano GM. Plasma levels of melatonin in buffalo cows. Proc. Intern. Symp Prospect of Buffalo Production in the Med/Middle East, Cairo, Egypt 1993; vol. 62: pp. 401-3.

Borghese A, Barile VL, Terzano GM, Pilla AM, Parmeggiani A. Melatonin trend during season in heifers and buffalo cows. Bubalus Bubalis 1995; 1: 61-5.

Di Palo R, Parmeggiani A, Spadetta M, et al. Influence of changing farm on repeatability of melatonin plasma level in Italian Mediterranean buffalo. Proc. Fifth World Buffalo Congress, Caserta, Italy 1997; pp. 758-61.

Zicarelli L. Reproductive seasonality in buffalo. Proc. of the Third Course on Biotechnology of Reproduction in Buffaloes, Caserta, Italy 1997; Issue II: pp. 29-52.

Parmeggiani A, Di Palo R, Zicarelli L, et al. Melatonina e stagionalità riproduttiva della bufala. Agric Ricerca 1994; 16: 41-8.

Seren E, Parmeggiani A, Campanile G. The control of ovulation in Italian buffalo. Reproduction and Animal Breeding advances and strategy, Eds. Enne G, Greppi GF. And Lauria A, Elsevier Amsterdam 1995; pp. 265-75.

Afify AA, Kassim Nany SI, Hassan Hoda Z, Zeidan Soheir M. Relationship between photoperiod and melatonin level at growth stages of buffalo heifers. SPSA 2008; 2(7). Available from http://www.spsa-egy.org/?p=873.

Shah RG, Mehta VM. Correlated behaviour of blood and corpus luteum progesterone levels with luteal cell types in Surti buffaloes. Buff J 1992; 8(2): 167-73.

Kamboj M, Prakash BS. Relationship of progesterone in plasma and whole milk of buffaloes during cyclicity and early pregnancy. Trop Anim Helth Prod 1993; 25: 185-92. http://dx.doi.org/10.1007/BF02236239 DOI: https://doi.org/10.1007/BF02236239

Mondal S, Palta P, Prakash BS. Influence of season on peripheral plasma progesterone in cycling Murrah buffaloes. Proc 29th British Congress of Obstetrics and Gynaecology, Birmingham, UK 2001; p. 177.

Mondal S, Prakash BS. Peripheral plasma progesterone concentrations in relation to oestrus expression in Sahiwal cows and Murrah buffaloes. Reprod 2002; 28: 29-30.

Mondal S, Prakash BS. Peripheral plasma progesterone concentrations in relation to oestrus expression in Murrah buffalo (Bubalus bubalis). Ind J Anim Sci 2002; 73: 292-93.

Mondal S, Prakash BS, Palta P. Relationship between peripheral plasma inhibin and progesterone concentrations in Sahiwal cattle (Bos indicus) and Murrah buffaloes (Bubalus bubalis). Asian-Aust J Anim Sci 2003; 16(1): 6-10. DOI: https://doi.org/10.5713/ajas.2003.6

Ahmed A, Agarwal SP, Agarwal VK, Rehman SA, Laumas KR. Steroid hormones. Part II. Serum progesterone concentrations in buffaloes. Ind J Exptl Biol 1977; 15: 591-93.

Bachalaus NK, Arora RC, Prasad AR, Pandey S. Plasma levels of gonadal hormones in cycling buffalo heifers. Ind J Exptl Biol 1979; 17: 823-25.

Pahwa GS, Pandey RS. Gonadal steroid hormone concentration in blood plasma and milk of primiparous and multiparous pregnant and non pregnant buffaloes. Theriogenology 1983; 19: 491-505. http://dx.doi.org/10.1016/0093-691X(83)90170-X DOI: https://doi.org/10.1016/0093-691X(83)90170-X

Batra SK, Arora RC, Bachalaus NK, Pandey RS. Blood and milk progesterone in pregnant and non pregnant buffalo. J Dairy Sci 1979; 62: 1390-93. http://dx.doi.org/10.3168/jds.S0022-0302(79)83434-7 DOI: https://doi.org/10.3168/jds.S0022-0302(79)83434-7

Srivastava SK, Sahni KL, Shaker U, Sanwal PC, Varshney VP. Seasonal variation in P4 concentration during the oestrus cycle in Murrah buffaloes. lndian J Anim Sci 1999; 69 (9): 700-1.

