Evidence for quadratic association between serum anti-Müllerian hormone (AMH) concentration and fertility in dairy cows

https://doi.org/10.1016/j.anireprosci.2020.106457Get rights and content

Highlights

  • AMH concentration did not have linear association with reproductive parameters of dairy cows.

  • AMH concentration had quadratic relationship with reproductive performance of dairy cows.

  • Cows with minimal and maximal levels of AMH had inferior fertility than their counterparts with moderate levels of AMH.

Abstract

In cattle, results of some but not other studies indicated there has been an association of circulating anti-Müllerian hormone (AMH) concentration with reproductive variables. Considering the inconsistency in results among previous studies, there was evaluation of associations between circulating AMH and reproductive performance in dairy cows, and to this end, the prevailing data of serum AMH concentration and reproductive variables were used (n = 172). Preliminarily, association of AMH concentration with reproductive indices were analyzed using linear and quadratic models. Subsequently, cows were categorized based on AMH concentrations in four equal quartiles, including cows with the least (Q1; n = 43), moderately lesser (Q2; n = 43), moderately greater (Q3; n = 43) and greatest (Q4; n = 43) AMH concentrations, and reproductive variables were compared among the respective AMH quartiles. Initially, assessments indicated reproductive variables were not linearly associated with serum AMH (P > 0.05); however, for all reproductive variables except days to first breeding service (DFS) there was a quadratic association with serum AMH (P < 0.05). Results from analysis of reproductive performance in various AMH quartiles indicated there was a longer period of DFS for cows in Q3 than Q1 (P < 0.05). First postpartum insemination to conception and calving to conception intervals were shorter for cows in Q3 than Q1 and Q4 (P < 0.05) and for cows in Q2 than Q1 (P < 0.05). In conclusion, results from the present study indicate cows with intermediate AMH concentrations had greater reproductive performance.

Introduction

Anti-Müllerian hormone (AMH) is a dimeric glycoprotein, which belongs to the transforming growth factor β (TGF-β) family of growth and differentiation factors (Cate et al., 1986). During sexual development of the embryo, AMH, which is produced by Sertoli cells in testes of male embryos, has important functions in regression of paramesonephric ducts in the male embryos, whereas in female embryos, absence of AMH would lead to development of paramesonephric ducts to female reproductive organs (Jost, 1947; Josso et al., 1993). With further embryo/fetal development, there would be initiation of AMH secretion from granulosa cells of ovarian follicles in the females of various species including cattle (Takahashi et al., 1986), sheep (Bézard et al., 1987), mice (Ueno et al., 1989; Durlinger et al., 1999) and humans (La Marca and Volpe, 2006). The production of AMH initiates when activation of primordial follicles occurs, with maximal secretions from preantral and small antral follicles and there is a subsequent decrease in secretion from follicles that develop to the antral stage (McGee and Hsueh, 2000; Weenen et al., 2004; Monniaux et al., 2008; Mossa et al., 2017). In terms of functions, AMH inhibits primordial follicle activation and attenuates the stimulatory effect of FSH on follicular growth; therefore, it is believed that AMH contributes to preservation of ovarian primordial follicle reserve pool, and in turn, extension of reproductive lifespan in females by suppressing the early depletion of primordial follicles from the ovarian pool and inhibiting development of activated follicles (Durlinger et al., 1999, 2001; Dewailly et al., 2014; Mossa et al., 2017).

Irrespective of AMH biochemical and biological properties, this hormone has been recognized to be associated with antral follicle count (AFC; Ireland et al., 2008; Rico et al., 2009; Baldrighi et al., 2014; Gobikrushanth et al., 2017), and both of these biological variables are considered as reliable indirect markers for size of ovarian primordial follicle reserve pool in cattle (Ireland et al., 2008; Tenley et al., 2019) and other species including humans (La Marca and Volpe, 2006). The AMH concentration, therefore, has been evaluated to assess effects of various factors on the ovarian primordial follicle reserve pool in different studies (Mossa et al., 2013; Akbarinejad et al., 2017, 2018). Furthermore, considering the relationship between AMH and size of ovarian reserves and the extent of repeatability of AMH concentrations among individuals (Ireland et al., 2008, 2011; Rico et al., 2009, 2011, Ribeiro et al., 2014; Souza et al., 2015; Gobikrushanth et al., 2017), a number of studies have been conducted to evaluate the association of circulating AMH concentration with reproductive performance of cows so as to understand whether a single assessment of circulating AMH could serve as a predictor of fertility in cattle (Ribeiro et al., 2014; Baruselli et al., 2015; Jimenez-Krassel et al., 2015; Gobikrushanth et al., 2018, 2019). Rebeiro et al. (2014) reported that AMH concentration was positively associated with pregnancy rate when cows were inseminated based on observation of spontaneous estrus. Furthermore, Jimenez-Krassel et al. (2015) reported that fewer cows with the least concentration of AMH were pregnant considering all lactation periods and there was a lesser retention in the herd of these cows as a result of culling practices. More recently, Gobikrushanth et al. (2019) reported that there were lesser pregnancy rates of cows with the least plasma AMH concentration. Nevertheless, results of other studies indicate there is no relationship between blood serum/plasma AMH concentrations and reproductive performance in cattle (Baruselli et al., 2015; Gobikrushanth et al., 2018). Considering these inconsistences in results among studies in terms of the association between concentration of circulating AMH and fertility of cows, there was assessment, in a retrospective study, of the associations between serum AMH concentration and reproductive performance in dairy cows using both linear and quadratic statistical models.

