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Estrus Synchronization of Lactating Dairy Cows with GnRH, Progesterone, and Prostaglandin F2α
Estrus Synchronization of Lactating Dairy Cows with GnRH, Progesterone, and Prostaglandin F2α Z. Z. Xu, and L. J. Burton Livestock Improvement Corporation Ltd., Private Bag 3016, Hamilton, New Zealand
ABSTRACT The reproductive performance of synchronized cows was compared with that of nonsynchronized cows. In trial 1, cyclic cows in five seasonal herds were randomly divided into two groups. Cows in one group (n = 515) were treated with a GnRH agonist and an intravaginal progesterone device, followed in 7 d by a PGF2α injection, and the device was removed 1 d after PGF2α. Cows in the other group (n = 512) did not receive any treatment and acted as control. In trial 2, the treatments were similar to those used in trial 1 except that the progesterone device was removed at the time of PGF2α injection (synchronized: n = 516; control: n = 512). The estrus synchronization rate was 92.8% in trial 1 and 92.2% in trial 2. Conception rate to first artificial insemination (AI) was lower for synchronized cows than for control cows in trial 1 (56.5 vs. 62.7%), but similar in trial 2 (64.6 vs. 63.3%). Across both trials, the pregnancy rate during the AI breeding period was greater for the synchronized cows (85.6%) than for the control cows (81.2%). The synchronization treatment reduced the interval from start of the breeding season to conception for cows conceiving by AI (8.9 vs. 14.8 d) or by AI or natural mating (14.1 vs. 21.6 d). The synchronization protocol used in trial 2 achieved better conception rate than that used in trial 1, but the precision of estrus was less in trial 2 than in trial 1. (Key words: estrus synchronization, reproductive performance, dairy cow) Abbreviation key: CIDR = controlled internal drug release device (InterAg, Hamilton, New Zealand), CL = corpus luteum, ISBC = interval from start of breeding to conception. INTRODUCTION Previous studies have shown that most progestogenbased estrus synchronization programs for cattle are associated with a reduction in conception rate at the synchronized estrus (11, 12, 18, 26, 41, 42). The reduc-
Received May 24, 1999. Accepted October 21, 1999. Corresponding author: Z. Z. Xu; e-mail:[email protected] 2000 J Dairy Sci 83:471–476
tion in fertility after estrus synchronization with progestogens has been attributed to the development of persistent dominant follicles and subsequently the ovulation of aged oocytes that, if fertilized, result in a poorquality embryos with reduced developmental capacity (16, 28, 32, 39). These results suggest that a successful estrus synchronization program should aim to synchronize follicular wave development as well as onset of estrus and ovulation. Progesterone, GnRH, estrogen, or a combination of progesterone and estrogen have been used to synchronize the onset of follicular waves in cattle (2, 3, 4, 5, 7, 34). Recently, an ovulation synchronization program involving GnRH and PGF2α (ovsynch) has been developed for use on dairy cows (19, 21, 31). The ovsynch program improves reproductive performance mainly by eliminating some of the errors associated with estrus detection because cows treated with the ovsynch program are inseminated at a fixed time after the second GnRH injection and estrus detection is not required (6, 19, 31). In the ovsynch program, GnRH is administered to cows at random stages of the estrous cycle. As a result, those cows that are in the late luteal, follicular, or early luteal phase of the estrous cycle at the time of GnRH treatment will experience an extended period of low progesterone before ovulation. Previous studies have shown that progesterone concentration during the late luteal phase before insemination is positively associated with conception rate (8, 9, 10, 23, 24). Progesterone supplementation to cows that were synchronized with PGF2α increased the estrous response and conception rate of cows in the early stage of the luteal phase at the time of the second PGF2α treatment (43). Therefore, the reproductive performance of cows receiving the ovsynch treatment may be improved if progesterone is administered during the period between the GnRH and PGF2α injections. Such progesterone treatment can also prevent premature ovulation, after spontaneous luteolysis during the treatment period, in a small percentage of cows whose dominant follicles are not responsive to the GnRH treatment (20, 25, 36, 38). The objective of the present study was to compare the reproductive performance of cows that were synchronized with a GnRH agonist (buserelin), progesterone, and PGF2α with that of nonsynchronized herd mates.