Mondal S, Palta P, Prakash BS. Influence of season on peripheral plasma progesterone in cycling Murrah buffaloes (Bubalus bubalis). Buff J 2004; 1: 95-100.

Gwazdauskas FC, Thatchar WW, Wilcox CJ. Adrenocortocotropin alteration of bovine peripheral plasma concentrations of cortisol, corticosterone and progesterone. J Dairy Sci 1972; 55: 1165-69. http://dx.doi.org/10.3168/jds.S0022-0302(72)85640-6 DOI: https://doi.org/10.3168/jds.S0022-0302(72)85640-6

Wagner WC, Strohbehn RE, Harris PA. ACTH, corticoids and luteal function in heifers. J Anim Sci 1972; 35: 789-93. DOI: https://doi.org/10.2527/jas1972.354789x

Abilay TA, Johnson HD, Madan ML. Influence of environmental heat on peripheral plasma progesterone and cortisol during bovine oestrous cycle. J Dairy Sci 1975; 58: 1836-40. http://dx.doi.org/10.3168/jds.S0022-0302(75)84795-3 DOI: https://doi.org/10.3168/jds.S0022-0302(75)84795-3

Ronchi B, Stradaioli G, Verini Supplizi A, Bernabucci U, Lacetera N, Accorsi P. Influence of heat stress or feed restriction on plasma P4, oestradiol 17, LH, FSH, prolactin and cortisol in Holstein heifers. Livest Prod Sci 2001; 68: 231-41. http://dx.doi.org/10.1016/S0301-6226(00)00232-3 DOI: https://doi.org/10.1016/S0301-6226(00)00232-3

Prakash BS, Palta P, Bansal N, Manik RS, Madan ML. Development of a sensitive direct enzymeimmunoassay for progesterone determination in follicular fluid from individual buffalo follicles. Ind J Anim Sci 1997; 67: 36-8.

Palta P, Bansal N, Prakash BS, Manik RS, Madan ML. Endocrinological observation of atresia in individual buffalo ovarian follicles. Ind J Anim Sci 1998; 68: 444-7.

Palta P, Bansal N, Prakash BS, Manik RS, Madan L. Interrelationship between follicular size and follicular fluid estradiol-17, progesterone and testosterone concentrations in individual buffalo ovarian follicles. Asian-Aust J Anim Sci 1998; 11: 293-9. DOI: https://doi.org/10.5713/ajas.1998.293

Mondal S, Prakash BS, Palta P. Endocrine aspects of oestrous cycle in buffaloes (Bubalus bubalis): an overview. Asian-Aust J Anim Sci 2007; 20(1): 124-31. DOI: https://doi.org/10.5713/ajas.2007.124

Hattab SA, Kadoom AK, Palmo R, Bamberg E. Effects of Crestar and the relationship between faecal and plasma concentrations of progestagens in buffalo cows. Theriogenology 2000; 54: 1007-17. http://dx.doi.org/10.1016/S0093-691X(00)00409-X DOI: https://doi.org/10.1016/S0093-691X(00)00409-X

Terzano GM, Barile VL, Mongiorgi S, e Borghese A. Effetto di differenti livelli alimentari sulla pubertà in bufale di razza mediterranea. Atti S.I.Vet. Riccione, Italy 1993; p. 47.

Terzano GM, Galasso A, Barile VL, Pacelli C, Montemurro N, Borghese A. Effect of feeling system and pubertà on blood metabolites trends in buffalo heifers. Proc. Fifth World Buffalo Congress: Caserta, Italy 1997; pp. 951-56.

Borghese A. Pubertà e mantenimento dell’attività ciclica ovarica nella bufala. Agricoltura e Ricerca 1994; 5-15.