Section snippets

Animals

The present study was performed at a commercial Holstein dairy herd, in which voluntary waiting period before the first postpartum insemination was 50 days and cows were inseminated 12 h after detection of standing estrus. Estrus was detected thrice daily by visual observation for at least 30 min each time. All artificial inseminations were conducted by the same technician and pregnancy diagnosis was initiated 40–45 days after AI using trans-rectal palpation methods.

Data

In the present study, there

Association of AMH concentration with reproductive variables

Mean ± SEM, median, minimum and maximum values of serum AMH concentration were 503 ± 26, 365, 46, 2089 pg/mL, respectively (Fig. 1). None of the reproductive variables had linear associations with concentration of AMH (P > 0.05; Table 1). In contrast, there was a quadratic association of FSCR, SPC, RB, FSCI and CCI with AMH concentration (P < 0.05); however, results from the statistical analysis indicated there was no association between values for DFS and serum AMH (P > 0.05; Table 2).

Reproductive performance of cows when AMH values were in different quartiles

Discussion

The results of the present study indicate there is a quadratic association between serum AMH concentration and fertility in dairy cows, indicating that cows with intermediate concentrations of serum AMH, particularly those with moderately greater concentrations of serum AMH, had a greater reproductive performance as compared with cows with either the least or greatest concentrations of serum AMH. Likewise, when there was partitioning of cows in four quartiles based on AMH concentration,

Conclusion

In conclusion, results of the present study indicate cows with intermediate concentrations of AMH had optimal reproductive performance. When there were concentrations of AMH in the least and greatest quartile classifications, fertility of cows with these classifications was less. Indeed, large scale studies with more numbers would allow for elucidation of the optimal range of AMH concentration, which could be used for selections to assist beef and dairy producers to improve reproductive

CRediT authorship contribution statement

V. Akbarinejad: Conceptualization, Data curation, Formal analysis, Writing - original draft, Writing - review & editing. F. Gharagozlou: Conceptualization, Writing - review & editing. M. Vojgani: Conceptualization, Writing - review & editing. A. Ranji: Data curation.

Declaration of Competing Interest

The authors affirm that there is no conflict of interest.

Acknowledgement

The authors would express their gratitude to Mr. A. Nazeri for his kind assistance in data acquisition.

References (54)

  • A.K. McNeel et al.

    Beef heifers with diminished numbers of antral follicles have decreased uterine protein concentrations

    Anim. Reprod. Sci.

    (2017)
  • M.Y. Nawaz et al.

    Genomic heritability and genome-wide association analysis of anti-Müllerian hormone in Holstein dairy heifers

    J. Dairy Sci.

    (2018)
  • A.T. Peter et al.

    Postpartum anestrus in dairy cattle

    Theriogenology

    (2009)
  • E.S. Ribeiro et al.

    Plasma anti-Müllerian hormone in adult dairy cows and associations with fertility

    J. Dairy Sci.

    (2014)
  • A.H. Souza et al.

    Relationship between circulating anti-Müllerian hormone (AMH) and superovulatory response of high-producing dairy cows

    J. Dairy Sci.

    (2015)
  • S.C. Tenley et al.

    Maternal age influences the number of primordial follicles in the ovaries of yearling. Angus heifers

    Anim. Reprod. Sci.

    (2019)
  • J. Baldrighi et al.

    Anti-Müllerian hormone concentration and antral ovarian follicle population in Murrah heifers compared to Holstein and Gyr kept under the same management

    Reprod. Domest. Anim.

    (2014)
  • P.S. Baruselli et al.

    Relationship between follicle population, AMH concentration and fertility in cattle

    Anim. Reprod.

    (2015)
  • J. Bézard et al.

    Immunocytochemical study of anti-Müllerian hormone in sheep ovarian follicles during fetal and post-natal development

    J. Reprod. Fertil.

    (1987)
  • D.S. Burns et al.

    Numbers of antral follicles during follicular waves in cattle: evidence for high variation among animals, very high repeatability in individuals, and an inverse association with serum follicle-stimulating hormone concentrations

    Biol. Reprod.

    (2005)
  • A. Busato et al.

    Body condition scores in dairy cows: associations with metabolic and endocrine changes in healthy dairy cows

    J. Vet. Med. A Physiol. Pathol. Clin. Med.

    (2002)
  • D. Dewailly et al.

    The physiology and clinical utility of anti-Müllerian hormone in women

    Hum. Reprod. Update

    (2014)
  • A. Dumont et al.

    Role of anti-Müllerian hormone in pathophysiology, diagnosis and treatment of polycystic ovary syndrome: a review

    Reprod. Biol. Endocrinol.

    (2015)
  • A.L.L. Durlinger et al.

    Control of primordial follicle recruitment by anti-Müllerian hormone in the mouse ovary

    Endocrinology

    (1999)
  • A.L. Durlinger et al.

    Anti- Müllerian hormone attenuates the effects of FSH on follicle development in the mouse ovary

    Endocrinology

    (2001)
  • P. Filippou et al.

    Is foetal hyperexposure to androgens a cause of PCOS?

    Hum. Reprod. Update

    (2017)
  • J.J. Ireland et al.

    Follicle numbers are highly repeatable within individual animals but are inversely correlated with FSH concentrations and the proportion of good-quality embryos after ovarian stimulation in cattle

    Hum. Reprod.

    (2007)
  • Cited by (14)

    View all citing articles on Scopus
    View full text