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MATERIALS AND METHODS Cows and Treatment Protocol Trial 1. This trial was conducted in 1996 with lactating cows from five spring-calving dairy herds. On d – 35, [i.e., 35 d before the start of the breeding season (d 0)], cows in these herds were tailpainted for identification of cyclic cows (13) and date of onset of estrus was recorded. On d –11, ovaries of cows that had not been detected in estrus during the previous 24 d were examined by palpation per rectum for the presence of a corpus luteum (CL). Cows that had a palpable CL on the ovary were considered as cyclic cows and were included in the study. Cows in each herd were paired by breed, age, calving date, and stage of the estrous cycle; cows in each pair were assigned randomly to each of two treatment groups. On d –10, cows in one group (the synchronized group) were each treated with an intravaginal progesterone releasing device containing 1.9 g of progesterone (CIDR, InterAg, Hamilton, New Zealand) and 10 µg of buserelin, a GnRH agonist (Receptal, AGVET NZ Ltd, Auckland, New Zealand). On d –3, they were injected with 25 mg of PGF2α (Lutalyse, Phamacia & Upjohn, Auckland, New Zealand). The CIDR device was removed on d –2, 8 d after insertion. Cows in the other group (the control group) did not receive any treatment. Breeding by AI started on the second day after CIDR removal. Ovaries of cows that had not been detected in estrus 11 d (synchronized group) or 24 d (control group) after the start of the breeding season were examined by palpation per rectum for the presence of a CL. Cows with a palpable CL were treated with PGF2α to induce luteolysis, while those without a palpable CL in both groups were treated with progesterone and estradiol benzoate to induce estrus and ovulation (40). Trial 2. This trial was conducted in 1997 using cyclic cows from four spring-calving herds. The treatment protocol for trial 2 was similar to that used in trial 1 except that the period of progesterone treatment was 7 d (i.e., the CIDR device was removed at the time of PGF2α injection). As a result, the time of initiation of trial 2 relative to the start of the breeding season was 1 d later than in trial 1. Breeding and Pregnancy Diagnosis Breeding started 2 d after CIDR removal. Cows in both groups were bred by AI with the same batches of frozen semen from bulls of known fertility. Semen usage from each bull was balanced between the treatment groups. AI was carried out once a day in the morning on cows detected in estrus during the previous 24 h by visual observation aided by the tailpainting technique Journal of Dairy Science Vol. 83, No. 3, 2000
(13). Breeding by AI continued for between 5 and 7 wk depending on herds. Thereafter, herd sires of beef breeds were used for natural service. Dates of all matings were recorded. Date of conception was confirmed by pregnancy diagnosis through palpation per rectum by each herd owner’s attending veterinarian between 6 and 8 wk after the end of AI and natural mating periods, respectively. Conception dates were further confirmed by calving dates for cows remaining in the herds in the following calving season. Data and Statistical Analysis Conception rate was defined as the percentage of inseminations that resulted in a confirmed pregnancy. Pregnancy rate was defined as the percentage of cows in a group that conceived within a defined period. In addition, the percentage of cows that failed to conceive during the breeding period (nonpregnancy rate) and the interval from the start of the breeding season to conception (ISBC) were also analyzed. Categorical data, such as conception rate, pregnancy rate and nonpregnancy rate, were analyzed by the CATMOD procedure of SAS (27), which was used to perform maximum likelihood estimation of parameters on data after logit transformation. The ISBC data was analyzed by the LIFETEST procedure of SAS (27), which was used to perform survival analysis on the interval data to take into account the right-censored observations for cows that did not conceive during the breeding period. RESULTS AND DISCUSSION Seventeen cows (two from the control group in trial 1, eight from the control group in trial 2, and seven from the synchronized group in trial 2) died or were culled before their pregnancy status could be established for reasons not related to the treatments applied in the study. These cows were included in the analyses of estrous responses, but were excluded from analyses of pregnancy-related parameters. Estrous Response Detection of estrus over the first 6 d of the breeding season (i.e., within 7 d after CIDR removal) was taken as a response to the treatments. The estrous response rate for cows in the synchronized group was 92.8% in trial 1 and 92.2% in trial 2 (Table 1). Most of the cows that responded to the synchronization treatment were detected in estrus and inseminated in the first 2 (trial 1) or 3 (trial 2) d of the breeding season. Changing the synchronization program from 8 d in trial 1 to 7 d in
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ESTRUS SYNCHRONIZATION OF LACTATING COWS Table 1. Estrous response of control cows and cows that had been synchronized with progesterone, GnRH, and PGF2α in trial 1 and trial 2. Trial 1
Total number of cows, n Cows inseminated, % d0 d1 d2 d3 d4 d5 Total in 6 d Veterinary examination results1 Cows examined, n Cows with CL,2 % Cows without CL,2 %
Trial 2
Control
Synchronized
Control
Synchronized
512
515
512
516
5.7 7.4 5.9 2.9 6.1 5.3 33.2
55.7 27.8 3.1 2.7 2.3 1.2 92.8
6.1 4.5 6.3 4.7 4.1 6.3 31.8
21.5 47.1 17.2 1.7 2.1 2.5 92.2
23 47.8 52.2
29 51.7 48.3
22 18.2 81.8
22 22.7 77.3
1 Cows that had not been detected in estrus 11 d (synchronized group) or 24 d (control group) after the start of the breeding season were examined by palpation per rectum for the presence of a corpus luteum on the ovary. 2 CL = corpus luteum.