Singh B, Dixit VD, Singh P, Georgie GC, Dixit VP. Plasma inhibin levels in relation to steroids and gonadotrophins during the oestrus cycle in buffalo. Reprod Dom Anim 2001; 36(3-4): 163-7. http://dx.doi.org/10.1046/j.1439-0531.2001.00280.x DOI: https://doi.org/10.1046/j.1439-0531.2001.00280.x

Malfatti A. Recent advances in buffalo endocrinology. Atti Secondo Congresso Nazionale sull'Allevamento del Bufalo, Monterotondo, Roma 2003; pp. 161-76.

Baruselli PS, Mucciolo RG, Visintin JA, et al. Ovarian follicular dynamics during the oestrus cycle in buffalo (Bubalus bubalis). Theriogenology 1997; 47: 1531-47. DOI: https://doi.org/10.1016/S0093-691X(97)00159-3

Manik RS, Singla SK, Palta P, Madan ML. Ovarian follicular dynamics monitored by real-time ultrasonography during oestrous cycle in buffalo (Bubalus bubalis). Asian-Aust J Anim Sci 1998; 11: 480-5. DOI: https://doi.org/10.5713/ajas.1998.480

Batra SK, Pandey RS. Luteinizing hormone and oestradiol-17 in blood plasma and milk during oestrous cycle and early pregnancy in Murrah buffaloes. Anim Reprod Sci 1982/83; 5: 247-57. http://dx.doi.org/10.1016/0378-4320(83)90046-5 DOI: https://doi.org/10.1016/0378-4320(83)90046-5

Batra SK, Arora RC, Bachalaus NK, Pahwa GS, Pandey RS. Quantitative relationships between oestradiol-17 in the milk and blood of lactating buffaloes. J Endocrinol 1980; 84: 205-9. http://dx.doi.org/10.1677/joe.0.0840205 DOI: https://doi.org/10.1677/joe.0.0840205

Palta P, Jailkhani S, Prakash BS, Manik RS, Madan ML. Development of direct radioimmunoassay for oestradiol-17 determination in follicular fluid from individual buffalo ovarian follicles. Ind J Anim Sci 1996; 66: 126-30.

Parmar AP, Mehta VM. Seasonal endocrine changes in steroid hormones of developing ovarian follicles in Surti buffaloes. Ind J Anim Sci 1994; 64: 111-3.

Rao LV, Pandey RS. Seasonal variations in oestradiol-17 and luteinizing hormone in the blood of buffalo cows (Bubalus bubalis). J Endocrinol 1983; 98: 251-5. http://dx.doi.org/10.1677/joe.0.0980251 DOI: https://doi.org/10.1677/joe.0.0980251

Rao LV, Pandey RS. Seasonal changes in the plasma progesterone concentration in buffalo cow (Bubalus bubalis). J Reprod Fertil 1982; 66: 57-61. http://dx.doi.org/10.1530/jrf.0.0660057 DOI: https://doi.org/10.1530/jrf.0.0660057

Kaker ML, Razdan MN, Galhotra MM. Serum LH concentrations in cyclic buffaloes (Bubalus bubalis). J Reprod Fertil 1980; 60: 419-24. http://dx.doi.org/10.1530/jrf.0.0600419 DOI: https://doi.org/10.1530/jrf.0.0600419

Palta P, Madan ML. Alterations in hypophysial responsiveness to synthetic GnRH at different postpartum intervals in Murrah buffalo (Bubalus bubalis). Theriogenology 1995; 44: 403-11. http://dx.doi.org/10.1016/0093-691X(95)00194-D DOI: https://doi.org/10.1016/0093-691X(95)00194-D

Palta P, Madan ML. Effects of gestation on GnRH-induced LH and FSH release in buffalo (Bubalus bubalis). Theriogenology1997; 46: 993-8. http://dx.doi.org/10.1016/S0093-691X(96)00263-4 DOI: https://doi.org/10.1016/S0093-691X(96)00263-4

Presicce GA, Parmeggiani AM, Senatore EM, et al. Hormonal dynamics and follicular turnover in prepuberal Mediterranean Italian buffaloes. Theriogenology 2003; 1-9. DOI: https://doi.org/10.1016/S0093-691X(03)00034-7

Janakiraman K, Desai MC, Amin DR, Sheth AR, Moodbidri SB, Wadadekar KB. Serum gonadotropin levels in buffaloes in relation to phases of oestrous cycle and breeding periods. Ind J Anim Sci 1980; 50: 601-606.

