Advertisement

Effect of progesterone administration during growing phase of first dominant follicle on follicular wave pattern in buffalo heifers

  • M. H. JanEmail author
  • H. Kumar
  • S. Kumar
  • R. K. Sharma
  • A. Gupta
  • K. L. Mehrara
Regular Articles
  • 16 Downloads

Abstract

In buffaloes, like other domestic mammals, antral follicles develop in a wave-like pattern. Factors predictive of a particular follicular wave pattern are yet to be identified. In this study, we examined the preponderance of 2- versus 3-wave patterns in 46 interovulatory intervals (IOIs) from 36 buffalo heifers, in which a subset of 10 heifers was scanned for 2 consecutive IOIs to record the repeatability of follicular wave pattern. Two-wave pattern was detected in 63.0% and 3-wave follicular pattern in 27.0% IOIs. The dominant follicles (DF) of both wave 1 as well as the ovulatory wave attained a smaller (P < 0.05) maximum diameter in 3-wave cycle as compared to 2-wave cycle. The mean duration of IOI was significantly shorter in 2-wave compared to three-wave cycles (20.5 ± 0.3 vs. 22.3 ± 0.2 days; P < 0.05). Out of 10 buffalo heifers, 7 displayed non-alternating patterns and 3 had alternating follicular wave patterns. We also tested the hypothesis that progesterone administration during early IOI results in increased preponderance of 3-wave pattern and heifers inseminated after ovulation of the third wave DF will have greater fertility. Sixteen heifers subjected to progesterone treatment from D0 (day of ovulation) in a decreasing dose until D5 were compared with control heifers (n = 10). Progesterone treatment significantly reduced the maximum diameter of DF of wave 1 (P < 0.001), whereas the mean duration of IOI remained unchanged (P > 0.05) between the two groups. Progesterone administration during early IOI significantly increased the proportion of 3-wave cycles as compared to control (P < 0.05). The hypothesis that progesterone administration during IOI results in increased preponderance of 3-wave pattern was supported. However, no change in fertility was recorded in progesterone-treated heifers (7 pregnant out of 16; 43.8%) as compared to untreated control heifers (4 out of 10 heifers; 40.0%). In summary, progesterone administration in buffalo heifers during the growing phase of wave 1 resulted in greater preponderance of 3-wave follicular patterns, with no significant effect on fertility.

Keywords

Buffalo heifers Follicular wave Fertility Interovulatory interval Progesterone 

Notes

Acknowledgements

Our thanks to Director, ICAR-Central Institute for Research on Buffaloes for providing necessary facilities.

Authors’ contributions

M. H. Jan conducted the experiment and prepared the manuscript, S. Kumar and A. Gupta assisted in animal experimentation, K. L. Mehrara provided assistance in animal handling and ultrasonography, R. K. Sharma and H. Kumar conceived and supervised the work.

Funding information

This study was funded by ICAR-Central Institute for Research on Buffaloes, Hisar (Haryana), India.

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflict of interest.

