Animal Reproduction Science 82–83 (2004) 479–486 The use of hormonal treatments to improve reproductive performance of anestrous beef cattle in tropical climates P.S. Baruselli a,∗ , E.L. Reis a , M.O. Marques a , L.F. Nasser a , G.A. Bó b a b Departamento de Reprodução Animal, FMVZ-USP, Rua Prof. Orlando Marques de Paiva, 87, CEP 05508-000, Sao Paulo, SP, Brazil Instituto de Reproducción Animal Córdoba, J.L. de Cabrera 106, X5000GVD Córdoba e Facultad de Ciencias Agropecuarias, Universidad Católica de Córdoba, Argentina Abstract Most of the world’s bovine herd is found in tropical regions. Bos indicus predominates, due to their adaptation to the climate and management conditions. Anestrous is the main factor that negatively affects reproductive performance of animals bred in these regions of the globe. Several factors affect postpartum anestrous, including suckling and maternal-offspring bond, and pre- and postpartum nutritional status. The short duration of estrus and the tendency to show estrus during the night, greatly affect the efficiency of artificial insemination (AI) programs in B. indicus cattle managed in tropical areas. Several restricted suckling or weaning procedures (temporary or permanent), and hormonal treatments have been used to induce ovulation and cyclicity in postpartum cows. Most hormonal treatments are based on progesterone/progestogen (P4) releasing devices associated with estradiol benzoate (EB), or a combination of GnRH/PGF2␣ /GnRH (Ovsynch). Treatments with GnRH/PGF2␣ /GnRH has presented inconsistent results, probably due to the variable number of cows in anestrous. Treatments using P4 devices and EB have resulted in apparently more consistent results than Ovsynch programs in B. indicus cattle; however, pregnancy rates are low in herds presenting high anestrous rates and moderate to low body condition. The addition of an eCG treatment at the time of device removal, which increased plasma progesterone concentrations and pregnancy rates in anestrous postpartum suckled B. indicus cows, may be useful to improve reproductive performance of beef cattle in tropical climates. © 2004 Elsevier B.V. All rights reserved. Keywords: Anestrous; B. indicus; Progesterone; Pregnancy rate; Postpartum; Ovarian activity ∗ Corresponding author. E-mail address: barusell@usp.br (P.S. Baruselli). 0378-4320/$ – see front matter © 2004 Elsevier B.V. All rights reserved. doi:10.1016/j.anireprosci.2004.04.025 480 P.S. Baruselli et al. / Animal Reproduction Science 82–83 (2004) 479–486 1. Introduction Most of the bovine herds are located in tropical regions, characterized by high pluviometric indices and high temperatures, which provide favourable conditions for forage growth and low-cost beef production. In the tropics, Bos indicus animals predominate, due to their greater adaptation to high temperatures and humidity. A female, when kept under favorable conditions, has the potential to produce one calf a year, with a 12-month calving interval (Stagg et al., 1995). To achieve this calving index, cows must conceive within 75–85 days after parturition. However, cows bred in tropical conditions present a high incidence of postpartum anestrous, that increases the calving to conception interval and, as a consequence, negatively affects reproductive performance. Ruiz-Cortez and Olivera-Angel (1999) observed that B. indicus suckled cows kept in natural pasture conditions in Colombia re-established their cyclicity from 217 to 278 days after calving, resulting in a 17–19 month calving interval. This demonstrates that anestrous is one of the main factor that interferes with the productivity of cattle reared in tropical regions. Thus, techniques used to hasten the re-establishment of cyclicity in the postpartum period may have a great impact on beef production worldwide. The objectives of this review are to discuss the impact of anestrous on reproductive efficiency of beef cattle bred in tropical conditions and to present hormonal treatments that may enhance reproductive performance by shortening the postpartum anestrous and enable the application of artificial insemination (AI). 