Razdan MN, Kaker ML, Galhotra MM. Serum FSH levels during oestrus and a 4-week period following mating in Murrah buffaloes (Bubalus bubalis). Theriogenology 1982; 17: 175-81. http://dx.doi.org/10.1016/0093-691X(82)90077-2 DOI: https://doi.org/10.1016/0093-691X(82)90077-2

Maurel MC, Malfatti A, Debenedetti A, Catalano A, Barile VL. Detection of the preovulatory LH surge in the buffalo by an enzyme-immunologic assay. Reproduction and Animal Breeding advances and strategy, Enne G, Greppi GF, Lauria A, Ed.; Elsevier Amsterdam 1995; pp. 405-6.

Rahe CH, Owens RE, Fleiger JL, Newton HJ, Harms PG. Pattern of plasma luteinizing hormone in the cyclic cow: Dependence upon the period of the cycle. Endocrinol 1980; 107: 498-505. http://dx.doi.org/10.1210/endo-107-2-498 DOI: https://doi.org/10.1210/endo-107-2-498

Sheth A, Wadadekar RKB, Moodbidri SB, Janakiraman J, Parameshwardan M. Seasonal alteration in serum prolactin and LH levels in water buffalo. Curr Sci 1978; 47: 75-7.

Heranja DD, Sheth AR, Desai R, Rao SS. Serum gonadotropins and prolactin levels during oestrous cycle in Murrah buffaloes. Ind J Dairy Sci 1979; 32: 247-9.

Arora RC, Pandey RS. Plasma concentration of progesterone, oestradiol-17 and luteinizing hormone in relation to repeat breeding in buffalo (Bubalus bubalis). Anim Prod 1982; 34: 139-44. http://dx.doi.org/10.1017/S0003356100000611 DOI: https://doi.org/10.1017/S0003356100000611

Kanai Y, Shimizu H. Plasma concentrations of LH, progesterone and oestradiol during oestrous cycle in Swamp buffaloes (Bubalus bubalis). J Reprod Fertil 1984; 70: 507-10. http://dx.doi.org/10.1530/jrf.0.0700507 DOI: https://doi.org/10.1530/jrf.0.0700507

Avenell JA, Saepudin Y, Fletcher IC. Concentrations of LH and progesterone in the peripheral plasma of Swamp buffalo cow (Bubalus bubalis) around the time of estrus. J Reprod Fertil 1985; 74: 419-24. http://dx.doi.org/10.1530/jrf.0.0740419 DOI: https://doi.org/10.1530/jrf.0.0740419

Barile VL, Galasso A, Terzano GM, Malfatti A, Barbato O. Valutazione del picco di LH in bufale sottoposte a sincronizzazione dell'estro ai fini della inseminazione artificiale. Atti S.I.S.Vet. 1998; 52: 85-86.

Kumar R, Jindal R, Rattan PJS. Plasma hormonal profiles during oestrous cycle of Murrah buffalo heifers. Ind J Anim Sci 1991; 61: 382-5.

Kanai Y, Shimizu H. Changes in the plasma concentration of luteinizing hormone, progesterone and oestradiol-17 during the periovulatory period in cyclic Swamp buffaloes (Bubalus bubalis). Anim Reprod Sci 1986; 11: 17-24. http://dx.doi.org/10.1016/0378-4320(86)90098-9 DOI: https://doi.org/10.1016/0378-4320(86)90098-9

Aboul Ela, Barkawi AH. Pulsatile secretion of LH in cyclic buffalo heifer as affected by season and stage of oestrous cycle. In Proceedings of 11th International Congress on Animal Reproduction and Artificial Insemination, Dublin, Ireland 1988; 2: 3.

