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, and progesterone1
* Department of Animal Sciences and Industry, Kansas State University, Manhattan 66506-0201, and
and
Northwest Research and Extension Center, Kansas State University, Colby 67701-0786
2 Correspondence:
Weber Hall 254 (phone: 785-532-1243; fax: 785-532-7059; E-mail:
jstevens{at}oznet.ksu.edu).
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Abstract |
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 Top Abstract IntroductionMaterials and MethodsResultsDiscussionImplicationsLiterature Cited |
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, preceded by progesterone (P4), GnRH, or both, and to examine the variability of estrual characteristics in heifers before first and second AI. Dairy (n = 247) and beef (n = 193) heifers were assigned randomly to each of three treatments: 1) 50 µg of GnRH (injected i.m.) administered on d -7 followed by 25 mg of PGF2 (i.m.) on d -1 (GnRH + PGF; modified Select Synch protocol); 2) placement of an intravaginal progesterone (P4)-releasing insert on d -7, PGF2 on d -1, and insert removal on d 0 (P4+PGF); and 3) 50 µg of GnRH plus a P4 insert on d -7, followed by 25 mg of PGF2 on d -1, and insert removal on d 0 (P4+GnRH+PGF). Characteristics of estrus were examined before first AI and before the next eligible AI (18 to 26 d later), including duration of estrus, number of standing events, and total and individual duration of standing events. In addition, all heifers were checked visually at least twice daily for estrus. Blood samples were collected on d -7, -1, and 0 for determination of P4, and pregnancy status was diagnosed by ultrasonography 27 to 34 d after AI. Rates of detected estrus were less (P < 0.05) in dairy than in beef heifers, and greater (P < 0.05) in heifers treated with P4. Pattern of conception and pregnancy rates among treatments differed between beef and dairy heifers (treatment x group interaction; P < 0.05). In dairy heifers, conception and pregnancy rates were greatest with P4+PGF, followed by P4+GnRH+PGF and GnRH+PGF, respectively. The opposite was observed among treatments in beef heifers. Administration of P4 without the preceding injection of GnRH produced the lowest pregnancy rates in beef heifers. Of the quantified sexual behavioral characteristics during the synchronized estrus, the number of standing events and total duration of standing events were greater (P < 0.01) than those observed during the next eligible estrus before second AI, whereas duration of estrus was unaffected.
Key Words: Beef • Cows • Dairy Heifers • Estrus • Fertility • Progesterone
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Introduction |
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TopAbstractIntroductionMaterials and MethodsResultsDiscussionImplicationsLiterature Cited |
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Estrus can be synchronized by shortening the luteal phase with PGF2 or by artificially extending it with progestins (Odde, 1990; Beal, 1998). Short-term treatment with intravaginal progesterone (P4)-releasing inserts (CIDR-B, InterAg, Hamilton, New Zealand) produced tight synchrony of estrus, but fertility was variable and related to duration of insert treatment (Iwazumi et al., 1994; Xu and Burton, 2000).
The Select Synch protocol (injection of GnRH 7 d before an injection of PGF2) produced estrus detection, conception, and pregnancy rates in beef heifers similar to those achieved after feeding melengestrol acetate for 14 d followed in 17 to 19 d of PGF2 or two injections of PGF2 (Stevenson et al., 1999). Similar pregnancy outcomes were reported for dairy heifers after two injections of PGF2 and the Select Synch protocol (Stevenson et al., 2000). One of the limitations of the Select Synch protocol is the early expression of estrus before PGF2 in <10% of treated females, which can be resolved by addition of a progestin source at the time of GnRH and its removal just prior to PGF2 injection (Stevenson et al., 1997). Further, these inserts, like other progestin-releasing inserts or implants, may substitute for GnRH in their ability to turn over persistent follicles prior to PGF2 (Lucy et al., 1992).
Our objectives were to compare: 1) the ability of P4, GnRH, or both, prior to injection of PGF2 to synchronize estrus; and 2) variability of estrual characteristics in virgin heifers before their first AI and with their next eligible estrus preceding their second AI.