trial 2 altered the pattern of estrous response (P < 0.001; Table 1). In trial 1 where the CIDR device was removed 1 d after PGF2α injection, 55.7% of the cows were detected in estrus on d 0 (i.e., between 24 and 48 h after CIDR removal), 27.8% on d 1, and between 1.2 and 3.1% on the following 4 d. In trial 2 where the CIDR device was removed at the time of PGF2α injection, only 21.5% were detected in estrus on d 0, 47.1% on d 1, 17.2% on d 2, and between 1.7 and 2.5% on each of the following 3 d. It is postulated that the dominant follicles that developed after the GnRH treatment were at a more advanced stage of development at the time of CIDR removal in trial 1 than in trial 2. The percentages of control group cows that were detected in estrus in the first 6 d of the breeding season were 33.2% in trial 1 and 31.8% in trial 2. In the present study, about 6% of synchronized cows in both trials were detected in estrus and inseminated on d 3, 4, and 5 of the breeding season (i.e., between 5 and 7 d after CIDR removal, Table 1). It is likely that these cows did not have a functionally dominant follicle at the time of CIDR removal possibly because the dominant follicle had recently turned over. This situation could occur if the dominant follicle was too small (< 9 mm in diameter) at the time of GnRH injection to respond to the GnRH-induced LH surge because of a lack of LH receptors on the granulosa cells (35, 44). In cows that were synchronized with the ovsynch program, 7% of the cows did not ovulate in response to the second GnRH injection (38). There was no difference between trials or treatments in the percentage of cows that were examined on d 11 (synchronized groups) or 24 (control groups) because they had not been submitted for an insemination by
that time. A higher (P < 0.01) percentage of the cows in trial 1 were found to have a palpable CL than those in trial 2, but there were no effects of treatment or treatment by trial interactions on the percentage of cows with palpable CL. Reproductive Performance In trial 1, the conception rate of synchronized cows to the first insemination at the synchronized estrus (56.5%) was lower (P = 0.05) than that of control cows to the first insemination during the first 24 d of the breeding season (62.7%; Table 2). In trial 2, the conception rates to the first insemination were not different between cows in the control (63.3%) and synchronized (64.6%) groups. The reasons for the reduced conception rate of synchronized cows in trial 1 could not be determined in the present study. The only difference in the treatment protocols between the two trials was a reduction in the duration of progesterone treatment from 8 d in trial 1 to 7 d in trial 2. It is possible that the extra day of progesterone treatment after PGF2α injection in trial 1 allowed some dominant follicles to be maintained for a longer than optimal period, resulting in the ovulation of “aged” oocytes with reduced developmental capacity (16, 17, 22). In cows that were treated with GnRH and PGF2α to synchronize ovulation, the size of the dominant follicle at the time of the second GnRH injection was negatively associated with conception rate (38). If persistent dominant follicles did develop in the present study, those cows with persistent dominant follicles would most likely be detected in estrus and inseminated on the first day of the breeding season because persistent dominant follicles are at a more advanced Journal of Dairy Science Vol. 83, No. 3, 2000
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stage of development and they produce more estradiol than growing dominant follicles (1, 30). However, the conception rate of synchronized cows in trial 1 that were inseminated on the first day of the breeding season (58.9%, n = 287) was similar (P = 0.32) to that of cows inseminated on the second day (53.9%, n = 143). Caution should be taken in interpreting this result because of the small number of observations on the second day. Conception rate to second AI was similar (P = 0.31) between treatment groups. At the end of the AI breeding period, the pregnancy rate of cows in the synchronized group was higher than that of cows in the control group in both trial 1 (86.2 vs. 82.2%, P = 0.08) and trial 2 (85.1 vs. 80.2%, P < 0.05; Table 2). The nonpregnancy rate at the end of the breeding season was not different between treatment groups. Across both trials, the mean interval from the start of the breeding season to conception for cows conceived by AI or by AI or natural mating was, respectively, 5.9 and 7.5 d shorter (P < 0.001) for the synchronized group than for the control group. General Discussion In the present study, we compared the reproductive performance of lactating dairy cows after estrus synchronization by two slightly different protocols with that of nonsynchronized cows. The synchronization protocol used in trial 2 eliminated the reduction in conception rate that has often been observed after estrus synchronization under the New Zealand conditions (42, 43). Across both trials, the reproductive performance of synchronized cows, as measured by the pregnancy rate during the AI period or by the interval from start
of the breeding season to conception, was higher than that of control cows. A GnRH treatment followed 7 d later by an injection of PGF2α has been successfully used for synchronizing follicular wave development and luteolysis (19, 20, 31, 35, 37). In the present study, cows were also treated with a CIDR device to supplement progesterone to those cows that were likely to have a low progesterone concentration during the treatment period. Previous studies have shown that progesterone concentration in the late luteal phase before insemination is positively associated with conception rate (8, 9, 10, 23, 24, 43). Additionally, it has been observed that progesterone concentration during one estrous cycle affects the endometrial morphology in the subsequent cycle (29). Therefore, the use of the CIDR device in the program should improve conception rate at the synchronized estrus compared with GnRH and PGF2α alone. In trial 1, the CIDR device was inserted for 8 d and removed 1 d after the PGF2α injection. The removal of the CIDR device 1 d after PGF2α injection was intended to improve the precision of estrus. The results showed that 55.7% of treated cows were detected in estrus between 24 and 48 h after CIDR removal and another 27.8% during the following 24 h, giving a total of 83.5% over a 48-h period. Thus this treatment protocol offers the opportunity for fixed-time AI at 48 h if onset of estrus or ovulation is further synchronized with an injection of estradiol or GnRH 36 h after CIDR removal. In herds with estrus detection problems, the use of estrus synchronization and fixed-time AI might improve reproductive performance by eliminating the problems associated with estrus detection even though