Moioli BM, Napolitano F, Puppo S, et al. Patterns of oestrus, time of LH release and ovulation and effects of time of artificial insemination in Mediterranean buffalo cows. Anim Sci 1998; 66: 87-91. http://dx.doi.org/10.1017/S1357729800008869 DOI: https://doi.org/10.1017/S1357729800008869

Borghese A, Barile VL, Terzano GM, Galasso A, Malfatti A, Barbato O. Time of LH peak in oestrus synchronized buffaloes in two different season. Proc 50th EAAP Annual Meeting, Zurich, Switzerland 1999; 166.

Terzano GM, Malfatti A, Todini L, et al. Timing of the LH peak and P4 blood concentration after the ovulations in buffalo cows during different superovulatory treatments. 60th Annual Meeting of the European Association for Animal Production; Barcelona, Spain 2009; p. 389.

Razdan MN, Kakkar ML. Summer sterility and endocrine profiles of buffaloes. Ind Dairyman 1980; 32: 459-64.

Clegg MT, Ganong WF. The effect of hypothalamic lesions on ovarian function in the ewe. Endocrinol 1960; 67: 179-86. http://dx.doi.org/10.1210/endo-67-2-179 DOI: https://doi.org/10.1210/endo-67-2-179

Radford HM. The effect of hypothalamic lesions on reproductive activity in sheep. J Endocrinol 1967; 39: 415-22. http://dx.doi.org/10.1677/joe.0.0390415 DOI: https://doi.org/10.1677/joe.0.0390415

Karsch FJ, Legan SJ, Ryan KD, Foster DL. Importance of oestradiol and progesterone in regulating LH secretion and oestrus behaviour during the sheep oestrous cycle. Biol Reprod 1980; 23: 404-13. http://dx.doi.org/10.1095/biolreprod23.2.404 DOI: https://doi.org/10.1095/biolreprod23.2.404

Lockwood GM, Muttukrishna S, Groome NP. Circulating inhibins and activin-A during GnRH-analogue down-regulation and ovarian hyperstimulation with recombinant FSH for in vitro ertilization-embryo transfer. Clin Endocrinol 1996; 45: 741-48. http://dx.doi.org/10.1046/j.1365-2265.1996.8510861.x DOI: https://doi.org/10.1046/j.1365-2265.1996.8510861.x

Seifer DB, Lambert-Messerlian G, Hogan JW. Day 3 Serum inhibin-B is predictive of assisted reproductive technologies outcome. J Fertil Steril 1997; 67: 110-14. http://dx.doi.org/10.1016/S0015-0282(97)81865-1 DOI: https://doi.org/10.1016/S0015-0282(97)81865-1

Findlay JK. Peripheral and local regulators of folliculogenesis. Reproduction, Fertility and Development 1994; 6: 127-39. http://dx.doi.org/10.1071/RD9940127 DOI: https://doi.org/10.1071/RD9940127

Knight PG. Roles of inhibin, activins and follstatin in female reproductive system. Front Neuroendocrinol 1996; 17: 476-509. http://dx.doi.org/10.1006/frne.1996.0013 DOI: https://doi.org/10.1006/frne.1996.0013

Tsigkou A, Luisi S, Reis FM, Petraglia F. Inhibins as diagnostic markers in human re production. Adv Clin Chem 2008; 45: 1-29. http://dx.doi.org/10.1016/S0065-2423(07)00001-7 DOI: https://doi.org/10.1016/S0065-2423(07)00001-7

Buckler HM, Robertson WR, Sun JG, Morris ID. Immunoactive inhibin levels during ovarian hyperstimulation may predict granulosa cell maturity. Clin Endocrinol 1992; 37: 552-7. http://dx.doi.org/10.1111/j.1365-2265.1992.tb01487.x DOI: https://doi.org/10.1111/j.1365-2265.1992.tb01487.x