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Materials and Methods |
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TopAbstractIntroductionMaterials and MethodsResultsDiscussionImplicationsLiterature Cited |
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Beef heifers at the Manhattan location (April 2001) were purebred Angus, Hereford, or Simmental. Average age of these heifers was 14 ± 0.1 mo (12 to 15 mo). Crossbred heifers at Hays born to high-percentage Angus dams and sired by Angus, South Devon, and Limousin bulls (April 2001) averaged 13 ± 0.1 mo (11 to 15 mo) of age. Only one beef heifer was <12 mo of age at the initiation of treatments.
Dairy heifers were maintained in dry lots with concrete feed aprons and fed a total mixed diet of chopped prairie or alfalfa hay, corn or milo grain, soybean meal, and minerals and vitamins to exceed NRC (1989) guidelines for growing heifers by 15% for all nutrients. Beef heifers at the Manhattan location were maintained in dry lots and fed prairie or alfalfa hay ad libitum plus a concentrate consisting of milo, protein supplement, vitamins, and minerals to meet or exceed NRC (1996) standards for growing heifers. At the Hays location, heifers were housed as previously described, but were fed a sorghum silage-based diet.
Heifers were assigned randomly (within breed or breed composition and age) to each of three treatments (Figure 1
): 1) 50 µg of GnRH (injected i.m.; Cystorelin, Merial Ltd., Iselin, NJ) administered on d -7 followed by 25 mg of PGF2 (i.m.; Lutalyse, Pharmacia Animal Health, Kalamazoo, MI) on d -1 (GnRH + PGF; modified Select Synch); 2) intravaginal placement of a P4-releasing CIDR-B insert on d -7, and PGF2 on d -1, and insert removal on d 0 (P4+PGF); and 3) 50 µg of GnRH plus a P4 insert on d -7, followed by 25 mg of PGF2 on d -1, and insert removal on d 0 (P4+GnRH+PGF).
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Procedures for Detecting Estrus and Insemination
Number and duration of total standing events, and of each individual standing event, duration of estrus (interval between first and last standing events), and interval from the PGF2 injection to estrus were determined using an electronic estrus-detection system in only dairy heifers (HeatWatch, DDX, Inc., Denver, CO). The detection devices were attached to each Holstein heifer before d -7 and maintained in place until pregnancy was diagnosed. In addition, beginning on d -1, all dairy heifers were observed visually twice daily for signs of estrus. Beef heifers were observed for estrus multiple times daily during daylight hours following injection of PGF2.
All heifers were inseminated between 6 and 18 h after first detected estrus. At each location, AI was performed by two technicians. Pregnancy was diagnosed between 27 and 34 d after insemination by visualization of fluid and/or the embryo using transrectal ultrasonography.
Blood Collection and Radioimmunoassays
Blood samples were collected via puncture of a coccygeal vessel from all heifers (Figure 1
) on d -7, -1, and 0. An additional sample was collected from all dairy heifers on d 1 (no blood was collected from the 16 heifers treated in the last dairy replication). Progesterone was measured in blood sera using a specific, validated radioimmunoassay (Skaggs et al., 1986). The inter- and intraassay coefficients of variation were 11.3 and 8.6%, respectively, for 14 assays.
Statistical Analyses
Rates of detected estrus (number of heifers detected in estrus during 120 h after PGF2), conception (number of pregnant heifers divided by number of heifers inseminated), and pregnancy (number of pregnant heifers after synchronized insemination divided by the number of heifers treated) were calculated. Intervals from injection of PGF2 to visual observation or electronic detection of first standing event were determined.
Characteristics of estrus were calculated as described above for dairy heifers before first AI (synchronized estrus) and at the subsequent postinsemination estrus (18 to 26 d later). Comparisons of these characteristics, with each heifer as her own control within replication, were made using procedure GLM of SAS (SAS Inst. Inc., Cary, NC). Preliminary models that included preinsemination estrus-synchronization treatments detected no significant effects of treatments on estrual characteristics as determined by electronic estrus detection. Therefore, those effects were not considered in the final model, which included estrual characteristics before first or second AI, month of first AI, and their interaction.
Categories of the pubertal status of heifers were created according to the pattern of P4 concentrations in heifers. For this study, puberty was defined by a pattern of P4 concentrations on d -7, -1, and 0. Prepubertal heifers had only low (L; <1 ng/mL) concentrations of P4 on d -7, -1, and 0 (i.e., LLL [n = 18]). Pubertal heifers (were classified further as having absence (<1 ng/mL; LLH [n = 3], HLL [n = 36], or HLH [n = 1]) or presence (
1 ng/mL; LHL [n = 46], LHH [n = 84], HHL [n = 59], and HHH [n = 175]) of elevated blood P4.
