J. Anim Sci.
HOME HELP FEEDBACK SUBSCRIPTIONS ARCHIVE SEARCH TABLE OF CONTENTS
QUICK SEARCH:   [advanced]


     

J. Anim Sci. 2007. 85:937-943. doi:10.2527/jas.2006-592
© 2007 American Society of Animal Science
This Article
Right arrow Abstract Freely available
Right arrow Full Text (PDF)
Right arrow All Versions of this Article:
jas.2006-592v1
85/4/937    most recent
Right arrow Alert me when this article is cited
Right arrow Alert me if a correction is posted
Services
Right arrow Similar articles in this journal
Right arrow Similar articles in PubMed
Right arrow Alert me to new issues of the journal
Right arrow Download to citation manager
Right arrow reprints & permissions
Citing Articles
Right arrow Citing Articles via Google Scholar
Google Scholar
Right arrow Articles by Mussard, M. L.
Right arrow Articles by Day, M. L.
Right arrow Search for Related Content
PubMed
Right arrow PubMed Citation
Right arrow Articles by Mussard, M. L.
Right arrow Articles by Day, M. L.

ANIMAL GROWTH, PHYSIOLOGY, AND REPRODUCTION

Influence of premature induction of a luteinizing hormone surge with gonadotropin-releasing hormone on ovulation, luteal function, and fertility in cattle1

M. L. Mussard, C. R. Burke2, E. J. Behlke3, C. L. Gasser4 and M. L. Day5

Department of Animal Sciences, The Ohio State University, Columbus 43210-1095


   Abstract
Top
 Abstract
INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 LITERATURE CITED
 
We tested the hypothesis that luteal function and fertility would be reduced in cattle induced to ovulate prematurely compared with those ovulating spontaneously. Estrus was synchronized in 56 beef cows (24 that were nonlactating and 32 that were nursing calves). At 6.4 ± 0.1 d after estrus, all follicles ≥5 mm were aspirated (day of aspiration = d 0) with a 17-gauge needle using the ultrasound-guided transvaginal approach. On d 1.5 and 2, cows were administered 2 luteolytic doses of PGF2{alpha}. Ovarian structures were monitored by transrectal ultrasonography from d –2 to 12, or ovulation. Emergence of a new follicular wave occurred on d 1.7 ± 0.1. When the largest follicle of the newly emerged wave was 10 mm in diameter (d 4.8 ± 0.1), cows were assigned on an alternating basis to receive 100 µg of GnRH (GnRH-10; n = 29) to induce ovulation or, upon detection of spontaneous estrus, to the spontaneous (SPON) treatment (n = 24). Cows were bred by AI at 12 h after GnRH (GnRH-10) or 12 h after the onset of estrus (SPON) as detected using an electronic surveillance system. Blood samples were collected every other day beginning 2 d after ovulation until pregnancy diagnosis 30 d after AI. Ovulation and AI occurred in 29/29 cows in the GnRH-10 and in 24/24 cows in the SPON treatment. Ovulation occurred later (P < 0.05) in the SPON (d 7.7 ± 0.1) than GnRH-10 (d 6.8 ± 0.1) treatment. Double ovulations were detected in 47% of cows, resulting in 1.5 ± 0.1 ovulations per cow. Diameters of the ovulatory and the second ovulatory (in cows with 2 ovulations) follicles were greater (P < 0.05) in the SPON (12.0 ± 0.3 mm and 10.5 ± 0.4 mm, respectively) than in the GnRH-10 (10.7 ± 0.1 mm and 9.2 ± 0.3 mm) treatment. Cross-sectional areas of luteal tissue and plasma concentrations of progesterone during the midluteal phase were greater (P < 0.05) in the SPON (3.62 ± 0.2 cm2 and 6.4 ± 0.3 ng/mL) than in the GnRH-10 (3.0 ± 0.2 cm2 and 5.4 ± 0.2 ng/mL) treatment. The conception rate to AI in the SPON (100%) treatment was greater (P < 0.05) than in the GnRH-10 (76%) treatment. The animal model used in this study resulted in unusually high conception rates and double ovulations. In conclusion, premature induction of the LH surge reduced the diameter of ovulatory follicle(s), the luteal function, and the conception rate to AI.