References

  1. Adams, G.P., Matteri, R.L.and Ginther, O.J., 1992. Effect of progesterone on ovarian follicles, emergence of follicular waves and circulating follicle-stimulating hormone in heifers. Journal of Reproduction and Fertility, 95, 627–640.CrossRefGoogle Scholar
  2. Adams, G.P., Kot, K., Smith, C.A. and Ginther, O.J., 1993. Effect of the dominant follicle on regression of its subordinates in heifers. Canadian Journal of Animal Science, 73, 267–275.CrossRefGoogle Scholar
  3. Ahmad, N., Beam, S.W., Butler, W., Deaver, D., Duby, R.T., Elder, D. Fortune, J.E., Griel Jr, L.C., Jones, L.S., Milvae, R., Pate, J., Revah, I., Schreiber Jr, D.T., Townson, D., Tsang, P.C.W. and Inskeep, K., 1996. Relationship of fertility to patterns of ovarian follicular development and associated hormonal profiles in dairy cows and heifers. Journal of Animal Science, 74, 1943–1952.CrossRefGoogle Scholar
  4. Ahmad, N., Townsend, E.C., Dailey, R.A. and Inskeep, E.K., 1997. Relationship of hormonal patterns and fertility to occurrence of two or three waves of ovarian follicles, before and after breeding, in beef cows and heifers. Animal Reproduction Science, 49, 13–28.PubMedCrossRefGoogle Scholar
  5. Araujo, R.R., Ginther, O.J., Ferreira, J.C., Palhão, M.M., Beg, M.A. and Wiltbank, M.C., 2009. Role of follicular estradiol-17beta in timing of luteolysis in heifers. Biology of Reproduction, 81, 426–437.PubMedPubMedCentralCrossRefGoogle Scholar
  6. Austin, E.J., Mihm, M., Ryan, M.P., Williams, D.H.and Roche, J.F., 1999. Effect of duration of dominance of the ovulatory follicle on onset of estrus and fertility in heifers. Journal of Animal Science, 77, 2219–2226.PubMedCrossRefGoogle Scholar
  7. Badinga, L., Thatcher, W.W., Diaz, T., Drost, M. and Wolfenson, D., 1993. Effect of environmental heat stress on follicular development and steroidogenesis in lactating Holstein cows. Theriogenology, 39(4), 797–810.PubMedCrossRefGoogle Scholar
  8. Baruselli, P.S., Mucciolo, R.G., Visintin, J.A., Viana, W.G., Arruda, R.P., Madureira, E.H., Oliveira, C.A. and Molero-Filho, J.R., 1997. Ovarian follicular dynamics during the oestrus cycle in buffalo (Bubalus bubalis). Theriogenology, 47, 1531–1547.PubMedCrossRefGoogle Scholar
  9. Bleach, E.C.L., Glencross, R.G. and Knight, P.G., 2004. Association between ovarian follicle development and pregnancy rates in dairy cows undergoing spontaneous oestrous cycles. Reproduction, 127, 621–629.PubMedCrossRefGoogle Scholar
  10. Boer, H.M.T., Röblitz, S., Stötzel, C., Veerkamp, R.F., Kemp, B. and Woelders, H., 2011. Mechanisms regulating follicle wave patterns in the bovine estrous cycle investigated with a mathematical model. Journal of Dairy Science, 94(12), 5987–6000.PubMedCrossRefGoogle Scholar
  11. Burke, C.R., Mihm, M., Macmillan, K.L. and Roche, J.F., 1994. Some effects of prematurely elevated concentrations of progesterone on luteal and follicular characteristics during the oestrous cycle in heifers. Animal Reproduction Science, 35, 27–39.CrossRefGoogle Scholar
  12. Celik, H.A., Aydin, I., Sendag, S. and Dinc, D.A., 2005. Number of follicular waves and their effect on pregnancy rate in the cow. Reproduction in Domestic Animals, 40, 87–92.PubMedCrossRefGoogle Scholar
  13. Fortune, J.E., 1993. Follicular dynamics during the bovine estrous cycle: a limiting factor in improvement of fertility? Animal Reproduction Science, 33, 111–125.CrossRefGoogle Scholar
  14. Fortune, J.E., Sirois, J. and Quirk, S.M., 1988. The growth and differentiation of ovarian follicles during the bovine estrous cycle. Theriogenology, 29, 95–109.CrossRefGoogle Scholar
  15. Ginther, O.J., 1970. Effect of progesterone on length of estrous cycle in cattle. American Journal of Veterinary Research, 31, 493–496.PubMedGoogle Scholar
  16. Ginther O.J. and Bashir, S.T., 2013. Length of the luteal phase and frequency of the four permutations between two or three follicular waves and ipsilateral or contralateral locations of the corpus luteum and ovulatory follicle in heifers. Theriogenology, 80(2), 114–119.PubMedCrossRefGoogle Scholar
  17. Ginther, O.J., Kastelic, J.P. and Knopf, L., 1989a. Composition and characteristics of follicular waves during the bovine oestrous cycle. Animal Reproduction Science, 20, 187–200.CrossRefGoogle Scholar