Mitchell R, Buckler HM, Matson P. Oestradiol and immunoreactive inhibin-like secretory patterns following controlled ovarian hyperstimulation with urinary (Metrodin) or recombinant follicle stimulating hormone (Puregon). Hum Reprod 1996; 11: 962-7. http://dx.doi.org/10.1093/oxfordjournals.humrep.a019332 DOI: https://doi.org/10.1093/oxfordjournals.humrep.a019332

Schneyer AL, Mason AJ, Burton LE. Immunoreactive Inhibin-Alpha-subunit in human serum: implication for radioimmunoassay. J Clin Endocrinol Metab 1990; 70: 1208-12. http://dx.doi.org/10.1210/jcem-70-4-1208 DOI: https://doi.org/10.1210/jcem-70-4-1208

Miyamoto A, Umezu M, Ishii S, et al. Serum inhibin, FSH, LH, and testosterone levels and testicular inhibin content in beef bulls from birth to puberty. Anim Reprod Sci 1989; 20: 165-78. http://dx.doi.org/10.1016/0378-4320(89)90082-1 DOI: https://doi.org/10.1016/0378-4320(89)90082-1

Matsubayashi K, Watanabe G, Taya K, et al. Seasonal changes in plasma concentrations of immunoreactive Inhibin-And testicular activity in male Japanese monkeys. Biol Reprod1991; 44: 822-26. http://dx.doi.org/10.1095/biolreprod44.5.822 DOI: https://doi.org/10.1095/biolreprod44.5.822

Lee VWK, Cumming IA, deKretser DM, Findlay JK, Hudson B, Keogh EJ, Regulation of gonadotrophin secretion in rams from birth to sexual maturity. 1. Plasma LH, FSH, and testosterone levels. J Reprod Fertil 1976; 46: 1-6. http://dx.doi.org/10.1530/jrf.0.0460001 DOI: https://doi.org/10.1530/jrf.0.0460007

Kentaro N, Yasuo N, Natsuko N, et al. A selective increase in circulating Inhibin- And inhibin pro- C at the time of ovulation in the mare. Am J Physiol Endocrinol Metab 1999; 277: E870-E875. DOI: https://doi.org/10.1152/ajpendo.1999.277.5.E870

Medan Mohamed S, Yasuo N, Natsuko N, Hiromi S, Gen W, Nigel G. Kazuyoshi TPlasma concentrations of ir-inhibin, Inhibin-A, inhibin pro-C, FSH, and estradiol-17during estrous cycle in mares and their relationship with follicular growth Endocrine. Endocrine 2004; 25: 7-14. DOI: https://doi.org/10.1385/ENDO:25:1:07

Price CA, Salah N, Groome NP. Plasma concentrations of dimeric inhibin and oestradiol in heifers undergoing superovulation with eCG or FSH. J Reprod Fertility 1995; 49: 507-10.

Tohei A, Shi F, Ozawa M, et al. Dynamic changes in plasma concentration of gonadotropins, inhibins, estradiol-17 and P4 in cows with ultrasound-guided follicular aspiration. J Vet Med Sci 2001; 63 (1): 45-50. DOI: https://doi.org/10.1292/jvms.63.45

Bleach ECL, Glencross RG, Feist SA, Groome NP, Knight PGPlasma inhibin-A in heifers: relationship with follicle dynamics, gonadotropins, and steroids during the estrous cycle and after treatment with bovine follicular fluid. Biol Reprod 2001; 64: 743-52. http://dx.doi.org/10.1095/biolreprod64.3.743 DOI: https://doi.org/10.1095/biolreprod64.3.743

Nakada K, Moriyoshi M, Nakao T, Watanabe G, Taya K. Changes in concentrations of plasma immunoreactive follicle-stimulating hormone, luteinizing hormone, estradiol-17, testosterone, P4 and inhibin in heifers from birth to puberty. Dom Anim Endocrinol 2000; 18: 57-69. DOI: https://doi.org/10.1016/S0739-7240(99)00063-6

