Follicular-phase concentrations of progesterone, estradiol-17β, LH, FSH, and a PGF2α metabolite and daily clustering of prolactin pulses, based on hourly blood sampling and hourly detection of ovulation in heifers

doi:10.1016/j.theriogenology.2012.12.015

Theriogenology

Volume 79, Issue 6, 1 April 2013, Pages 918-928

https://doi.org/10.1016/j.theriogenology.2012.12.015 Get rights and content

Abstract

Circulating concentrations of hormones were determined each hour in 13 heifers from the end of the luteolytic period to ovulation (follicular phase, 3.5 days). Diameter of the preovulatory follicle was determined every 8 hours, and the time of ovulation was determined hourly. The diameter of the preovulatory follicle decreased 0.8 ± 0.1 mm/h in heifers when there was 1 to 3 hours between the last two diameter measurements before ovulation. The concentration of progesterone (P4) after the end of the luteolytic period (P4 < 1 ng/mL) changed (P < 0.0001), as shown by a continued decrease until Hour −57 (Hour 0 = ovulation), then was maintained at approximately 0.2 ng/mL until 2 hours before the peak of the LH surge at Hour −26, and then a decrease to 0.1 ng/mL along with a decrease in estradiol-17β. Concentrations of LH gradually increased (P < 0.007) and concentrations of FSH gradually decreased (P < 0.0001) after the end of luteolysis until the beginning nadirs of the respective preovulatory surges. A cluster of prolactin (PRL) pulses occurred (P < 0.0001) each day with approximately 24 hours between the maximum value of successive clusters. Hourly concentrations of a PGF_2α metabolite decreased (P < 0.007) until Hour −40, but did not differ among hours thereafter. Novel observations included the gradual increase in LH and decrease in FSH until the beginning of the preovulatory surges and follicle diameter decrease a few hours before ovulation. Results supported the following hypotheses: (1) change in the low circulating P4 concentrations during the follicular phase are temporally associated with change in LH concentrations; and (2) PRL pulses occur in a cluster each day during the follicular phase of the estrous cycle.

Introduction

Folliculogenesis and follicular waves [1], luteal periods [2], and events within the preovulatory follicle [3] have been reviewed. The luteolytic period in the absence of pregnancy has been studied extensively, because of the pivotal role of the corpus luteum (CL) in controlling the length of the estrous cycle. The term luteolysis refers to the entire luteolytic period and is characterized by decreasing progesterone (P4) concentrations. Luteolysis begins on a mean of 17 days after ovulation in heifers [4]. Based on hourly sampling, luteolysis encompasses 24 hours and extends from the transition between preluteolysis and luteolysis to the end of luteolysis. For standardization among laboratories, the beginning of postluteolysis is commonly defined as the first P4 concentration that reaches <1 ng/mL [5]. The period of postluteolysis can also be called the follicular phase in cattle.

A previous study of hormone and follicle interrelationships that encompassed ovulation used blood sampling every hour [6]. However, determination of the time of ovulation was done every 6 hours, thereby weakening the interpretation of temporal relationships between the changes in hormone concentrations and the time of ovulation. The initial portion of the postluteolytic period was not included in the reported study, and P4, PRL, and PGFM were not considered.

Although the synchrony of the preovulatory LH and FSH surges is known [6], it has not been determined adequately if the preovulatory surges are temporally associated with changes in circulating concentrations of P4, PRL, and a PGF_2α metabolite (PGFM). Observations in individual cows have indicated that basal concentrations of P4 before the LH surge seemed similar to the observed concentrations after the surge [7]. Concentration of P4 in the vena cava increased and decreased concomitantly with the LH surge in four of five cows, but the increase was not detected in the jugular vein. Although a positive effect of LH on P4 has been demonstrated during the luteal phase [8], the relationship between LH and changes in the low concentrations of P4 (<1 ng/mL) throughout the follicular phase has not been reported.

The preovulatory FSH surge in cattle is followed immediately by a distinct periovulatory FSH surge, which gives origin to the first follicular wave of the estrous cycle [6]. The preovulatory and periovulatory FSH surges are separated by a common nadir that ends the preovulatory surge and begins the periovulatory surge.