Key Words: cattle • corpus luteum • fertility • ovarian follicle


   INTRODUCTION
Top
 Abstract
 INTRODUCTION
MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 LITERATURE CITED
 
Estrous synchronization regimens designed such that all female cattle are bred by AI at a fixed time (timed AI), regardless of spontaneous estrus, are used in beef and dairy cattle production to circumvent the challenges associated with detection of estrus or to permit handling of animals in groups rather than as individuals, or both. Commonly used timed-AI protocols include the Ovsynch (Pursley et al., 1998Go) and CO-Synch (Geary et al., 1998Go) programs. These synchronization programs use GnRH and PGF2{alpha} to sequentially control ovarian follicular dynamics, luteolysis, and ovulation.

The intent of the initial treatment with GnRH, given 7 d before injection of PGF2{alpha}, is to induce ovulation and reset follicular growth, leading to the synchronized development of mature dominant follicles that are induced to ovulate by a second GnRH injection given 2 to 3 d after PGF2{alpha}. However, the initial GnRH injection has been reported to reset follicular growth in only 66% of beef (Geary et al., 2000Go) and 64% of dairy (Vasconcelos et al., 1999Go) cows, and the variation in follicular size when the second GnRH treatment is given has been characterized (Perry et al., 2002Go).

The lack of precision in resetting follicular waves with GnRH will inevitably alter the age and diameter of the preovulatory follicle at the time of synchronized ovulation and timed AI, resulting in ovulatory follicles of varying maturity. Determination of the impact on fertility of variation in the maturity of follicles at the time of synchronized ovulation is critical when modifying timed AI programs to optimize the conception rate. The mechanisms by which follicular maturity at ovulation influences fertility are of primary interest.

The objective of the current study was to test our working hypothesis, that luteal function and conception rate would be reduced when follicles that had not reached full maturity were induced to ovulate, compared with cows that spontaneously exhibited estrus and had ovulated.


   MATERIALS AND METHODS
Top
 Abstract
 INTRODUCTION
 MATERIALS AND METHODS
RESULTS
 DISCUSSION
 LITERATURE CITED
 
Animals and Treatments
All animals were handled in accordance with procedures approved by The Ohio State University Agricultural Animal Care and Use Committee.

Multiparous Angus and Angus x Simmental cows, either nursing calves (n = 32) or nonlactating (n = 24), were enrolled in the study. Cows were 4.6 ± 0.2 yr of age, with all cows having at least 1 prior calf. Animals that were suckling calves were 74.3 ± 4.3 d postpartum. Animals were fed mixed grass hay ad libitum throughout the experiment. Estrus was synchronized in all cows with 2 injections of PGF2{alpha} (Lutalyse, 25 mg of dinoprost tromethamine per injection; Pfizer Animal Health, New York, NY) separated by 11 d. At 6.4 ± 0.1 d after synchronized estrus, all ovarian follicles ≥5 mm in diameter were aspirated (d 0 of the experiment) with a 17-gauge needle by using the ultrasonography-guided transvaginal approach (Bergfelt et al., 1994Go) with a 5-MHz convex array transducer (Aloka 500V, Corometrics Inc., Wall-ingford, CT). After follicular aspiration, injections of PGF2{alpha} (Lutalyse, 25 mg each) were administered on d 1.5 and 2 to induce luteolysis.

The location and diameter of all ovarian follicles ≥5 mm in diameter were monitored daily from d –2 until detection of ovulation by transrectal ultrasonography using a 7.5-MHz linear array transducer attached to the Aloka 500V. When the largest follicle of the new cohort of follicles that emerged after aspiration was determined to be ≥10 mm in diameter, cows were alternately assigned, within lactation status, to receive GnRH (100 µg, Cystorelin, Merial, Inselin, NJ) at that time (GnRH-10, n = 29) or no treatment (n = 27). All untreated cows that exhibited a spontaneous estrus (n = 24) were assigned to the spontaneous (SPON) treatment. The day of ovulation was defined as the first day on which the preovulatory follicle was no longer visible. The diameter of the corpus luteum (CL) was determined 12 d after ovulation, and the cross-sectional area of the CL was also determined at this time using the ellipse function of the Aloka 500V instrument. In cows with 2 CL, the cross-sectional area was calculated as the sum of the area for the 2 CL.

Estrous Detection, AI, and Pregnancy Diagnosis
Estrus was monitored with the Heatwatch estrous detection system (CowChips LLC, Denver, CO) in both treatments. Onset of estrus was defined as the first time that an animal was recorded to have been mounted by herdmates at least 3 times within a 4-h period. Artificial insemination was performed 12 h after the onset of estrus in the SPON treatment and 12 h after the GnRH injection in the GnRH treatment. A single experienced technician performed AI with semen from 3 bulls, which was used equally across treatments. Pregnancy diagnosis was performed at 30 and 60 d after AI using a 7.5-MHz linear array transducer (Aloka). Additionally, at 60 d after AI the number of fetuses present was determined for cows with double ovulations.