2. Behavior and reproductive physiology in Bos indicus cows Reports from different parts of the world indicate low service rates in cattle submitted to AI, are due to both mistakes in heat detection or a high incidence of anestrous. This low service rates to service is even more evident in B. indicus herds, which present reproductive behavior different from that of Bos taurus, with a short duration of estrus, and high rates of estrus expression during the night (Galina et al., 1996; Pinheiro et al., 1998). Mizuta (2003), using radiotelemetry, demonstrated that the mean duration of standing estrus was 3.4 h shorter in Nelore cows (12.9 h) compared to that in Angus cows (16.3 h), while Nelore × Angus crossbred cows (12.4 h) were not different from purebred Nelore cows. Other trials using radiotelemetry confirmed that crossbred B. indicus females present a shorter duration of estrus (approximately 10 h; Bertam Membrive, 2000; Rocha, 2000), and found a greater mounting activity during the night (56.6%). These findings are in agreement with the results obtained by Pinheiro et al. (1998), who reported 53.8% of the estrus expression at night with 30.7% of these beginning and ending during the night. Several studies characterized follicular-wave dynamics in B. indicus cattle (reviewed by Bó et al., 2003). In general, characteristics of follicular growth and dominance were similar to those in B. taurus; however, B. indicus cattle seemed to have smaller diameter of the dominant follicle and corpus luteum (CL) relative to those of B. taurus cattle. Randel (1989) observed that the CL of pure and crossbred zebu females have less P4 per gram of luteal tissue than that in B. taurus, and Segerson et al. (1984) reported that serum P4 concentrations were lower in B. indicus compared to that in B. taurus. P.S. Baruselli et al. / Animal Reproduction Science 82–83 (2004) 479–486 481 3. Postpartum anestrous At the end of pregnancy, the hypothalamic-pituitary axis responds to a negative feedback effect of placental and ovarian steroids by suppressing FSH release and accumulating this hormone in the anterior pituitary and depleting LH stores (reviewed by Yavas and Walton, 2000b). Following parturition, there is a dramatic increase in FSH that is followed by the emergence of the first follicular wave (2–7 days postpartum, (reviewed by Wiltbank et al., 2002). Follicular dominance was observed from 10 to 21 days postpartum. However, the first dominant follicle may not be released and may become atretic, leading to the subsequent growth of new follicular waves (Murphy et al., 1990; Stagg et al., 1995). Data indicate that it is LH, and not FSH, that is the limiting hormone for the onset of postpartum ovarian activity. After LH stores are re-established between 15 and 30 days postpartum (Yavas and Walton, 2000a), nutritional status and suckling may be the most important factors that inhibit postpartum ovulation in beef cows. Poor nutrition is a recognized cause of reduced fertility in cattle grazing in subtropical/tropical areas (Bó et al., 2003). Investigations on postpartum reproduction in cattle indicate that body condition score (BCS) is a useful indicator of energy status and rebreeding potential (DeRouen et al., 1994). Other studies also demonstrate the effect of BCS on ovarian cyclicity and pregnancy rates in beef cows (D’occhio et al., 1990; Viscarra et al., 1998). Rasby et al. (1992) reported that nutrition restriction has a negative influence on LH release while Rekwot et al. (2004) have shown that cows supplemented with 600 g of cotton seed daily resumed cyclicity earlier than the controls (136 ± 8 days versus 107 ± 5 days, P < 0.05). We have also demonstrated a significant effect of BCS on conception rates in animals submitted to fixed-time AI (FTAI) in cows bred in Brazil and in Argentina (Baruselli et al., 2003a; Cutaia et al., 2003b), with a 2.5 score on a scale of 1–5, being the minimum acceptable BCS for successful estrus synchronization in B. indicus cattle. After re-establishment of LH stores in the anterior pituitary, maternal-offspring bond increases postpartum anestrous due to the negative effect on LH release (Williams et al., 1996), which, in turn, affect the final maturation and ovulation of the dominant follicle. Suckling is not the only factor responsible for the effect described, but olfaction, vision, touch and auditory stimulus (between calf and cow) may also lead to anestrous (Williams et al., 1996). As the postpartum period proceeds, the negative effect of suckling becomes less intense and cows eventually ovulate and begin to cycle (Stahringer et al., 1994). Restricted suckling or calf removal increases LH pulse frequency and stimulates follicular growth and ovulation in cows >30 days postpartum (Yavas and Walton, 2000a). Henao et al. (2000) observed that duration of postpartum anestrous in suckled Brahman cows is longer than that in non-suckling cows (64.0 ± 4.8 days versus 34.8 ± 5.8 days, P < 0.05). When calf removal was performed for 96 h in primiparous zebu × Holstein cows, Soto Belloso et al. (2002) reported a shorter calving to first service interval (151.2±8.4 days) than that in cows in the control group in which calves were allowed to suckle (186.8 ± 7.3 days; P < 0.05). Recently, Barreiros et al. (2003) have shown a 22% increase in pregnancy rate after calf removal, between P4 device removal and FTAI (54 h) in B. indicus cows (n = 148). These results demonstrated the benefits of this technique in postpartum cattle treated with P4 releasing devices. 