Table 2. Reproductive performance of control cows (C group) and cows that had been synchronized with progesterone, GnRH, and PGF2α (S group) in trial 1 and trial 2. Trial 1
Total number of cows, n Number of 1st AI,1 n Conception rate to 1st AI, % Number of 2nd AI, n Conception rate to 2nd AI, % Pregnancy rate to all AI, % Nonpregnancy rate, % ISBC-AI,2 d ISBC-all,3 d
Trial 2
Combined
C
S
C
S
C
S
510 485 62.7 147 60.5 82.2 4.7 15.2 21.8
515 478 56.5a 194 67.5 86.2c 4.3 9.8b 14.4b
504 482 63.3 140 54.3 80.2 5.2 14.4 21.3
509 469 64.6 166 54.8 85.1a 5.1 8.0b 13.9b
1014 967 63.0 287 57.4 81.2 4.9 14.8 21.6
1024 947 60.5 360 61.7 85.6b 4.7 8.9b 14.1b
P ≤ 0.05 when compared with the corresponding value for the C group. P < 0.01 when compared with the corresponding value for the C group. c P < 0.10 when compared with the corresponding value for the C group. 1 Over the first 24 d for cows in the C group and over the first 6 d for cows in the S group. 2 Mean interval from the start of the breeding season to conception for cows that conceived by AI. 3 Mean interval from the start of the breeding season to conception for cows that conceived by AI or by natural mating. a b
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conception rate at the synchronized estrus may be slightly compromised (31). In trial 2, the duration of CIDR treatment was reduced from 8 to 7 d to investigate if the observed reduction in conception rate at the synchronized estrus in trial 1 could be eliminated. Results from trial 2 showed that similar conception rates were obtained in the synchronized and control cows. However, reducing the duration of progesterone treatment increased the distribution in the onset of estrus over a 3-d period. Such a wide spread in the onset of estrus pattern is not precise enough to allow fixed-time AI to achieve an acceptable conception rate. Although the precision of estrus or ovulation can be improved by an injection of estradiol or GnRH after the CIDR treatment, induction of premature ovulation has been shown to reduce conception rate (15, 31, 33). Under the seasonal dairy farming system in New Zealand, the efficiency and accuracy of estrus detection in most herds are very high (14, 42, 45). In herds with good estrus detection performance, some spread in the onset of estrus pattern may not be a major problem if the main reason for using estrus synchronization is to improve the overall reproductive performance. For large seasonal herds in which all cows are treated at the same time, less tight synchrony in the onset of estrus may be advantageous because spreading inseminations over a few days reduces the number of farm staff and AI technicians required each day and helps to minimize the likely adverse effects due to bad weather or other operational problems on a particular day. CONCLUSIONS The present study showed that onset of estrus of lactating dairy cows in seasonal herds can be successfully synchronized with progesterone, GnRH, and PGF2α. The program involving an 8-d progesterone treatment resulted in tight synchrony of onset of estrus, but reduced conception rate at the synchronized estrus. In contrast, the program involving a 7-d progesterone treatment resulted in normal conception rate at the synchronized estrus, but the synchrony was more dispersed than the 8-d program. Both programs improved reproductive performance compared with nonsynchronized control cows. When a tight synchrony is not required, the protocol used in trial 2 is preferred over that used in trial 1 because it did not reduce conception rate at the synchronized estrus. ACKNOWLEDGMENTS We thank the participating herd owners and veterinarians for their help and cooperation during the trial,
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32 Stock, A. E., and J. E. Fortune. 1993. Ovarian follicular dominance in cattle: relationship between prolonged growth of the ovulatory follicle and endocrine parameters. Endocrinology 132:1108–1114. 33 Taponen, J., T. Katila, and H. Rodrı´guez-Martı´nez. 1999. Induction of ovulation with gonadotropin-releasing hormone during proestrus in cattle: influence on subsequent follicular growth and luteal function. Anim. Reprod. Sci. 55:91–105. 34 Twagiramungu, H., J. J. Dufour, and L. A. Guilbault. 1994. Follicular development and estrous synchronization in cattle: effect of a GnRH agonist. J. Dairy Sci. 77(Suppl. 1):143. (Abstr.) 35 Twagiramungu, H., L. A. Guilbault, and J. J. Dufour. 1995. Synchronization of ovarian follicular waves with a gonadotropin-releasing hormone agonist to increase the precision of estrus in cattle: a review. J. Anim. Sci. 73:3141–3151. 36 Twagiramungu, H., L. A. Guilbault, J. Proulx, P. Villeneuve, and J. J. Dufour. 1992. Influence of an agonist of gonadotropin-releasing hormone (Buserelin) on estrus synchronization and fertility in beef cows. J. Anim. Sci. 70:1904–1910. 37 Twagiramungu, H., G. L. Roy, G. Laverdiere, and J. J. Dufour. 1995. Fixed-time insemination in cattle after synchronization of estrus and ovulation with GnRH and prostaglandin. Theriogenology 43:341. (Abstr.) 38 Vasconcelos, J.L.M., R. W. Silcox, G. J. Rosa, J. R. Pursley, and M. C. Wiltbank. 