Determination of Progesterone Concentrations
Blood samples were collected every other day from d 2 to 30 after ovulation to quantify progesterone concentrations. Blood was collected from a coccygeal vessel into tubes containing an anticoagulant (EDTA) and was centrifuged at 1,500 x g for 15 min within 1 h after collection. Plasma was stored at –20°C until progesterone concentrations were determined using a commercially available RIA kit (Coat-a-Count, Diagnostic Products Corporation, Los Angeles, CA), as described previously for our laboratory (Burke et al., 2003Go). All samples from an individual cow were included in a single assay, and each assay had equal numbers of cows from both treatments. The average intraassay CV was 2.6%, and the interassay CV (2 assays) for pooled plasma samples containing 1.5 and 7.5 ng/mL were 18.2 and 14.9%, respectively. The average sensitivity of the assays was 0.2 ng/mL.

Statistical Analyses
The effects of treatment, time, and the treatment x time interaction on concentrations of progesterone were analyzed by ANOVA using the MIXED procedure of SAS (SAS Inst. Inc., Cary, NC), accounting for repeated measures. The model was Yijk = µ + Ti + cj:i + Hk + (TH)ik + eijk, where Yijk is the observation of the jth cow in the ith treatment at the kth time, µ is the overall mean, Ti is the ith treatment, cj:i is the random effect of the jth cow within the ith treatment (cj:i ~ N[0, Formula]), Hk is the kth time, (TH)ik is the treatment x time interaction term, and eijk is the residual effect (eijk ~ N[0,{sum}], where {sum} is the variance-covariance of the residual errors with a first-order autoregressive structure for repeated measures within cows).

The lactation status of cows and the interaction with treatment were tested in the initial analyses of all data. This interaction was not significant in any analyses; therefore, the interaction term for lactation status x treatment was removed from the final analyses. The effects of treatment on the interval from follicle emergence to ovulation and follicle diameter at ovulation were analyzed using the MIXED procedure of SAS (Yij = µ + Ti + eij, with the notations defined above). The effect of treatment on pregnancy rate and incidence of double ovulation was tested using Fisher’s exact test (PROC FREQ in SAS). Data are expressed as means ± SEM.


   RESULTS
Top
 Abstract
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
DISCUSSION
 LITERATURE CITED
 
Aspiration of ovarian follicles was performed 6.4 ± 0.1 d after the synchronized estrus (d 0). Emergence of a new wave of follicular development was detected on d 1.7 ± 0.1, and the largest follicle of this cohort attained a diameter of 10 mm on d 4.8 ± 0.1. Three cows that were eligible to be assigned to the SPON treatment were not detected in estrus and were not used in the experiment, resulting in 29 cows in the GnRH-10 treatment and 24 females in the SPON treatment. No cows in the GnRH-10 treatment were detected in estrus before or at the time of the GnRH injection.

The interval from follicle aspiration to injection of GnRH in the GnRH-10 treatment was 4.8 ± 0.1 d, and the interval to the onset of estrus in the SPON treatment was 6.2 ± 0.2 d. Thus, the intervals from PGF2{alpha} injection to the preovulatory LH surge were approximated as 3.3 and 4.7 d in the GnRH-10 and SPON treatments, respectively. The day of ovulation and the diameter of the largest follicle (F1) that ovulated were less (P < 0.05) in the GnRH-10 than in the SPON treatment (Table 1Go). The incidence of double ovulations was 41% in the GnRH-10 and 54% in the SPON treatment and did not differ between treatments. The diameter of the second ovulatory follicle (F2) in cows with double ovulations was also smaller (P < 0.05) in the GnRH-10 than in the SPON treatment (Table 1Go).


View this table:
[in this window]
[in a new window]

  		Table 1. Timing of ovulation, characteristics of ovulatory follicles, and conception rate in cows induced to ovulate follicles of approximately 10 mm in diameter with GnRH (GnRH-10) or in cows that ovulated spontaneously (SPON)
 