482 P.S. Baruselli et al. / Animal Reproduction Science 82–83 (2004) 479–486 4. Hormonal treatments to improve the reproductive performance of anestrous beef cattle The commonly used treatments for the re-establishment of postpartum ovarian cyclicity, include the insertion of P4 releasing devices for 5–10 days. The P4 releasing devices maintain plasma concentrations of P4 for a given period of time. As P4 concentrations reach sub-luteal levels during treatment, there is an increase in LH pulse-frequency, leading to follicular growth which, in turn, prevents atresia of the dominant follicle (Stock and Fortune, 1993; Savio et al., 1993). This mechanism enables the growth and maturation of the dominant follicle capable of ovulation, even in anestrous animals (Rhodes et al., 2002). The P4 released by the devices prevents the formation of a short-lived CL (Breuel et al., 1993; Rivera et al., 1998). Thus, ovulation preceded by P4 treatment leads to normal CL activity and enables the development and maintenance of pregnancy (Wiltbank et al., 2002). Using syncro-mate-B implants, Soto Belloso et al. (2002) decreased the interval between calving and first estrus from 186.8±7.3 days (control) to 145.2±8.5 days (treated animals), without compromising conception rates (62.5% control versus 67.7% treated) in B. indicus × B. taurus crossbred primiparous cows. In Brazil, our research group compared different FTAI protocols that employ progesterone/progestogen releasing devices (CIDR, n = 100 or Crestar, n = 103) and the “Ovsynch” protocol (n = 100) in suckled Brangus cows (69.7 ± 22.1 days postpartum). Treatments were set up so that the FTAI coincided with the first day of the breeding season (Baruselli et al., 2002). A group of cows served as control (n = 94) and were not synchronized for FTAI. After FTAI, all animals were kept together in a breeding scheme that consisted of 45 days of monitoring for estrus detection and AI 12 h later and a 45-day exposure period with clean up bulls, to complete a 90-day breeding season (BS). Table 1 shows that pregnancy rates in cows treated with CIDR and Crestar were superior to those treated with the Ovsynch protocol. The low conception rate in the Ovsynch protocol group raises doubts on the efficacy of using it in beef cows in tropical regions. Other trials have confirmed that Ovsynch protocol yields low conception rate in beef herds showing high percentage of anestrous (Barros et al., 2000; Fernandes et al., 2001; Diskin et al., 2002). Animals treated with P4 devices also showed increased service rates during the first 45 days of the breeding season compared to the controls (Table 1). Treatments with P4 led to a Table 1 Reproductive performance of beef Brangus cows treated with CIDR-B, Crestar or Ovsynch and fixed-time artificial insemination (FTAI) at the beginning of the breeding season (adapted from Baruselli et al., 2002) Group Control CIDR Crestar Ovsynch First day of breeding season (BS) Pregnancy rate to FTAI (%) – 52.0 (52/100) a 42.7 (44/103) a 15.0 (15/100) b Monitoring (45-day) period in BS (estrus detection and AI) Service rate (%) 23.4 (22/94) c 45.8 (22/48) d 44.1 (26/59) d 32.9 (28/85) cd Conception rate (%) 81.8 (18/22) 68.2 (15/22) 80.8 (21/26) 82.1 (23/28) Values with different letters (a–g) differ in the same columns (P < 0.01). 