1997. Synchronization rate, size of the ovulatory follicle, and conception rate after synchronization of ovulation with GnRH on different days of the estrous cycle. J. Dairy Sci. 80(Suppl. 1):178. (Abstr.) 39 Wishart, D. F. 1977. Synchronisation of oestrus in heifers using steroid (SC5914, SC9880 and SC21009) treatment for 21 days. 2. The effect of treatment on the ovum collection and fertilisation rate and the development of the early embryo. Theriogenology 8:249–269. 40 Xu, Z. Z., and L. J. Burton. 1997. Reproductive performance of postpartum anoestrous dairy cows treated with progesterone and oestradiol benzoate. N.Z. Vet. J. 45:213–214. 41 Xu, Z. Z., and L. J. Burton. 1999. Reproductive performance of dairy heifers after estrus synchronization and fixed-time artificial insemination. J. Dairy Sci. 82:910–917. 42 Xu, Z. Z., L. J. Burton, and K. L. Macmillan. 1996. Reproductive performance of lactating dairy cows following oestrus synchronisation with progesterone, oestradiol and prostaglandin. N.Z. Vet. J. 44:99–104. 43 Xu, Z. Z., L. J. Burton, and K. L. Macmillan. 1997. Reproductive performance of lactating dairy cows following estrus synchronization regimens with PGF2α and progesterone. Theriogenology 47:687–701. 44 Xu, Z. Z., H. A. Garverick, M. F. Smith, G. W. Smith, S. A. Hamilton, and R. S. Youngquist. 1995. Expression of follicle-stimulating hormone and luteinizing hormone receptor messenger ribonucleic acids in bovine follicles during the first follicular wave. Biol. Reprod. 53:951–957. 45 Xu, Z. Z., D. J. McKnight, R. Vishwanath, C. J. Pitt, and L. J. Burton. 1998. Estrus detection using radiotelemetry or visual observation and tail painting in dairy cows on pasture. J. Dairy Sci. 81:2890–2896.
ABSTRACT The reproductive performance of synchronized cows was compared with that of nonsynchronized cows. In trial 1, cyclic cows in five seasonal herds were randomly divided into two groups. Cows in one group (n = 515) were treated with a GnRH agonist and an intravaginal progesterone device, followed in 7 d by a PGF2α injection, and the device was removed 1 d after PGF2α. Cows in the other group (n = 512) did not receive any treatment and acted as control. In trial 2, the treatments were similar to those used in trial 1 except that the progesterone device was removed at the time of PGF2α injection (synchronized: n = 516; control: n = 512). The estrus synchronization rate was 92.8% in trial 1 and 92.2% in trial 2. Conception rate to first artificial insemination (AI) was lower for synchronized cows than for control cows in trial 1 (56.5 vs. 62.7%), but similar in trial 2 (64.6 vs. 63.3%). Across both trials, the pregnancy rate during the AI breeding period was greater for the synchronized cows (85.6%) than for the control cows (81.2%). The synchronization treatment reduced the interval from start of the breeding season to conception for cows conceiving by AI (8.9 vs. 14.8 d) or by AI or natural mating (14.1 vs. 21.6 d). The synchronization protocol used in trial 2 achieved better conception rate than that used in trial 1, but the precision of estrus was less in trial 2 than in trial 1. (Key words: estrus synchronization, reproductive performance, dairy cow) Abbreviation key: CIDR = controlled internal drug release device (InterAg, Hamilton, New Zealand), CL = corpus luteum, ISBC = interval from start of breeding to conception. INTRODUCTION Previous studies have shown that most progestogenbased estrus synchronization programs for cattle are associated with a reduction in conception rate at the synchronized estrus (11, 12, 18, 26, 41, 42). The reduc-
Received May 24, 1999. Accepted October 21, 1999. Corresponding author: Z. Z. Xu; e-mail:[email protected] 2000 J Dairy Sci 83:471–476
tion in fertility after estrus synchronization with progestogens has been attributed to the development of persistent dominant follicles and subsequently the ovulation of aged oocytes that, if fertilized, result in a poorquality embryos with reduced developmental capacity (16, 28, 32, 39). These results suggest that a successful estrus synchronization program should aim to synchronize follicular wave development as well as onset of estrus and ovulation. Progesterone, GnRH, estrogen, or a combination of progesterone and estrogen have been used to synchronize the onset of follicular waves in cattle (2, 3, 4, 5, 7, 34). Recently, an ovulation synchronization program involving GnRH and PGF2α (ovsynch) has been developed for use on dairy cows (19, 21, 31). The ovsynch program improves reproductive performance mainly by eliminating some of the errors associated with estrus detection because cows treated with the ovsynch program are inseminated at a fixed time after the second GnRH injection and estrus detection is not required (6, 19, 31). In the ovsynch program, GnRH is administered to cows at random stages of the estrous cycle. As a result, those cows that are in the late luteal, follicular, or early luteal phase of the estrous cycle at the time of GnRH treatment will experience an extended period of low progesterone before ovulation. Previous studies have shown that progesterone concentration during the late luteal phase before insemination is positively associated with conception rate (8, 9, 10, 23, 24). Progesterone supplementation to cows that were synchronized with PGF2α increased the estrous response and conception rate of cows in the early stage of the luteal phase at the time of the second PGF2α treatment (43). Therefore, the reproductive performance of cows receiving the ovsynch treatment may be improved if progesterone is administered during the period between the GnRH and PGF2α injections. Such progesterone treatment can also prevent premature ovulation, after spontaneous luteolysis during the treatment period, in a small percentage of cows whose dominant follicles are not responsive to the GnRH treatment (20, 25, 36, 38). The objective of the present study was to compare the reproductive performance of cows that were synchronized with a GnRH agonist (buserelin), progesterone, and PGF2α with that of nonsynchronized herd mates.