A treatment x day interaction was detected (P < 0.05) for concentrations of progesterone from d 2 to 16 after ovulation when all cows (pregnant and not pregnant) were included in the analyses. The interaction was largely due to greater concentrations of progesterone in the SPON than in the GnRH-10 treatment from d 8 to 16 after ovulation (Figure 1Go). Consistent with the observation of greater concentrations of progesterone during the midluteal phase, the cross-sectional area of the CL was greater (P < 0.05) in the SPON (3.6 ± 0.2 cm2) than in the GnRH-10 (3.0 ± 0.2 cm2) treatment on d 12 after ovulation. A second analysis of progesterone concentrations that included only pregnant cows and observations through d 30 after ovulation (Figure 2Go) indicated that greater (P < 0.05) concentrations of progesterone in the SPON treatment were maintained through d 24 after ovulation (treatment x day, P < 0.05). The cross-sectional area of the CL did not differ when nonpregnant cows were excluded from this comparison (SPON 3.6 ± 0.2; GnRH-10; 3.3 ± 0.2). Across treatments, cows with 2 CL had greater (P < 0.05) concentrations of circulating progesterone (Figure 3Go; group x day, P < 0.05) and total cross-sectional areas of the CL 12 d after ovulation than did cows with a single CL (2 CL, 4.2 ± 0.2 cm2; 1 CL, 2.7 ± 0.1 cm2; P < 0.05).


Figure 1
View larger version (10K):
[in this window]
[in a new window]

  		Figure 1. Circulating concentrations of progesterone in cows induced to ovulate follicles of approximately 10 mm in diameter with GnRH (GnRH-10) or in cows that ovulated spontaneously (SPON) after a PGF2{alpha}-induced luteal regression that occurred 1.5 d after follicular aspiration. Day 0 represents the day of ovulation [treatment x time, P < 0.05; an asterisk (*) indicates that means within time differ, P < 0.05].

 

Figure 2
View larger version (13K):
[in this window]
[in a new window]

  		Figure 2. Circulating concentrations of progesterone in cows induced to ovulate follicles of approximately 10 mm in diameter with GnRH (GnRH-10) or in cows that ovulated spontaneously (SPON) and that were pregnant 30 d after AI either 12 h after GnRH (GnRH-10) or 12 h after detection of estrus (SPON). Concentrations of progesterone in cows from the GnRH-10 treatment that were not pregnant 30 d after AI (not pregnant; n = 7) are included for illustrative purposes. Day 0 represents the day of ovulation. A treatment x time interaction (P < 0.05; pregnant cows in the GnRH-10 and SPON treatment) was detected [an asterisk (*) indicates that means within time differed between treatments, P < 0.05].

 

Figure 3
View larger version (11K):
[in this window]
[in a new window]

  		Figure 3. Circulating concentrations of progesterone in cows with either 1 corpus luteum (CL) or 2 CL. Cows across the GnRH and spontaneous ovulation treatments were grouped according to the number of CL. Day 0 represents the day of ovulation [treatment x group, P < 0.05; an asterisk (*) indicates that means within time differ, P < 0.05].

 
The proportion of cows that were pregnant 30 d after AI was 24% smaller (P < 0.05) in the GnRH-10 than in the SPON treatment (Table 1Go). All cows in the GnRH-10 treatment that were pregnant on d 30 were pregnant on d 60, whereas pregnancies were lost in 3 cows in the SPON treatment between the d 30 and d 60 pregnancy diagnoses.

In cows with double ovulations, 11 of 12 cows in the GnRH-10 treatment and 13 of 13 cows in the SPON treatment were pregnant on d 30. In cows with a single ovulation, the conception rate on d 30 was 65% (11/17) in the GnRH-10 and 100% (11/11) in the SPON treatment. Accordingly, the conception rate was greater (P < 0.05) for cows ovulating 2 follicles (96%) than those ovulating a single follicle (79%). Two fetuses were detected at 60 d after AI in 50% (6/12) of cows with double ovulations in the GnRH-10 treatment and in 62% (8/13) of females in the SPON treatment; this proportion did not differ between treatments.


   DISCUSSION
Top
 Abstract
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
LITERATURE CITED
 
The current study was designed to compare luteal function and subsequent fertility between cows induced to ovulate immature follicles and those that ovulated spontaneously. Animals that were induced to ovulate immature follicles had lesser concentrations of progesterone during the ensuing luteal phase and early stages of pregnancy. Furthermore, we demonstrated that fertility was reduced when cows were induced to ovulate a less mature dominant follicle compared with cows that ovulated spontaneously.