  18. Ginther, O.J., Kastelic, J.P. and Knopf, L., 1989b. Intraovarian relationship among dominant and subordinate follicles and corpus luteum in heifers. Theriogenology, 32, 787–795.PubMedCrossRefGoogle Scholar
  19. Ginther, O.J., Bashir, S.T., Hoffman, M.M. and Beg, M.A., 2013a. Endocrinology of number of follicular waves per estrous cycle and contralateral or ipsilateral relationship between corpus luteum and preovulatory follicle in heifers. Domestic Animal Endocrinology, 45(2), 64–71.PubMedCrossRefGoogle Scholar
  20. Ginther, O.J., Bashir, S.T., Rakesh, H.B. and Hoffman, M.M., 2013b. Hormone concentrations temporally associated with contralateral and ipsilateral relationships between corpus luteum and preovulatory follicle during the third follicular wave in heifers. Theriogenology, 80(7), 738–747.PubMedCrossRefGoogle Scholar
  21. Ginther, O.J., Bashir, S.T., Rakesh, H.B. and Hoffman, M.M., 2013c. Two-way coupling between FSH and the dominant follicle in heifers. Theriogenology, 80(5), 463–469PubMedCrossRefGoogle Scholar
  22. Ginther, O.J., Bashir, S.T., Santos, V.G. and Beg, M.A., 2013d. Contralateral ovarian location between the future ovulatory follicle and extant corpus luteum increases the length of the luteal phase and number of follicular waves in heifers. Theriogenology, 79(7), 1130–1138.PubMedCrossRefGoogle Scholar
  23. Ginther, O.J., Rakesh, H.B., Bashir, S.T. and Hoffman, M.M., 2014a. Relationship between days of the luteolytic period and locations of the preovulatory follicle and CL in interovulatory intervals with two or three follicular waves in heifers. Theriogenology, 81(6), 787–-796.PubMedCrossRefGoogle Scholar
  24. Ginther, O.J., Rakesh, H.B., Bashir, S.T. and Hoffman, M.M., 2014b. Minor FSH surge, minor follicular wave, and resurgence of preovulatory follicle several days before ovulation in heifers. Theriogenology, 81(3), 437–445.PubMedCrossRefGoogle Scholar
  25. Ginther, O.J., Baldrighi, J.M., Siddiqui, M.A.R., Bashir, S.T. and Rakesh, H.B., 2015. Mechanism for greater frequency of contralateral than ipsilateral relationship between corpus luteum and ovulatory follicle for wave 3 in heifers. A review. Theriogenology, 85(3), 361–367.PubMedCrossRefGoogle Scholar
  26. Imron, M., Cipelang, B.E.T., Supriatna, I. and Setiadi, M.A., 2016. Follicular dynamic and repeatability of follicular wave development in Peranakan Ongole (PO) cattle. JITV:Indonesian Journal Animal and Veterinary Science, 21, 26–33.CrossRefGoogle Scholar
  27. Ireland, J.J. and Roche, J.F., 1982. Effect of progesterone on basal LH and episodic LH and FSH secretion in heifers. Journal of Reproduction and Fertility, 64, 295–302.PubMedCrossRefGoogle Scholar
  28. Jaiswal, R.S., 2007. Regulation of follicular wave pattern in cattle. Thesis, Ph.D. University of Saskatchewan, Saskatoon. p.106.Google Scholar
  29. Jaiswal, R.S., Singh, J., Marshall, L. and Adams, G.P. 2009. Repeatability of 2-wave and 3-wave patterns of ovarian follicular development during the bovine estrous cycle. Theriogenology, 72, 81–90.PubMedCrossRefGoogle Scholar
  30. Kastelic, J.P., Ko, J.C.H. and Ginther, O.J., 1990. Suppression of dominant and subordinate ovarian follicles by a proteinaceous fraction of follicular fluid in heifers. Theriogenology, 34, 499–509.PubMedCrossRefGoogle Scholar
  31. Ko, J.C.H., Kastelic, J.P., Del Campo, M.R. and Ginther, O.J., 1991. Effects of a dominant follicle on ovarian follicular dynamics during the oestrous cycle in heifers. Journal of Reproduction and Fertility, 91, 511–519.PubMedCrossRefGoogle Scholar
  32. Lemon, M., 1975.The effect of oestrogens alone or in association with progestagens on the formation and regression of the corpus luteum of the cyclic cow. Annales de Biologie Animale, Biochimie, Biophysique, 15, 243–253.CrossRefGoogle Scholar
  33. Mackey, D.R., Wylie, A.R., Sreenan, J.M., Roche, J.F. and Diskin, M.G., 2000. The effect of acute nutritional change on follicle wave turnover, gonadotropin, and steroid concentration in beef heifers. Journal of Animal Science, 78, 429–442.PubMedCrossRefGoogle Scholar
  34. Manik, R.S., Singla, S.K., Palta, P. and Madan, M.L., 1998. Ovarian follicular dynamics monitored by real-time ultrasonography during oestrous cycle in buffalo (Bubalus bubalis). Asian-Australasian Journal of Animal Sciences, 11, 480–485.CrossRefGoogle Scholar