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MATERIALS AND METHODS Cows and Treatment Protocol Trial 1. This trial was conducted in 1996 with lactating cows from five spring-calving dairy herds. On d – 35, [i.e., 35 d before the start of the breeding season (d 0)], cows in these herds were tailpainted for identification of cyclic cows (13) and date of onset of estrus was recorded. On d –11, ovaries of cows that had not been detected in estrus during the previous 24 d were examined by palpation per rectum for the presence of a corpus luteum (CL). Cows that had a palpable CL on the ovary were considered as cyclic cows and were included in the study. Cows in each herd were paired by breed, age, calving date, and stage of the estrous cycle; cows in each pair were assigned randomly to each of two treatment groups. On d –10, cows in one group (the synchronized group) were each treated with an intravaginal progesterone releasing device containing 1.9 g of progesterone (CIDR, InterAg, Hamilton, New Zealand) and 10 µg of buserelin, a GnRH agonist (Receptal, AGVET NZ Ltd, Auckland, New Zealand). On d –3, they were injected with 25 mg of PGF2α (Lutalyse, Phamacia & Upjohn, Auckland, New Zealand). The CIDR device was removed on d –2, 8 d after insertion. Cows in the other group (the control group) did not receive any treatment. Breeding by AI started on the second day after CIDR removal. Ovaries of cows that had not been detected in estrus 11 d (synchronized group) or 24 d (control group) after the start of the breeding season were examined by palpation per rectum for the presence of a CL. Cows with a palpable CL were treated with PGF2α to induce luteolysis, while those without a palpable CL in both groups were treated with progesterone and estradiol benzoate to induce estrus and ovulation (40). Trial 2. This trial was conducted in 1997 using cyclic cows from four spring-calving herds. The treatment protocol for trial 2 was similar to that used in trial 1 except that the period of progesterone treatment was 7 d (i.e., the CIDR device was removed at the time of PGF2α injection). As a result, the time of initiation of trial 2 relative to the start of the breeding season was 1 d later than in trial 1. Breeding and Pregnancy Diagnosis Breeding started 2 d after CIDR removal. Cows in both groups were bred by AI with the same batches of frozen semen from bulls of known fertility. Semen usage from each bull was balanced between the treatment groups. AI was carried out once a day in the morning on cows detected in estrus during the previous 24 h by visual observation aided by the tailpainting technique Journal of Dairy Science Vol. 83, No. 3, 2000
(13). Breeding by AI continued for between 5 and 7 wk depending on herds. Thereafter, herd sires of beef breeds were used for natural service. Dates of all matings were recorded. Date of conception was confirmed by pregnancy diagnosis through palpation per rectum by each herd owner’s attending veterinarian between 6 and 8 wk after the end of AI and natural mating periods, respectively. Conception dates were further confirmed by calving dates for cows remaining in the herds in the following calving season. Data and Statistical Analysis Conception rate was defined as the percentage of inseminations that resulted in a confirmed pregnancy. Pregnancy rate was defined as the percentage of cows in a group that conceived within a defined period. In addition, the percentage of cows that failed to conceive during the breeding period (nonpregnancy rate) and the interval from the start of the breeding season to conception (ISBC) were also analyzed. Categorical data, such as conception rate, pregnancy rate and nonpregnancy rate, were analyzed by the CATMOD procedure of SAS (27), which was used to perform maximum likelihood estimation of parameters on data after logit transformation. The ISBC data was analyzed by the LIFETEST procedure of SAS (27), which was used to perform survival analysis on the interval data to take into account the right-censored observations for cows that did not conceive during the breeding period. RESULTS AND DISCUSSION Seventeen cows (two from the control group in trial 1, eight from the control group in trial 2, and seven from the synchronized group in trial 2) died or were culled before their pregnancy status could be established for reasons not related to the treatments applied in the study. These cows were included in the analyses of estrous responses, but were excluded from analyses of pregnancy-related parameters. Estrous Response Detection of estrus over the first 6 d of the breeding season (i.e., within 7 d after CIDR removal) was taken as a response to the treatments. The estrous response rate for cows in the synchronized group was 92.8% in trial 1 and 92.2% in trial 2 (Table 1). Most of the cows that responded to the synchronization treatment were detected in estrus and inseminated in the first 2 (trial 1) or 3 (trial 2) d of the breeding season. Changing the synchronization program from 8 d in trial 1 to 7 d in
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ESTRUS SYNCHRONIZATION OF LACTATING COWS Table 1. Estrous response of control cows and cows that had been synchronized with progesterone, GnRH, and PGF2α in trial 1 and trial 2. Trial 1
Total number of cows, n Cows inseminated, % d0 d1 d2 d3 d4 d5 Total in 6 d Veterinary examination results1 Cows examined, n Cows with CL,2 % Cows without CL,2 %
Trial 2
Control
Synchronized
Control
Synchronized
512
515
512
516
5.7 7.4 5.9 2.9 6.1 5.3 33.2
55.7 27.8 3.1 2.7 2.3 1.2 92.8
6.1 4.5 6.3 4.7 4.1 6.3 31.8
21.5 47.1 17.2 1.7 2.1 2.5 92.2
23 47.8 52.2
29 51.7 48.3
22 18.2 81.8
22 22.7 77.3
1 Cows that had not been detected in estrus 11 d (synchronized group) or 24 d (control group) after the start of the breeding season were examined by palpation per rectum for the presence of a corpus luteum on the ovary. 2 CL = corpus luteum.