Palta P, Kumar M, Jailkani S, Manik RS, Madan ML. Changes in peripheral inhibin levels and follicular development following treatment of buffalo with PMSG and Neutra-PMSG for superovulation. Theriogenology 1997; 48: 233-40. http://dx.doi.org/10.1016/S0093-691X(97)84070-8 DOI: https://doi.org/10.1016/S0093-691X(97)84070-8

Malfatti A, Terzano GM, Neglia G, Maschio M, Allegrini S, Todini L. Follicular development, plasma Inhibin-A and Estradiol-17-beta concentrations in Buffalo cows during different treatment schedules for MOET programs. Italian J Anim Sci 2007; 6(2): 684-7. DOI: https://doi.org/10.4081/ijas.2007.s2.684

Terzano GM. Inhibin-A: experiences and role in buffalo reproductive physiology. Revista Veterinaria; Guest Editors: Gustavo A. Crudeli, Exequiel M. Patino, Josè L. Konrad; 2010; 21(1): 172-8.

Palta P, Mondal S, Prakash BS, Madan ML. Peripheral inhibin levels in relation to climatic variations and stage of estrous cycle in buffalo. Theriogenology 1997; 47: 989-95. http://dx.doi.org/10.1016/S0093-691X(97)00055-1 DOI: https://doi.org/10.1016/S0093-691X(97)00055-1

Terzano GM, Catone G, Todini L, et al. Plasma inhibin A level and follicular development in prepuberal buffalo heifers superovulated with FSH or FSH/eCG: preliminary results. Proc. Seventh World Buffalo Congress, Manila, Philippines 2004; pp. 644-7.

Barbato O, Sousa NM, Malfatti A, Beckers JF, De Santis G, Debenedetti A. Purification of pregnancy-associated glycoproteins (Pags) in buffalo (Bubalus bubalis): preliminary results. Atti Secondo Congresso Nazionale sull'Allevamento del Bufalo, Monterotondo, Roma 2003; pp. 279-83.

Gonzalez F, Calero P, Quesada E, Garbayo JM, Beckers JF. The Pregnancy Associated Glycoproteins (PAGs) in the caprine species: fundamental and clinical approach. International Conference on Goats 2000; 1: 413-5.

Butler JE, Hamilton WC, Sasser RG, Ruder CA, Hass GM, Williams J. Detection and partial characterization of two

bovine pregnancy-specific proteins. Biol Riprod 1982; 26: 925-33. http://dx.doi.org/10.1095/biolreprod26.5.925 DOI: https://doi.org/10.1095/biolreprod26.5.925

Willard ST, White DR, Wesson CAR, Stellflug J, Sasser RG. Detection of fetal twins in sheep using a radioimmunoassay for pregnancy-specific proteins. J Anim Sci 1995 ; 73: 960-6. DOI: https://doi.org/10.2527/1995.734960x

Zoli AP, Beckers JF, Ectors F. Isolement et caractérization partielle d'une glycoproteine associée à la gestation chez la brebis. Ann Med Veterin 1995; 139: 177-84.

Garbayo JM, Remy B, Alabart JL, et al. Isolation and partial characterization of a pregnancy-associated glycoprotein (PAG) family from the goat placenta. Biol Reprod 1998; 58 (1): 109-15. http://dx.doi.org/10.1095/biolreprod58.1.109 DOI: https://doi.org/10.1095/biolreprod58.1.109

Debenedetti A, Malfatti A, Borghese A, Barile VL, Humblot P. Pregnancy specific protein B (PSPB) detection by RIA in buffalo cows. Proc. Fifth World Buffalo Congress. Caserta, Italy 1997; pp. 771-775.

Malfatti A, Debenedetti A, Barbato O, Mancini L, Borghese A, Terzano GM. II dosaggio delle glicoprotoine associato alla gravidanza (PAG, PSPB) nella bufala. Atti Primo Congr. Naz. sull'Allevamento del Bufalo, Eboli, ltaly 2001; pp. 332-6.