The differences in follicle maturity were achieved by inducing ovulation in one treatment when follicles were of a smaller diameter than is typical for ovulatory follicles vs. permitting follicles to mature spontaneously and ovulate in the second treatment. Although diameter was used as a benchmark for maturity, the animal model used provided precise control of other aspects of follicular development. First, the origin of all ovulatory follicles was the largest growing follicle(s) of a new follicular wave that emerged in a synchronized endocrine environment after aspiration of follicles at a similar stage of the estrous cycle. Second, the age (days from emergence) of ovulatory follicles was known, in addition to diameter. Third, the interval from PGF2{alpha} injection to the GnRH-induced LH surge or the onset of estrus (referred to hereafter as "duration of proestrus"), and thus the approximate interval from luteal regression to the LH surge, was known.

The immature ovulatory follicles in the GnRH-10 treatment in the current study were smaller by approximately 1.3 mm and were 1.1 d younger than in the SPON treatment, and cows experienced a proestrus period that was shorter by approximately 1.5 d. Follicle diameter at ovulation and the duration of proestrus have been identified in other reports as sources of variation in the conception rate in cattle. Decreased conception rates have been observed in female beef cattle induced to ovulate follicles of a smaller diameter within a CO-Synch synchronization program (Lamb et al., 2001Go; Perry et al., 2005Go). The influence on fertility of the duration of proestrus was evaluated in dairy cows through modification of the interval from PGF2{alpha} to the second GnRH treatment in an Ovsynch program (Peters and Pursley, 2003Go). Those authors demonstrated that the conception rate to timed AI was greater in cows with a 48-h interval from PGF2{alpha} to GnRH than when GnRH was given at the same time as PGF2{alpha}, and that the follicular size and conception rate increased when GnRH was given either 0, 12, 24, or 36 h after PGF2{alpha}. In those reports, the origin, functional status, and age of the follicles that were induced to ovulate and the endocrine status of the animals during the interval from follicle emergence to the onset of proestrus were not standardized among animals.

In the current study, the variables of follicular development and endocrine environment were closely controlled; however, it is important to reiterate that follicle age and diameter and the duration of proestrus were varied between treatments. Although follicle maturity has traditionally been defined by the size of the follicle, the results of the current study, taken together with the reports cited above, suggest that follicle maturity is more complex and may be the result of an interaction of several inputs. For example, Perry et al. (2005)Go reported that GnRH-induced ovulation of follicles that were ≤11 mm in size resulted in low pregnancy rates (18 to 29%) and a high rate of embryonic mortality (39%) between approximately 27 and 68 d after AI, but animals that spontaneously ovulated follicles of ≤11 mm had fertility and embryonic mortality similar to animals that ovulated larger follicles after AI. In the current study, cows that were induced to ovulate with GnRH when follicles were 10 to 11 mm in diameter had conception rates of 76% (65% in single-ovulating animals) and 0% embryonic mortality between 30 and 60 d postpartum. Questions remain regarding the relative importance of follicle age and diameter, the endocrine environment during development, the duration of proestrus preceding ovulation, and the interactions of these events to influence the maturity of ovulatory follicles and subsequent fertility.

Differences in follicle maturity likely result in differences in fertility by influencing one or more of a variety of physiological processes. Potential points of influence could include preovulatory estradiol concentrations, competence of the oocyte, oviductal function and sperm transport, the uterine environment, and luteal phase progesterone concentrations. Lower concentrations of estradiol were detected in dairy cows induced to ovulate follicles of a smaller diameter (Vasconcelos et al., 2001Go), whereas in beef cows, this response was inconsistent among experiments (Perry et al., 2005Go). Estradiol concentrations were not measured in the present experiment; however, the GnRH-induced LH surge, which induces a rapid decrease in estradiol concentrations, occurred approximately 1.5 d before detection of the onset of estrus. Presumably, this would coincide with attainment of the preovulatory peak in estradiol concentrations. The influences of GnRH-induced ovulation of immature follicles on the competence of the oocyte, oviductal function and sperm transport, and the uterine environment have not been investigated in depth.