trial 2 altered the pattern of estrous response (P < 0.001; Table 1). In trial 1 where the CIDR device was removed 1 d after PGF2α injection, 55.7% of the cows were detected in estrus on d 0 (i.e., between 24 and 48 h after CIDR removal), 27.8% on d 1, and between 1.2 and 3.1% on the following 4 d. In trial 2 where the CIDR device was removed at the time of PGF2α injection, only 21.5% were detected in estrus on d 0, 47.1% on d 1, 17.2% on d 2, and between 1.7 and 2.5% on each of the following 3 d. It is postulated that the dominant follicles that developed after the GnRH treatment were at a more advanced stage of development at the time of CIDR removal in trial 1 than in trial 2. The percentages of control group cows that were detected in estrus in the first 6 d of the breeding season were 33.2% in trial 1 and 31.8% in trial 2. In the present study, about 6% of synchronized cows in both trials were detected in estrus and inseminated on d 3, 4, and 5 of the breeding season (i.e., between 5 and 7 d after CIDR removal, Table 1). It is likely that these cows did not have a functionally dominant follicle at the time of CIDR removal possibly because the dominant follicle had recently turned over. This situation could occur if the dominant follicle was too small (< 9 mm in diameter) at the time of GnRH injection to respond to the GnRH-induced LH surge because of a lack of LH receptors on the granulosa cells (35, 44). In cows that were synchronized with the ovsynch program, 7% of the cows did not ovulate in response to the second GnRH injection (38). There was no difference between trials or treatments in the percentage of cows that were examined on d 11 (synchronized groups) or 24 (control groups) because they had not been submitted for an insemination by
that time. A higher (P < 0.01) percentage of the cows in trial 1 were found to have a palpable CL than those in trial 2, but there were no effects of treatment or treatment by trial interactions on the percentage of cows with palpable CL. Reproductive Performance In trial 1, the conception rate of synchronized cows to the first insemination at the synchronized estrus (56.5%) was lower (P = 0.05) than that of control cows to the first insemination during the first 24 d of the breeding season (62.7%; Table 2). In trial 2, the conception rates to the first insemination were not different between cows in the control (63.3%) and synchronized (64.6%) groups. The reasons for the reduced conception rate of synchronized cows in trial 1 could not be determined in the present study. The only difference in the treatment protocols between the two trials was a reduction in the duration of progesterone treatment from 8 d in trial 1 to 7 d in trial 2. It is possible that the extra day of progesterone treatment after PGF2α injection in trial 1 allowed some dominant follicles to be maintained for a longer than optimal period, resulting in the ovulation of “aged” oocytes with reduced developmental capacity (16, 17, 22). In cows that were treated with GnRH and PGF2α to synchronize ovulation, the size of the dominant follicle at the time of the second GnRH injection was negatively associated with conception rate (38). If persistent dominant follicles did develop in the present study, those cows with persistent dominant follicles would most likely be detected in estrus and inseminated on the first day of the breeding season because persistent dominant follicles are at a more advanced Journal of Dairy Science Vol. 83, No. 3, 2000
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stage of development and they produce more estradiol than growing dominant follicles (1, 30). However, the conception rate of synchronized cows in trial 1 that were inseminated on the first day of the breeding season (58.9%, n = 287) was similar (P = 0.32) to that of cows inseminated on the second day (53.9%, n = 143). Caution should be taken in interpreting this result because of the small number of observations on the second day. Conception rate to second AI was similar (P = 0.31) between treatment groups. At the end of the AI breeding period, the pregnancy rate of cows in the synchronized group was higher than that of cows in the control group in both trial 1 (86.2 vs. 82.2%, P = 0.08) and trial 2 (85.1 vs. 80.2%, P < 0.05; Table 2). The nonpregnancy rate at the end of the breeding season was not different between treatment groups. Across both trials, the mean interval from the start of the breeding season to conception for cows conceived by AI or by AI or natural mating was, respectively, 5.9 and 7.5 d shorter (P < 0.001) for the synchronized group than for the control group. General Discussion In the present study, we compared the reproductive performance of lactating dairy cows after estrus synchronization by two slightly different protocols with that of nonsynchronized cows. The synchronization protocol used in trial 2 eliminated the reduction in conception rate that has often been observed after estrus synchronization under the New Zealand conditions (42, 43). Across both trials, the reproductive performance of synchronized cows, as measured by the pregnancy rate during the AI period or by the interval from start