Preliminary comparisons of rates of detected estrus, conception, and pregnancy, interval from PGF2 to estrus, and concentrations of P4 were analyzed using a model consisting of treatment, pubertal status, location, and their two-way interactions, using procedures GLM and CATMOD in SAS (SAS Inst. Inc.). No differences were detected between the two beef locations, so they were combined into one group and compared to the dairy heifers in the final model, which included treatment, group (beef vs dairy), pubertal status, and their two-way interactions. Concentrations of P4 on d -1, 0, and 1 were analyzed by MIXED procedure in SAS (1998) using a split-plot model, where treatment was tested by the heifer within treatment variance.
Levene’s test for heterogeneity of variance (Milliken and Johnson, 1984) was used to analyze the variation (synchrony) of intervals from PGF2 to estrus, duration of standing estrus, total number and duration of standing events, and duration of individual standing events.
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Results |
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TopAbstractIntroductionMaterials and MethodsResultsDiscussionImplicationsLiterature Cited |
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. In both dairy and beef heifers treated with P4, estrus detection rates were greater (P < 0.05) than those in the GnRH+PGF treatment. Estrus detection rates tended (P = 0.07) to be less for prepubertal heifers compared to cycling heifers, and less (P = 0.06) for all heifers that had no corpus luteum (CL) on d -1 than for heifers with a CL on d -1 (Table 2). Average interval from PGF2 to estrus was greater (P < 0.01) for both P4 treatments (68 ± 1.8 h) than for the GnRH+PGF treated heifers (52 ± 1.9 h). In addition, estrus detection rates were 10% greater (P < 0.05) in beef than dairy heifers.
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, based on continual surveillance of the dairy heifers by an electronic estrus-detection system, is illustrated in Figure 2 (upper panel). More (P < 0.01) dairy heifers in the P4+PGF (67%) and P4+GnRH+PGF (75%) treatments began estrus between 49 and 72 h after PGF2 than those in the GnRH+PGF treatment (40%). In contrast, more (P < 0.05) heifers in the GnRH+PGF treatment began estrus between 25 and 48 h (44%) after PGF2 than in other treatments (<10%). The peak in expressed estrus was confined to a 24-h period for those heifers treated with P4 compared to those receiving only GnRH before PGF2.
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summarizes the estrual characteristics of the dairy heifers in each treatment based on an electronic estrus-detection system. Interval from PGF2 injection to estrus, and the number of standing events per heifer in estrus, were affected differently by P4. In the P4+PGF and P4+GnRH+PGF treatments, interval from PGF2 injection to estrus was 18 to 19 h greater (P < 0.001) than that for the GnRH+PGF treatment. In contrast, pre-estrual supplementation of P4 via the P4 insert tended (P = 0.11) to reduce the number of standing events, but not their duration (P = 0.17). Duration of standing estrus and of individual standing events was not altered by treatment. Seasonal effects were detected for the number of standing events per heifer and duration of individual standing events. Total standing time was 61 to 75% greater (P < 0.05) during spring (100 ± 16 s) and fall (107 ± 8 s) than during summer (61 ± 12 s), and 44% greater (P < 0.10) during winter (89 ± 10 s) than in summer.
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(lower panel), the pattern of detected estrus of beef heifers was similar to that of dairy heifers (upper panel). Most of the beef heifers showed estrus between 49 and 72 h after PGF2. More (P < 0.01) beef heifers treated with P4 (72%) were in estrus between 49 and 72 h, whereas fewer (P < 0.05) heifers in the GnRH+PGF treatment (51%) were detected in estrus during that period.
Based on concentrations of P4 in blood sera collected on d -7, -1, and 0, heifers were placed into three pubertal categories (Table 2). Addition of pubertal status to the model eliminated significant effects of group (dairy vs beef) and treatment on estrus detection rates (Table 1). A treatment x group interaction (P < 0.05) resulted in a 32 to 45% reduction in the variation in interval from PGF2 injection to estrus of beef heifers in both P4 treatments compared to that of the GnRH+PGF treatment. Further, interval to estrus after PGF2 treatment was shorter (P < 0.001) for heifers that had no CL (low [<1 ng/mL] concentrations of P4) on d -1 compared to those with a CL (Table 2).