In the present experiment, concentrations of progesterone did not differ during the early luteal phase, but were smaller during the midluteal phase and early pregnancy in cows that were induced to ovulate immature follicles. We (Burke et al., 2001Go) and others (Vasconcelos et al., 2001Go) have demonstrated that progesterone concentrations and the cross-sectional area of the CL were reduced in animals that were induced to ovulate prematurely. Others have noted decreased progesterone concentrations with ovulation of smaller follicles (Perry et al., 2005Go); however, this finding has not been consistent across reports (Perry et al., 2002Go; Taponen et al., 2002Go; Peters and Pursley, 2003Go). Maintenance of a functional CL is paramount to maintenance of early pregnancy. Decreased midluteal-phase progesterone concentrations have been detected in nonpregnant vs. pregnant cows (Lukaszewska and Hansel, 1980Go; Mann et al., 1995Go), and others have observed decreased pregnancy rates in cows that experienced a delayed rise in progesterone concentrations during the early luteal phase following insemination (Shelton et al., 1990Go; Mann and Lamming, 2001Go). A physiological minimum for the concentration of progesterone needed to support pregnancy has not been determined (Mann and Lamming, 1999Go). Because the signal in cattle for maternal recognition of pregnancy is provided via interferon-{tau} secretion from the embryo (Anthony et al., 1988Go), and progesterone concentrations and interferon-{tau} secretion by the embryo are highly correlated (Kerbler et al., 1997Go), it is possible that insufficient progesterone concentrations were responsible for the reduced conception rate in cows induced to ovulate immature follicles in the current study. However, further research is necessary to determine whether subtle reductions in progesterone concentrations (approximately 1 ng/mL beginning on d 8 after ovulation in the current study) will decrease conception rates in cows.

The high incidence of double ovulations (47% of all cows) observed in the current study was unexpected. One characteristic of the model used was that the time of luteal regression (d 1.5) coincided with the emergence of a new follicular wave (d 1.7 ± 0.1). Thus, the follicular wave progressed from emergence in an environment that would be characterized by low progesterone concentrations and an increased frequency of LH pulses characteristic of the follicular phase. Because the FSH increase in response to follicle aspiration peaks at approximately 30 h after aspiration (Burke et al., 2003Go), FSH was presumably beginning to decline on d 1.5. The development of codominant follicles occurred more often in the first follicular wave (35%) than in the second follicular wave (4%; Kulick et al., 2001Go), and Bleach et al. (1998)Go reported that cattle with 3 follicular waves during the estrous cycle exhibited more (30%) double ovulations than those with 2 waves (0%). Both studies are consistent with the idea that a high rate of codominance is associated with low peripheral concentrations of progesterone around the time of emergence of a follicular wave. Accordingly, Lane et al. (2005)Go reported that progesterone suppressed the increase in FSH that initiates the first follicular wave in cattle. In other experiments, we have used the same model except that CL regression was initiated 4 d after aspiration (~2.5 d after emergence of a new follicular wave; Mussard et al., 2003Go) or 5 d after aspiration (~3.5 d after emergence; Bailey et al., 2004Go), resulting in 15 and 0% incidences of double ovulation, respectively. Gibbons et al. (1997)Go, using a follicle aspiration model similar to the current study, detected double ovulations in 3 out of 6 heifers when luteal regression was induced approximately 1.5 d after emergence of a follicular wave. Taken together, these reports suggest that as the interval of luteal regression increases relative to emergence of a follicular wave after aspiration, the incidence of double ovulations decreases. The changes in circulating hormone patterns that are associated with luteolysis (i.e., reduced progesterone and increased LH) may have perturbed the normal process of dominant follicle selection. This remains speculative, and studies are ongoing to elucidate the mechanism responsible for the high incidence of double ovulations observed in the current study.

The high incidence of double ovulations likely contributed to the greater than normal conception rates in this experiment, because all but 1 of the 25 cows with 2 ovulations conceived to AI. In 56% of cows with 2 ovulations (14/25), 2 fetuses were present at 60 d after AI. This is noteworthy because the mean diameter of the second follicle that ovulated was 9.2 ± 0.3 mm in the GnRH-10 treatment and 10.5 ± 0.4 mm in the SPON treatment. The finding that over 50% of these "small" follicles were represented as fetuses at 60 d after AI emphasizes the point that if follicle maturity is defined as the capacity of a follicle to result in pregnancy, then diameter, in itself, is a questionable indicator of the maturity of ovulatory follicles.

In conclusion, premature ovulation of a dominant follicle with GnRH reduced the size of the ovulatory follicle(s), reduced fertility, and decreased subsequent luteal function. The underlying mechanisms that may be responsible for this reduction in conception rate include reduced preovulatory estradiol concentrations, incompetence of the oocyte, diminished oviductal function and sperm transport, an improper uterine environment, impaired luteal function, or a combination of these factors. It is possible that one of these represents the key mechanism for reduced conception or, alternatively, that deficiencies in several of these physiological systems may have contributed to a cumulative depression in the conception rate. Systematic studies are required that investigate these potential sources of infertility in isolation.

The practical implication of these findings is that timed AI synchronization programs must be structured in a manner to ensure that physiologically mature follicles are present in the ovary when treatments are administered to synchronize ovulation.