of the breeding season to conception, was higher than that of control cows. A GnRH treatment followed 7 d later by an injection of PGF2α has been successfully used for synchronizing follicular wave development and luteolysis (19, 20, 31, 35, 37). In the present study, cows were also treated with a CIDR device to supplement progesterone to those cows that were likely to have a low progesterone concentration during the treatment period. Previous studies have shown that progesterone concentration in the late luteal phase before insemination is positively associated with conception rate (8, 9, 10, 23, 24, 43). Additionally, it has been observed that progesterone concentration during one estrous cycle affects the endometrial morphology in the subsequent cycle (29). Therefore, the use of the CIDR device in the program should improve conception rate at the synchronized estrus compared with GnRH and PGF2α alone. In trial 1, the CIDR device was inserted for 8 d and removed 1 d after the PGF2α injection. The removal of the CIDR device 1 d after PGF2α injection was intended to improve the precision of estrus. The results showed that 55.7% of treated cows were detected in estrus between 24 and 48 h after CIDR removal and another 27.8% during the following 24 h, giving a total of 83.5% over a 48-h period. Thus this treatment protocol offers the opportunity for fixed-time AI at 48 h if onset of estrus or ovulation is further synchronized with an injection of estradiol or GnRH 36 h after CIDR removal. In herds with estrus detection problems, the use of estrus synchronization and fixed-time AI might improve reproductive performance by eliminating the problems associated with estrus detection even though
Table 2. Reproductive performance of control cows (C group) and cows that had been synchronized with progesterone, GnRH, and PGF2α (S group) in trial 1 and trial 2. Trial 1
Total number of cows, n Number of 1st AI,1 n Conception rate to 1st AI, % Number of 2nd AI, n Conception rate to 2nd AI, % Pregnancy rate to all AI, % Nonpregnancy rate, % ISBC-AI,2 d ISBC-all,3 d
Trial 2
Combined
C
S
C
S
C
S
510 485 62.7 147 60.5 82.2 4.7 15.2 21.8
515 478 56.5a 194 67.5 86.2c 4.3 9.8b 14.4b
504 482 63.3 140 54.3 80.2 5.2 14.4 21.3
509 469 64.6 166 54.8 85.1a 5.1 8.0b 13.9b
1014 967 63.0 287 57.4 81.2 4.9 14.8 21.6
1024 947 60.5 360 61.7 85.6b 4.7 8.9b 14.1b
P ≤ 0.05 when compared with the corresponding value for the C group. P < 0.01 when compared with the corresponding value for the C group. c P < 0.10 when compared with the corresponding value for the C group. 1 Over the first 24 d for cows in the C group and over the first 6 d for cows in the S group. 2 Mean interval from the start of the breeding season to conception for cows that conceived by AI. 3 Mean interval from the start of the breeding season to conception for cows that conceived by AI or by natural mating. a b
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conception rate at the synchronized estrus may be slightly compromised (31). In trial 2, the duration of CIDR treatment was reduced from 8 to 7 d to investigate if the observed reduction in conception rate at the synchronized estrus in trial 1 could be eliminated. Results from trial 2 showed that similar conception rates were obtained in the synchronized and control cows. However, reducing the duration of progesterone treatment increased the distribution in the onset of estrus over a 3-d period. Such a wide spread in the onset of estrus pattern is not precise enough to allow fixed-time AI to achieve an acceptable conception rate. Although the precision of estrus or ovulation can be improved by an injection of estradiol or GnRH after the CIDR treatment, induction of premature ovulation has been shown to reduce conception rate (15, 31, 33). Under the seasonal dairy farming system in New Zealand, the efficiency and accuracy of estrus detection in most herds are very high (14, 42, 45). In herds with good estrus detection performance, some spread in the onset of estrus pattern may not be a major problem if the main reason for using estrus synchronization is to improve the overall reproductive performance. For large seasonal herds in which all cows are treated at the same time, less tight synchrony in the onset of estrus may be advantageous because spreading inseminations over a few days reduces the number of farm staff and AI technicians required each day and helps to minimize the likely adverse effects due to bad weather or other operational problems on a particular day. CONCLUSIONS The present study showed that onset of estrus of lactating dairy cows in seasonal herds can be successfully synchronized with progesterone, GnRH, and PGF2α. The program involving an 8-d progesterone treatment resulted in tight synchrony of onset of estrus, but reduced conception rate at the synchronized estrus. In contrast, the program involving a 7-d progesterone treatment resulted in normal conception rate at the synchronized estrus, but the synchrony was more dispersed than the 8-d program. Both programs improved reproductive performance compared with nonsynchronized control cows. When a tight synchrony is not required, the protocol used in trial 2 is preferred over that used in trial 1 because it did not reduce conception rate at the synchronized estrus. ACKNOWLEDGMENTS We thank the participating herd owners and veterinarians for their help and cooperation during the trial,
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