Blood Progesterone
Delayed interval to estrus after removal of the P4 insert may be explained by changes in serum concentrations of P4 (Figures 3 [upper panel] and 4 [upper panel]). A P4 treatment effect (P < 0.001) was detected on d 0 (day of insert removal), when 30% of the dairy and 32% of the beef heifers in the GnRH+PGF treatment had elevated concentrations of P4 compared to 77% of the dairy and 80% of the beef heifers that were administered P4 inserts.
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[lower panel and 4 [lower panel]). However, most of the difference on d -1 occurred because of greater (P < 0.05) serum concentrations of P4 in the P4+GnRH+PGF treatment than in GnRH+PGF treatment of both dairy and beef heifers. No differences in serum P4 were detected among treatments in dairy heifers on d 1 (24 h after PGF2 injection).
Fertility
Conception and pregnancy rates were not different between dairy and beef heifers, but treatment x group interactions were detected (P < 0.05; Table 1). In the dairy heifers, conception and pregnancy rates were greatest in the P4+PGF treatment and least in the GnRH+PGF treatment, whereas those in the P4+GnRH+PGF treatment were intermediate. In contrast, conception and pregnancy rates in the P4+PGF treatment were the least in beef heifers, whereas those in the P4+GnRH+PGF and GnRH+PGF treatments were nearly identical.
Conception rates were unaffected by the pubertal status of heifers on d -1 (Table 2). However, pregnancy rates were reduced (P < 0.05) in heifers with no CL on d -1 regardless of their pubertal status. More (P < 0.01) dairy (98%; 237/247) than beef (93%; 180/193) heifers were pubertal. Of the 18 heifers that were not pubertal on d 0, 11 were inseminated during the breeding week (120 h after PGF2). Of those 11 inseminated prepubertal heifers, four (36%) conceived from the first insemination, whereas 57% of all pubertal heifers conceived. During the breeding week, two nonpubertal heifers conceived (2 of 3) in the P4+PGF treatment, and one nonpubertal heifer was not inseminated. One nonpubertal heifer conceived (1 of 6) in the P4+GnRH+PGF treatment (four not inseminated). One nonpubertal heifer conceived (1 of 2) in the GnRH+PGF treatment and two were not inseminated.
Illustrated in Figure 5 are the conception rates achieved in 227 dairy heifers based on the intervals between the onset of estrus (detected by electronic estrus detection) and insemination. Timing of AI relative to the onset of estrus did not affect pregnancy outcomes. When individual intervals from detected estrus to AI were analyzed as regression variables, the beta coefficients (slopes) were not significant, implying that timing of AI was not a significant source of variation in conception rates. If it were, the increase in conception per hour would have been only 0.9 ± 0.7% per hour for inseminations made from 2 to 28 h after the onset of estrus.
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. These data are a summary of 77 heifers that did not conceive at first AI during a 3-yr period. Duration of standing estrus was not different between periods. Total number of standing events before first insemination was greater (P < 0.01) than that before second insemination. Further, total duration of standing events before first insemination also was 29% greater (P < 0.01) than that before second insemination. However, more (P < 0.05) heifers (13 ± 1) per replicate (replicate heifers were housed together with some additional nonsynchronized heifers) were in estrus during the synchronized breeding week compared to those in estrus together during the subsequent period of estrus (5 ± 1) 18 to 26 d later. Duration of individual standing events varied (P < 0.001) among months. Although no consistent pattern of duration was detected, the shortest durations of individual standing events occurred in February and the longest in September.
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Discussion |
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TopAbstractIntroductionMaterials and MethodsResultsDiscussionImplicationsLiterature Cited |
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, and found only 22% in estrus 2 d after insert removal.