   Footnotes
 
1 Salaries and research support provided by state and federal funds appropriated to the Ohio Agricultural Resource Development Center (OARDC; Manuscript No. 33-06AS). Appreciation is expressed to Dave Grum for assistance provided in data collection and analyses and to Select Sires (Plain City, OH) for financial support of this project. Thanks are also extended to Pfizer Animal Health (New York, NY) for provision of Lutalyse. Back

2 Current address: Dexcel Research Ltd., Private Bag 3221, Hamilton, New Zealand. Back

3 Current address: University of Nebraska, Lincoln, NE 68528. Back

4 Current address: Southern Utah University, 351 W. University Blvd, Cedar City, UT 84720. Back

5 Corresponding author: day.5{at}osu.edu

Received for publication September 1, 2006. Accepted for publication November 22, 2006.


   LITERATURE CITED
Top
 Abstract
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 LITERATURE CITED
 


Anthony, R. V., S. D. Helmer, S. F. Sharif, R. M. Roberts, P. J. Hansen, W. W. Thatcher, and F. W. Bazer. 1988. Synthesis and processing of ovine trophoblast protein-1 and bovine trophoblast protein-1, conceptus secretory proteins involved in the maternal recognition of pregnancy. Endocrinology 123:1274–1280.[Abstract]

Bailey, C. J., C. R. Burke, M. L. Mussard, and M. L. Day. 2004. Double ovulations following induction of luteal regression during ovarian follicular wave emergence in heifers. J. Anim. Sci. 82(Suppl. 2):86. (Abstr.)

Bergfelt, D. R., K. C. Lightfoot, and G. P. Adams. 1994. Ovarian synchronization following ultrasound guided transvaginal follicle ablation in heifers. Theriogenology 42:895–907.[CrossRef][Medline]

Bleach, E. C., I. D. Peiris, T. S. Grewal, D. A. Shepherd, and D. Savva. 1998. Effect of administration of a novel recombinant bovine interferon on length of oestrous cycle in cattle. Res. Vet. Sci. 64:73–77.[CrossRef][Medline]

Burke, C. R., M. L. Mussard, C. L. Gasser, D. E. Grum, and M. L. Day. 2003. Estradiol benzoate delays new follicular wave emergence in a dose-dependent manner after ablation of the dominant ovarian follicle in cattle. Theriogenology 60:647–658.[CrossRef][Medline]

Burke, C. R., M. L. Mussard, D. E. Grum, and M. L. Day. 2001. Effects of maturity of the potential ovulatory follicle on induction of oestrus and ovulation in cattle with oestradiol benzoate. Anim. Reprod. Sci. 66:161–174.[CrossRef][Medline]

Geary, T. W., E. R. Downing, J. E. Bruemmer, and J. C. Whittier. 2000. Ovarian and estrous response of suckled beef cows to the select synch estrous synchronization protocol. Prof. Anim. Sci. 16:1–5.

Geary, T. W., J. C. Whittier, and D. G. Lefever. 1998. Effect of calf removal on pregnancy rates of cows synchronized with the Ovsynch or Co-Synch protocol. J. Anim. Sci. 81(Suppl.1):278. (Abstr.)

Gibbons, J. R., M. C. Wiltbank, and O. J. Ginther. 1997. Functional interrelationships between follicles greater than 4 mm and the follicle-stimulating hormone surge in heifers. Biol. Reprod. 57:1066–1073.[Abstract]

Kerbler, T. L., M. M. Buhr, L. T. Jordan, K. E. Leslie, and J. S. Walton. 1997. Relationship between maternal plasma progesterone concentration and interferon-tau synthesis by the conceptus in cattle. Theriogenology 47:703–714.[CrossRef][Medline]

Kulick, L. J., D. R. Bergfelt, K. Kot, and O. J. Ginther. 2001. Follicle selection in cattle: Follicle deviation and codominance within sequential waves. Biol. Reprod. 65:839–846.[Abstract/Free Full Text]

Lamb, G. C., J. S. Stevenson, D. J. Kesler, H. A. Garverick, D. R. Broan, and B. E. Salfen. 2001. Inclusion of an intravaginal progesterone insert plus GnRH and prostaglandin F2{alpha} for ovulation control in postpartum suckled beef cows. J. Anim. Sci. 79:2253–2259.[Abstract/Free Full Text]

Lane, E. A., V. Padmanabhan, J. F. Roche, and M. A. Crowe. 2005. Alterations in the ability of the bovine pituitary gland to secret gonadotropins in vitro during the first follicle-stimulating hormone increase of the estrous cycle and in response to exogenous steroids. Domest. Anim. Endocrinol. 28:190–201.[CrossRef][Medline]

Lukaszewska, J., and W. Hansel. 1980. Corpus luteum maintenance during early pregnancy in the cow. J. Reprod. Fertil. 59:485–493.[Abstract]

Mann, G. E., and G. E. Lamming. 1999. The influence of progesterone during early pregnancy in cattle. Reprod. Domest. Anim. 34:269–274.

