Elsevier

Animal Reproduction Science

Volume 202, March 2019, Pages 80-86
Animal Reproduction Science

Effect of plasma progesterone on oocyte recovery, oocyte quality, and early in-vitro developmental competence of embryos in Bos indicus dairy cows

https://doi.org/10.1016/j.anireprosci.2019.02.001Get rights and content

Abstract

The objective of present study was to determine the effect of plasma progesterone (P4) on oocyte recovery, oocyte quality, and early in-vitro developmental competence of embryos in Bos indicus dairy cows. The ovaries were collected in an abattoir. These ovaries (n = 750) were divided into two groups: 1) estrous CYCLIC (n = 318), and 2) estrous ACYCLIC (n = 432). Mean serum concentrations of P4 in a subset of (n = 85; 4.21 ± 0.4 ng/ml compared with 0.5 ± 0.2 ng/ml; P <  0.05) were greater in estrous CYCLIC as compared to ACYCLIC cows, respectively. The mean number of oocytes recovered per ovary (6.5 ± 0.5 compared with 4.0 ± 0.2; P <  0.05) was greater for estrous CYCLIC than ACYCLIC cows, respectively. The oocytes with grade I_+_II quality (55.3% compared with 47.6%; P <  0.05) were greater, whereas, there was lesser percentage with grade III_+_IV quality (44.5% compared with 52.4%; P <  0.05) from estrous CYCLIC as compared with ACYCLIC cows, respectively. Cleavage rate (70.9% compared with 52.8%; P < 0.05) was greater for embryos derived from estrous CYCLIC than ACYCLIC cows, respectively. Similarly, the embryo developmental rates to the 8- (38.5% compared with 20.8%; P < 0.05) and 16- (20.0% compared with 10.9%; P < 0.05) cell stage were greater for embryos derived from estrous CYCLIC as compared to ACYCLIC cows, respectively. In conclusion, the presence of greater plasma P4 has a beneficial effect on oocyte recovery, oocyte quality, and early IVEP outcomes in Bos indicus dairy cows.

Introduction

Assisted reproductive technologies have resulted in modernization of the dairy industry for the rapid multiplication of superior genetics (Moore and Hasler, 2017). The exploitation of genetics through in-vitro embryo production (IVEP) in farm animals, however, remained a challenge during the last 2 decades (Thompson, 1997). There are several factors that affect the outcome when there is use of IVEP, which include 1) ovarian follicular size in cows from which oocytes are collected (Pavlok et al., 1992; Lonergan et al., 1994a), 2) preparation method for sperm used for IVEP (Parrish et al., 1995), 3) lactation number of cows from which oocytes are collected (Snijders et al., 2000a), 4) ovarian phase of cows from which oocytes are collected (De Wit et al., 2000), 5) body condition score (BCS) of cows from which oocytes are collected (Snijders et al., 2000b), 6) heat stress of cows from which oocytes are collected (Wolfenson et al., 2000), 7) season of year when oocytes are collected (Al-Katanani et al., 2002), 8) origin of oocytes (Lonergan et al., 2003), 9) growth factors in follicle in which oocytes developed (Purohit et al., 2005), 10) presence of corpus luteum (CL) in cows from which oocytes are collected (Boediono et al., 1995), and 11) plasma P4 concentration in cows from which oocytes are collected (McEvoy et al., 1995). These factors, in addition to the laboratory procedures (Gordon, 2003) are the key determinants for the success of IVEP.

Results from previous in-vivo studies with cattle indicated the conception rates were less when there were relatively lesser P4 plasma concentrations during the growth phase of the follicle from which ovulation occurred in dairy cows (Pursley and Martins, 2011). It is now well established that the lesser conception rate is due to lesser concentrations of P4 that primarily alter the follicular development, leading to the oocytes that are released with ovulation having abnormalities, and resulting in the impaired early embryonic development (Mihm et al., 1994; Ahmad et al., 1995). The presence of greater plasma P4 concentrations was also associated with more than a two-fold increase in blastocyst size in recipient cows (Lonergan et al., 2007). Results of in-vitro studies indicate the presence of a CL at the time of oocyte collections is not only associated with an enhanced oocyte quality, but also an enhanced developmental competence of oocytes in Bos taurus cows (Pirestani et al., 2011). These results, however, are inconsistent with the results from other studies (Hajarian et al., 2016). In these studies estrous cyclic or acyclic status of cows at the time of oocyte collection was not considered when categorizing the treatment groups. This perhaps confounded the results from these previous studies where this variable was not considered (Neglia et al., 2003; Sugulle et al., 2008; Penitente et al., 2015). When considering results of these previous studies, it is assumed that recovery, quality and early in vitro developmental competence of oocytes collected from estrous cyclic cattle will be greater than when oocytes are collected from estrous acyclic Bos indicus dairy cows.

Bos indicus cows are known for heat tolerance and tick resistance in tropical and subtropical regions of Southeast of the USA and Asia (Glass et al., 2005; Khan et al., 2008). The reproductive physiology of Bos taurus is quite different than that of Bos indicus cows (Sartori et al., 2010). Bos indicus cows generally have a longer prepubertal period, have prolonged periods of postpartum anestrus, have a tendency for seasonal breeding, and a shorter duration of behavioral estrus with fewer overt signs of estrus (Bó et al., 2003). Most of the research with the ART has been conducted with Bos taurus cattle. Similar information is generally lacking in Bos indicus cows. The primary objective of the present study, therefore, was to determine the effect of plasma P4 at the time of oocyte collection on oocyte recovery rate, oocyte quality, as well as early in-vitro embryo development, and developmental competence of embryos derived from oocytes of Bos indicus dairy cows that were collected when cows were estrous cyclic or acyclic. It was hypothesized that for the oocytes recovered from the estrous cyclic cows there will be a greater recovery rate, oocyte quality, as well as an early in-vitro development, and developmental competence of embryos derived from oocytes of these cows compared with those from estrous acyclic Bos indicus dairy cows.