Fewer heifers treated with PGF2 alone were in estrus during 6 d after treatment compared to heifers fed melengestrol acetate (MGA) for 7 d before PGF2 on d 7 (Chenault et al., 1990). Although conception rates were greater in those heifers after PGF2 alone than after MGA+PGF, pregnancy rates were similar. An experiment of similar design to the previous one (Chenault et al., 1990) that utilized the P4 insert in the place of feeding MGA to dairy and beef heifers was described recently (Lucy et al., 2001). In both dairy and beef heifers, proportions of heifers detected in estrus during the 3-d synchronization period after PGF2 were increased by inclusion of the P4 insert as in our experiment. Rates of detected estrus were greater in their dairy heifers because over 40% of the beef heifers were not cycling prior to treatments. Our report confirms this poor response among prepubertal heifers (Lucy et al., 2001) in which estrus detection and pregnancy rates were lower in their prepubertal beef heifers treated with P4 inserts.
Consistent with the interval from PGF2 to estrus in our P4-treated heifers, visually observed heifers treated with a 7-d P4-releasing intravaginal device (PRID) and PGF2 on d 6 (Smith et al., 1984) averaged 73 ± 1 h to estrus. Similar results occurred in dairy heifers when a progestin (norgestomet) was implanted for 8 d with or without an up-front GnRH injection (Stevenson et al., 2000).
Serum concentrations of P4 were greater in our heifers treated with both GnRH and P4 compared to those treated with only GnRH. This difference in P4 between these two treatments illustrated the marginal increase in concentrations of P4 contributed by the combination of the P4 insert and GnRH beyond that of GnRH alone. The reduction in concentration of serum P4 of approximately 1 ng/mL from d 0 to 1 in the dairy heifers represented the contribution of the P4 insert to blood concentrations of P4 after regression of a functional CL (24 h after PGF2 injection). Further, concentrations of P4 on d 0 in both P4 treatments indicated that the used P4 insert in this study seemed to have sufficient residual P4 to produce blood serum concentrations of P4 whose averages ranged from 1.5 to 1.7 ng/mL in the presence of a CL (88% of heifers had elevated P4 on d 0).
In our experiment, the slightly greater concentrations of P4 detected before first insemination of dairy heifers treated with P4 were associated with a tendency for fewer standing events and less standing time. Although not detected in the current experiment with the P4 inserts, we reported that duration of estrus was reduced by one-third in heifers pretreated with norgestomet implants for 6 d before PGF2 compared to controls (Stevenson et al., 2000). Further, total duration of standing events and individual duration of standing events were reduced when heifers were pretreated with norgestomet for 6 d before PGF2 injection (Stevenson et al., 2000), which was not true for heifers in our current experiment treated with P4 inserts.
Total standing events and their duration were less during the first estrus after AI. If these heifers were pregnant after first AI and had greater P4 secretion early after estrus and experienced changes in follicular development and estrogen secretion, but lost their embryos before maternal recognition of pregnancy of d 15 to 17, then this may explain why characteristics of expressed estrus seemed to be subsequently suppressed at that estrus. This reduced estrual activity at the second estrus is consistent with that which tended to occur in P4-treated heifers prior to first AI.
Uninseminated heifers showed a different distribution pattern of estrus than previously inseminated heifers (Van Cleef et al., 1991). Progesterone controls the luteolytic signal and stimulates production of endometrial secretions necessary for embryo development (Geisert et al., 1992). The postovulatory rise in blood P4 is elevated sooner and concentrations of P4 are greater in pregnant vs nonpregnant mated heifers (Henricks et al., 1974). Embryo survival in sheep is related to the postovulatory increase in P4 (Ashworth et al., 1989). However, embryo survival also was decreased at very high rates of P4 secretion. Interferon-
production on d 16 is closely related to concentrations of P4 (Kerbler et al., 1997), as well as other potential conceptus-derived products that may lead to suppressed estrus activity once the embryo dies. Some embryo losses occur before d 7, and approximately 40% occur between d 8 and 17, with an additional 24% between d 17 and 24 (Thatcher et al., 1994). Other work (Thatcher et al., 1991) supports the hypothesis that presence of the embryo in utero affects follicular development, especially on the side ipsilateral to the CL-bearing ovary, which is also adjacent to the conceptus. This change in follicular development on the CL-bearing ovary is an effect of the conceptus because hysterectomy maintains normal follicular dynamics in both ovaries. Perhaps this effect of the conceptus also alters timing of luteal regression and occurrence of estrus in heifers that experienced embryo mortality (Van Cleef et al., 1996).