The characteristics and rhythmicity of PRL pulses have been described in heifers extending from 12 hours before the beginning of luteolysis to 36 hours after the end of luteolysis [9]. Individual pulses have a mean nadir-to-nadir interval of approximately 4 hours. The interval between pulses is minimal as indicated by the occurrence of the ending nadir of a pulse at the same hour as the beginning nadir of the next pulse in most (86%) pairs of adjacent pulses. In a recent study, preovulatory clusters of PRL pulses occurred in a circadian rhythm [10]. The maximal concentration in the cluster (pulse with greatest peak) usually (82%) occurred from 11 AM to 1 PM. However, the PRL clustering phenomenon has not been adequately described and has not been characterized for each day of the follicular phase.

The current study in heifers used 1-hour intervals for blood sampling from the end of luteolysis to 8 hours after ovulation. Ovulation was also detected hourly. The goal was to characterize hormone concentrations during the follicular phase to find previously unknown temporal associations that would provide a rationale for development of hypotheses for future studies. Specific hypotheses were: (1) changes in the low circulating P4 concentrations during the follicular phase are temporally associated with changes in LH concentrations; and (2) PRL pulses occur in a cluster each day during the follicular phase.

Section snippets

Heifers

Holstein dairy heifers (N = 13) aged 18 to 24 months and weighing 450 to 580 kg were used during July in the northern temperate zone. Only natural estrous cycles were used without induced luteolysis, induced ovulation, or synchronization of the time of estrus or ovulation. Heifers were selected that had docile temperament and no apparent abnormalities of the reproductive tract, as determined by transrectal ultrasonic examinations [11]. The heifers were kept under natural light in an open

Results

Data for six to 10 heifers were available from Hours −85 to −55 and thereafter for each of the 13 heifers, because of variation among animals in the length of the interval from the first blood sample to ovulation. The P4 concentration at Hour −85 was 0.98 ng/mL and represented the beginning of postluteolysis or the follicular phase. Diameter of the future ovulatory follicle at 8-hour intervals increased (P < 0.0001) at a mean rate of 0.56 ± 0.04 mm per 8 hours during Hours −85 to −29 (Hour 0 =

Follicle and E2

The length of the interovulatory interval, CL area (cm²), growth rate and maximum diameter of the ovulatory follicle [14], [27], and cessation of growth of the ovulatory follicle 24 hours before ovulation [28], [29] were similar to reported results. Based on hourly ovulation detection and blood sampling, the peaks of the LH and FSH preovulatory surges occurred 26 hours before ovulation, and E2 and P4 began to decrease 2 hours before the LH and FSH peaks. That is, the cessation of the follicle

Acknowledgments

This research was supported by the Eutheria Foundation, Cross Plains, WI, USA (Project B2-OJ-11). The authors thank M.M. Hoffman for assistance in data handling, manuscript processing, and figure preparation.

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Research articleFollicular-phase concentrations of progesterone, estradiol-17β, LH, FSH, and a PGF2α metabolite and daily clustering of prolactin pulses, based on hourly blood sampling and hourly detection of ovulation in heifers

Abstract

Introduction

Section snippets

Heifers

Results

Follicle and E2

Acknowledgments

Theriogenology

Theriogenology

Anim Reprod Sci

Anim Reprod Sci

Theriogenology

Theriogenology

Theriogenology

Theriogenology

Theriogenology

Theriogenology

Theriogenology

Anim Reprod Sci

Anim Reprod Sci

Steroids

Anim Reprod Sci

Anim Reprod Sci

Anim Reprod Sci

Theriogenology

Domest Anim Endocrinol

Adv Drug Deliv Rev

Dynamics of circulating progesterone concentrations before and during luteolysis: a comparison between cattle and horses

Biol Reprod

The periovulatory period in cattle: progesterone, prostaglandins, oxytocin and ADAMTS proteases

Anim Reprod

Research article
Follicular-phase concentrations of progesterone, estradiol-17β, LH, FSH, and a PGF_2α metabolite and daily clustering of prolactin pulses, based on hourly blood sampling and hourly detection of ovulation in heifers