  35. Menchaca, A. and Rubianes, E., 2002. Relation between progesterone concentrations during the early luteal phase and follicular dynamics in goats. Theriogenology, 57, 1411–1419.PubMedCrossRefGoogle Scholar
  36. Mihm, M., Baguisi, M.A., Boland, M.P. and Roche, J.F., 1994.Association between the duration of dominance of the ovulatory follicle and pregnancy rate in beef heifers. Journal of Reproduction and Fertility, 102, 123–130.PubMedCrossRefGoogle Scholar
  37. Murphy, M.G., Enright, W.J., Crowe, M.A., McConnell, K., Spicer, L.J., Boland, M.P. and Roche, J.F., 1991. Effect of dietary intake on pattern of growth of dominant follicles during the oestrous cycle in beef heifers. Journal of Reproduction and Fertility, 92, 333–338.PubMedCrossRefGoogle Scholar
  38. Paul, S.S. and Patil, N.V., 2007. Energy and protein requirements of growing Nili-Ravi buffalo heifers in tropical environment. Journal of Science of Food and Agriculture, 87(12), 2286–2293.CrossRefGoogle Scholar
  39. Perez-Marin, C.C., Rodriguez, I., Dorado, J., Hidalgo, M., Sanz, J. and Espana, F., 2003. Follicular growth patterns in repeat breeder cows. Veterinarni Medicina Czech, 48, 1–8.Google Scholar
  40. Price, C.A. and Carriere, P.D., 2004. Alternate two- and three follicle wave interovulatory intervals in holstein heifers monitored for two consecutive estrous cycles. Canadian Journal of Animal Science, 84, 145–147.CrossRefGoogle Scholar
  41. Rubianes, E., de Castro, T. and Carbajal, B., 1996. Effect of high progesterone levels during the growing phase of the dominant follicle of wave 1 in ultrasonically monitored ewes. Canadian Journal of Animal Science, 76, 473–475.CrossRefGoogle Scholar
  42. Savio, J.D., Keenan, L., Boland, M.P. and Roche, J.F., 1988. Pattern of growth of dominant follicles during the estrous cycle in heifers. Journal of Reproduction and Fertility, 83: 663–671.PubMedCrossRefGoogle Scholar
  43. Sichtar, J., Tolman, R., Rajmon, R., Klabanová, P., Berka, P. and Volek, J., 2010. A comparison of the follicular dynamics in heifers of the Czech Fleckvieh and Holstein breeds. Czech Journal of Animal Science 55, 234–242.CrossRefGoogle Scholar
  44. Singh, J., Pierson, R.A. and Adams, G.P., 1998. Ultrasound image attributes of bovine ovarian follicles and endocrine and functional correlates. Journal of Reproduction and Fertility, 112, 19–29.PubMedCrossRefGoogle Scholar
  45. Sirois, J. and Fortune, J.E., 1988. Ovarian follicular dynamics during the estrous cycle in heifers monitored by real-time ultrasonography. Biology of Reproduction, 39, 308–317.PubMedCrossRefGoogle Scholar
  46. Townson, D.H., Tsang, P.C.W., Butler, W.R., Frajblat, M., Griel, L.C., Johnson, C.J., Milvae, R.A., Niksic, G.M. and Pate, J.L., 2002. Relationship of fertility to ovarian follicular waves before breeding in dairy cows. Journal of Animal Science, 80, 1053–1058.PubMedCrossRefGoogle Scholar
  47. Vassena, R., Mapletoft, R.J., Allodi, S., Singh, J. and Adams, G.P., 2003. Morphology and developmental competence of bovine oocytes relative to follicular status. Theriogenology, 60, 923–932.PubMedCrossRefGoogle Scholar
  48. Villa-Godoy, A., Ireland, J.J., Wortman, J.A., Ames, N.K., Hughes, T.L. and Fogwell, R., 1985. Effect of ovarian follicles on luteal regression in heifers. Journal of Animal Science, 60, 519–527.PubMedCrossRefGoogle Scholar
  49. Viñoles, C., Meikle, A., Forsberg, M. and Rubianes, E., 1999.The effect of subluteal levels of exogenous progesterone on follicular dynamics and endocrine patterns during the early luteal phase of the ewe. Theriogenology, 51(7), 1351–1361.PubMedCrossRefGoogle Scholar
  50. Warriach, H.M. and Ahmad, N., 2007. Follicular waves during the oestrous cycle in Nili-Ravi buffaloes undergoing spontaneous and PGF 2α-induced luteolysis. Animal Reproduction Science, 101, 332–337.PubMedCrossRefGoogle Scholar
  51. Wilson, S.J., Marion, R.S., Spain, J.N., Spiers, D.E., Keisler, D.H. and Lucy, M.C., 1998. Effects of Controlled Heat Stress on Ovarian Function of Dairy Cattle. 1. Lactating Cows. Journal of Dairy Science, 81, 2124–2131.PubMedCrossRefGoogle Scholar

Copyright information

© Springer Nature B.V. 2019

Authors and Affiliations

  1. 1.ICAR-Central Institute for Research on BuffaloesNabhaIndia
  2. 2.ICAR-Indian Veterinary Research InstituteIzatnagarIndia
  3. 3.ICAR-Central Institute for Research on BuffaloesHisarIndia

Personalised recommendations