This proportional increase in estrual activity for heifers before first service compared to that before second service could be simply explained by more heifers in synchrony at the first estrus. Nearly 80% of all attempted mounts are made by estrual females and 90% of all mounted animals in a common group were estrual (Hurnik et al., 1975). In the same study, it was shown that as the number of animals in estrus increased (as would be the case for synchronized estrus), a proportional increase occurred in the number of mounts per hour. Maximal standing activity per cow occurs when four or more females are concurrently in estrus (Hurnik et al., 1975). However, in our study, a heifer that repeated to second estrus was, on average, in the presence of at least four other estrual heifers, indicating that her estrual activity should not have been compromised by the lack of sufficient estrual partners.
No difference in conception rates of dairy heifers was detected among intervals from onset of estrus to AI despite the trend for improved conception when inseminations were carried out closer (>16 h after the onset of estrus) to the time of ovulation (based on the estimate of 27.6 h after the onset of estrus [detected by the same electronic estrus-detection system], and subsequently determined by repeated ultrasound examinations; Walker et al., 1996). The general trend of this response is not consistent with that reported for dairy heifers (Nebel et al., 1996) and dairy cows (Nebel et al., 2000), in which optimal conception rates tended to occur between 4 and 12 h after onset of estrus for cows and before 16 h in heifers.
Conception rates tended to be less in PGF-treated beef heifers than those treated with a PGF+P4 insert; the converse was true for dairy heifers (Lucy et al., 2001). Those results contradict what we observed in our beef and dairy heifers after treatment with P4+PGF and GnRH+PGF. Consistent with the results in our beef heifers are other reports in which cattle treated with progestins (short-term) experienced decreased conception rates (Patterson et al., 1986; Beal et al., 1988). This difference in beef heifers could be explained by the effectiveness of the GnRH-induced turnover or GnRH-induced ovulation of a follicle after d -7 (Pursley et al., 1995), thus preventing formation of a persistent dominant follicle in heifers without a CL or those near the end of their luteal phase on d -7. Oocytes ovulated from persistent follicles are known to be less fertile (Savio et al., 1993; Revah and Butler, 1994; Mihm et al., 1999).
In contrast, the formulation of persistent follicles containing potentially less quality oocytes did not seem to occur in our dairy heifers where conception rates were greatest in the P4+PGF treatment. Perhaps few persistent follicles formed in the presence of the P4 inserts because a functional CL was present (Smith and Stevenson, 1995) in dairy heifers compared to that which occurred in similarly treated beef heifers. Mass of P4 absorbed from the insert per body or metabolic weight was likely different because variation in the average body weights of beef and dairy heifers is quite large, ranging from 50 to 150 kg.
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Implications |
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TopAbstractIntroductionMaterials and MethodsResultsDiscussionImplicationsLiterature Cited |
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, preceded by P4, GnRH, or both, produced unexplainable differing pregnancy-rate responses in dairy and beef heifers. Just less than 50% of all treated heifers were impregnated successfully following treatments. Possible factors associated with early but lost pregnancies may reduce subsequent sexual behaviors associated with the first eligible postinsemination estrus. Further study is warranted to determine if this speculation is true. The current study was conducted with previously used P4 inserts. Although precautions were taken to clean and sanitize the P4 inserts prior to their reuse, no guarantee of their purity, potency, or sterility is made nor do we recommend their reuse.
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Footnotes |
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Received for publication March 27, 2002. Accepted for publication July 2, 2002.
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Literature Cited |
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TopAbstractIntroductionMaterials and MethodsResultsDiscussionImplicationsLiterature Cited |
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. J. Anim. Sci. 66:599–602. in beef and dairy heifers. J. Anim. Sci. 68:296–303.[Abstract]
for synchronizing estrus and shortening the interval to pregnancy in postpartum beef cows, peripubertal beef heifers, and dairy heifers. J. Anim. Sci. 79:982–995. and GnRH. Theriogenology 44:915–923.[Medline]
and progestins in the absence or presence of a functional corpus luteum. J. Anim. Sci. 73:3743–3751.[Abstract]
. J. Anim. Sci. 77:(Suppl. 1):225 (Abstr.).
, norgestomet, and gonadotropin-releasing hormone. J. Dairy Sci. 83:2008–2015.[Abstract]
. J. Dairy Sci. 83:471–476.[Abstract]
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