Mann, G. E., and G. E. Lamming. 2001. Relationship between maternal endocrine environment, early embryo development and inhibition of the luteolytic mechanism in cows. Reproduction 121:175–180.[Abstract]

Mann, G. E., G. E. Lamming, and M. D. Fray. 1995. Plasma oestradiol and progesterone during early pregnancy in the cow and the effects of treatment with buserelin. Anim. Reprod. Sci. 37:121–131.

Mussard, M. L., C. R. Burke, C. L. Gasser, E. J. Behlke, K. A. Colliflower, D. E. Grum, and M. L. Day. 2003. Ovulatory response, luteal function and fertility in cattle induced to ovulate dominant follicles of early or late maturity. Biol. Reprod. 68(Suppl. 1):332. (Abstr.)

Perry, G. A., T. W. Geary, M. C. Lucy, and M. F. Smith. 2002. Effect of follicular size at time of GnRH-induced ovulation on luteal function and fertility. J. Anim. Sci. 80(Suppl. 2):114. (Abstr.)

Perry, G. A., M. F. Smith, M. C. Lucy, J. A. Green, T. E. Parks, M. D. MacNeil, A. J. Roberts, and T. W. Geary. 2005. Relationship between follicular size at insemination and pregnancy success. Proc. Natl. Acad. Sci. USA 102:5268–5273.[Abstract/Free Full Text]

Peters, M. W., and J. R. Pursley. 2003. Timing of final GnRH and the Ovsynch protocol affects ovulatory follicular size, subsequent luteal function, and fertility in dairy cows. Theriogenology 60:1197–1204.[CrossRef][Medline]

Pursley, J. R., R. W. Silcox, and M. C. Wiltbank. 1998. Effect of time of artificial insemination on pregnancy rates, calving rates, pregnancy loss, and gender ratio after synchronization of ovulation in lactating dairy cows. J. Dairy Sci. 81:2139–2144.[Abstract]

Shelton, K., M. F. Gayerie de Abreu, M. G. Hunter, T. J. Parkinson, and G. E. Lamming. 1990. Luteal inadequacy during the early luteal phase of subfertile cows. J. Reprod. Fertil. 90:1–10.[Abstract]

Taponen, J., M. Kulcsar, T. Katila, L. Katai, G. Huzenicza, and H. Rodriguez-Martinez. 2002. Short estrous cycles and estrous signs after premature ovulations induced with cloprostenol and gonadotropin-releasing hormone in cycling dairy cows. Theriogenology 58:1291–1302.[CrossRef][Medline]

Vasconcelos, J. L., R. Sartori, H. N. Oliveira, J. G. Guenther, and M. C. Wiltbank. 2001. Reduction in size of the ovulatory follicle reduces subsequent luteal size and pregnancy rate. Theriogenology 56:307–314.[CrossRef][Medline]

Vasconcelos, J. L., R. W. Silcox, G. J. Rosa, J. R. Pursley, and M. C. Wiltbank. 1999. Synchronization rate, size of the ovulatory follicle, and pregnancy rate after synchronization of ovulation beginning on different days of the estrous cycle in lactating dairy cows. Theriogenology 52:1067–1078.[CrossRef][Medline]



This Article
Right arrow Abstract Freely available
Right arrow Full Text (PDF)
Right arrow All Versions of this Article:
jas.2006-592v1
85/4/937    most recent
Right arrow Alert me when this article is cited
Right arrow Alert me if a correction is posted
Services
Right arrow Similar articles in this journal
Right arrow Similar articles in PubMed
Right arrow Alert me to new issues of the journal
Right arrow Download to citation manager
Right arrow reprints & permissions
Citing Articles
Right arrow Citing Articles via Google Scholar
Google Scholar
Right arrow Articles by Mussard, M. L.
Right arrow Articles by Day, M. L.
Right arrow Search for Related Content
PubMed
Right arrow PubMed Citation
Right arrow Articles by Mussard, M. L.
Right arrow Articles by Day, M. L.

HOME HELP FEEDBACK SUBSCRIPTIONS ARCHIVE SEARCH TABLE OF CONTENTS