Humblot P, Camous S, Martal J, et al. Pregnancy-specific protein B, P4 concentrations and embryonic mortality during early pregnancy in dairy cows. J Reprod Fert 1988; 83: 215-23. http://dx.doi.org/10.1530/jrf.0.0830215 DOI: https://doi.org/10.1530/jrf.0.0830215

Zachow RJ, Weitsman SR, Magoffin DA. Leptin impairs the synergistic stimulation by transforming growth factor-beta of follicle-stimulating hormonedependent aromatase activity and messenger ribonucleic acid expression in rat ovarian granulosa cells. Biol Reprod 1999; 61: 1104-09. http://dx.doi.org/10.1095/biolreprod61.4.1104 DOI: https://doi.org/10.1095/biolreprod61.4.1104

Agarwal SK, Vogel K, Weitsman SR, Magoffin DA. Leptin antagonizes the insulin-like growth factor-I augmentation of steroidogenesis in granulosa and theca cells of the human ovary. J Clin Endocrinol Metab 1999; 84: 1072-76. http://dx.doi.org/10.1210/jc.84.3.1072 DOI: https://doi.org/10.1210/jc.84.3.1072

Brannian LJD, Zhao Y, McElroy M. Leptin inhibits gonadotrophin-stimulated granulosa cell P4 production by antagonizing insulin action. Hum Reprod 1999; 14: 1445-8. http://dx.doi.org/10.1093/humrep/14.6.1445 DOI: https://doi.org/10.1093/humrep/14.6.1445

Campbell BK, Guitierrez CG, Armstrong DG, Webb R, Baird DT. Leptin: In vitro and in vivo evidence for direct effects on the ovary in monovulatory ruminants. Human Reprod 2000; 14: 15-6. DOI: https://doi.org/10.1093/humrep/14.Suppl_3.15

Barb CR, Kraeling RR. Role of leptin in the regulation of gonadotropin secretion in farm animals. Anim Reprod Sci 2004; 82: 155-67. http://dx.doi.org/10.1016/j.anireprosci.2004.04.032 DOI: https://doi.org/10.1016/j.anireprosci.2004.04.032

Vallinoto M, Schneider MPC, Silva A, Iannuzzi L, Brenig B. Molecular cloning and analysis of the swamp and river buffalo leptin gene. Anim Genet 2004; 35: 462-3. http://dx.doi.org/10.1111/j.1365-2052.2004.01186.x DOI: https://doi.org/10.1111/j.1365-2052.2004.01186.x

Orrù L, Terzano GM, Napolitano F, et al. DNA Polymorphisms in River Buffalo Leptin GeneItal. J Anim Sci 2007; 6(2): 342-4. DOI: https://doi.org/10.4081/ijas.2007.s2.342

Mihaiu R, Mihaiu M, Pintea A, et al. Comparative Study on the Fat Acids Profile from Buffalo Milk as Quality and Traceability Markers. Bulletin UASVM, Veterinary Medicine 2010; 67(2): 161-5.

Liefers SC, te Pas MFW, Veerkamp RF, van der Lende T. Association between leptin gene polymorphism and production, live weight, energy balance, feed intake and fertility in Holstein Heifers. J Dairy Sci 2002; 85: 1633-8. http://dx.doi.org/10.3168/jds.S0022-0302(02)74235-5 DOI: https://doi.org/10.3168/jds.S0022-0302(02)74235-5

Buchanan FC, Fitzsimmons CI, Van Kassel AG, Thue TD, Winkelman-Sim DC, Schumutz SM. Association of a missense mutation in the bovine leptin gene with carcass fat content and leptin mRNA levels. Genet Sel Evol 2002; 34: 105-16. http://dx.doi.org/10.1186/1297-9686-34-1-105 DOI: https://doi.org/10.1051/gse:2001006

Buchanan FC, Van Kassel AG, Waldner C, Christensen DA, Laarveld B, Schmutz SM. Hot Topic: an association between a leptin single nucleotide polymorphism and milk and protein yeld. J Dairy Sci 2003; 86: 3164-6. http://dx.doi.org/10.3168/jds.S0022-0302(03)73918-6 DOI: https://doi.org/10.3168/jds.S0022-0302(03)73918-6