Section snippets

Materials and methods

This study was conducted from December 2017 to April 2018 in embryology laboratory of Central Laboratory Complex of University of Veterinary and Animal Sciences, Ravi Campus, Pattoki. The experiments were performed using ready-made commercially available IVF media (Minitüb GmbH, Germany) and reagents of Sigma Chemical Company (St. Louis, MO, USA).

Results

The data for effect of CL on the serum P4 concentrations between estrous CYCLIC and ACYCLIC Bos indicus cows are presented in Table 1. Results indicate that the mean serum P4 concentrations (4.21 ± 0.4 ng/ml compared with 0.5 ± 0.2 ng/ml; P < 0.05) were greater for estrous CYCLIC as compared with ACYCLIC cows, respectively. Data for the effect of plasma P4 on the number of oocytes recovered per ovary are depicted in Fig. 1. The mean number of oocytes recovered per ovary (6.5 ± 0.5 compared with

Discussion

To the best of our knowledge, this is the first study in which there were determinations of the effect of plasma P4 on the oocyte recovery rate, oocyte quality, and early IVEP outcomes when oocytes were derived from estrous CYCLIC and ACYCLIC Bos indicus dairy cows. It was hypothesized that with oocyte recovery from ovaries of estrous cyclic (greater P4) cows there would be a greater recovery rate, oocyte quality, and early in-vitro developmental competence of embryos when oocytes were derived

Conflict of interest statement

The authors intend to submit manuscript entitled as “Effect of plasma progesterone on oocyte recovery, oocyte quality, and early in-vitro developmental competence of embryos in Bos indicus dairy cows” in Animal Reproduction Science and have no conflicts of interest.

Acknowledgments

This research was financially supported by NRPU project of Higher Education Commission (HEC), Islamabad, Pakistan. The authors are grateful to PAMCO (Punjab Agriculture & Meat Company) provision of ovaries. We gratefully acknowledge Dr. Naeem Iqbal, Head Section ART Lab/Sr. Clinical Scientist, King Faisal Specialist Hospital & Research Center, Jeddah, Kingdom of Saudi Arabia for providing constant help throughout the study. The authors are thankful to Mr. Muhammad Bilal for providing the

References (56)

  • M. Green et al.

    Relationships between maternal hormone secretion and embryo development on day 5 of pregnancy in dairy cows

    Anim. Reprod. Sci.

    (2005)
  • H. Hajarian et al.

    The presence of corpus luteum may have a negative impact on in vitro developmental competency of bovine oocytes

    Reprod. Biol.

    (2016)
  • B. Manjunatha et al.

    Selection of developmentally competent buffalo oocytes by brilliant cresyl blue staining before IVM

    Theriogenology

    (2007)
  • T. McEvoy et al.

    Dietary-induced suppression of pre-ovulatory progesterone concentrations in superovulated ewes impairs the subsequent in vivo and in vitro development of their ova

    Anim. Reprod. Sci.

    (1995)
  • S. Moore et al.

    A 100-year review: reproductive technologies in dairy science

    J. Dairy Sci.

    (2017)
  • J. Moreno et al.

    Influence of pregnancy and presence of a CL on quantity and quality of bovine oocytes obtained from ovarian follicles aspirated post-mortem

    Theriogenology

    (1993)
  • G. Neglia et al.

    Bovine and buffalo in vitro embryo production using oocytes derived from abattoir ovaries or collected by transvaginal follicle aspiration

    Theriogenology

    (2003)
  • J. Parrish et al.

    Effect of bovine sperm separation by either swim-up or Percoll method on success of in vitro fertilization and early embryonic development

    Theriogenology

    (1995)
  • L. Pfeifer et al.

    Effects of low versus physiologic plasma progesterone concentrations on ovarian follicular development and fertility in beef cattle

    Theriogenology

    (2009)
  • G. Purohit et al.

    Influence of epidermal growth factor and insulin-like growth factor 1 on nuclear maturation and fertilization of buffalo cumulus oocyte complexes in serum free media and their subsequent development in vitro

    Anim. Reprod. Sci.

    (2005)
  • M. Salhab et al.

    Kinetics of gene expression and signaling in bovine cumulus cells throughout IVM in different mediums in relation to oocyte developmental competence, cumulus apoptosis and progesterone secretion

    Theriogenology

    (2011)
  • A. Shaham-Albalancy et al.

    Delayed effect of progesterone on endometrial morphology in dairy cows

    Anim. Reprod. Sci.

    (1997)
  • S. Snijders et al.

    Effect of genetic merit, milk yield, body condition and lactation number on in vitro oocyte development in dairy cows

    Theriogenology

    (2000)
  • S. Snijders et al.

    Effect of genetic merit, milk yield, body condition and lactation number on in vitro oocyte development in dairy cows

    Theriogenology

    (2000)
  • D. Wolfenson et al.

    Impaired reproduction in heat-stressed cattle: basic and applied aspects

    Anim. Reprod. Sci.

    (2000)
  • N. Ahmad et al.

    Effect of persistent follicles on early embryonic losses in beef cows

    Biol. Reprod.

    (1995)
  • A. De Wit et al.

    Effect of ovarian phase and follicle quality on morphology and developmental capacity of the bovine cumulus-oocyte complex

    J. Anim. Sci.

    (2000)
  • T. Fair et al.

    The role of progesterone in oocyte acquisition of developmental competence

    Reprod. Domest. Anim.

    (2012)
  • Cited by (0)

    View full text