90-day of BS (AI + bull) Pregnancy rate (%) 19.1 (18/94) e 67.0 (67/100) f 63.1 (65/103) f 38.0 (38/100) g Pregnancy rate (%) 80.9 (76/94) 79.0 (79/100) 88.3 (91/103) 85.0 (85/100) P.S. Baruselli et al. / Animal Reproduction Science 82–83 (2004) 479–486 483 greater number of pregnancies after AI (FTAI+AI 12 h after estrus), in addition to improving the reproductive performance and increasing the number of pregnant animals at the beginning of the breeding season. These results confirm those of Fike et al. (1997), on the effect of P4+E2 treatment on the induction of cyclicity in B. taurus cows in postpartum anestrous. Another alternative to increase pregnancy rates in FTAI programs in B. indicus cattle in anestrous may be the addition of eCG at the time of removal of the P4 releasing devices (reviewed in Bó et al., 2003). Treatment with eCG has been shown to increase pregnancy rates in herds of postpartum suckled cows with high incidence of anestrous (reviewed in Bó et al., 2003). Three recent studies evaluated the effect of eCG at the time of P4 device removal, in postpartum suckled cows FTAI (Cutaia et al., 2003a; Baruselli et al., 2003b). The breeds tested involved suckled Braford, Nelore and crossbred Nelore and the cows were 60–90 days postpartum with a BCS of 1.5–2.5 (1–5 scale). Treatments consisted of insertion of a P4 device (PRID, Sanofi, France, CIDR-B, Pfizer or DIB, Syntex, Argentina) and 2 mg EB i.m. on Day 0. On Day 8, P4 devices were removed and all cows received PGF2␣ . Cows in the eCG groups also received 400 IU eCG on Day 8 (Novormón, Syntex, Argentina). All cows received 1 mg EB i.m. on Day 9 and were FTAI 52–56 h after P4 device removal. Ovarian activity was estimated by rectal palpation or ultrasonography on Day 0, and cows were classified: as those with a CL, those with medium to large follicles (≥8 mm in diameter), and those with ovaries containing no detectable structures (i.e. small follicles, <8 mm in diameter). The overall pregnancy rate was higher in cows treated with eCG than in the controls. The over all increase was mainly due to the increased pregnancy rate in cows with medium or small follicles at the beginning of the experiment (Table 2). In a follow-up study, we recently evaluated the effect of eCG treatment at the time of P4 device removal on follicular dynamics, ovulation and plasma P4 concentrations in 50 Table 2 Pregnancy rates in postpartum Bos indicus cows treated with progesterone (P4) releasing devices and EB, with or without 400 IU eCG at device removal (Day 8) (adapted from Cutaia et al., 2003a and Baruselli et al., 2003b) Breed Ovarian statusa Braford CL Medium follicles Small follicles Nelore Crossbred Nelore Overall Group EB 5/15 (33.3%) 7/24 (29.1%) 3/17 (17.6%) a Group eCG + EB 9/26 (34.6%) 6/18 (33.3%) 7/18 (38.8%) b Total 15/56 (26.7%) 22/62 (35.5%) CL Follicles ≥8 mm Follicles <8 mm 15/27 (55.5%) 22/64 (34.4%) c 5/17 (29.4%) e 16/25 (64.0%) 29/58 (50.0%) d 13/23(56.5%) f Total 42/108 (38.9%) a 58/106 (54.7%) b CL Medium follicles Small follicles 12/26 (46.1%) 23/48 (47.9%) 9/22 (40.9%) 16/26 (59.3%) 25/45 (55.5%) 17/27 (63.9)% Total 44/96 (46.8%) a 58/98 (59.1%) b 101/260 (38.8%) a 138/266 (51.9%) b Percentages within a row with different letters differ (a, b, P < 0.05; c, d, P < 0.06; e, f, P < 0.08). a Ovarian status was estimated by rectal palpation in Braford and crossbred Nelore cows and by ultrasonography in Nelore cows. 484 P.S. Baruselli et al. / Animal Reproduction Science 82–83 (2004) 479–486 Table 3 Effect eCG (400 IU) treatment at the time of removal of a P4 device on ovulation rate, size of the dominant ovulatory follicle and the resulting CL area, and plasma P4 concentrations 12 days after ovulation in crossbred Bos indicus suckled cows (adapted from Marques et al., 2003) eCG (25) No eCG (25) Ovulation rate (%) Time of ovulation (h) Maximum diameter of DF (mm) CL area (cm2 ) P4 total (ng/mL) P4 in cows that ovulated (ng/mL) 76.0 (19/25) 60.0 (15/25) 74.2 ± 4.0 78.0 ± 3.1 12.55 ± 0.36 12.50 ± 0.46 1.93 ± 0.05 1.82 ± 0.06 8.6 ± 0.9 a 4.5 ± 0.7 b 8.6 ± 0.4 a 6.4 ± 0.5 b Means in the same column with different letters (a, b) differ significantly (P < 0.05). crossbred B. indicus primiparous suckled cows (Marques et al., 2003). Table 3 clearly shows that eCG treatment increased plasma P4 concentrations 12 days after the termination of treatment, without significantly increasing the diameter of the ovulatory dominant follicle and the area of the CL measured by ultrasonography. It has been suggested recently that cows in anestrous treated with the current FTAI protocols may ovulate smaller follicles that produce little P4 to alter synthesis or release of uterine PGF2␣ or compromise pregnancy recognition and establishment (Macmillan et al., 2003). Our data indicate that treatment using eCG increases P4 production by the CL and may be an alternative to improve the reproductive performance of cows in anestrous, synchronized for FTAI. 5. Summary and conclusion The adaptation of B. indicus cattle to tropical environments has led to its widespread distribution around the world. However, the successful application of AI in B. indicus cattle not only has to overcome the problem of estrus detection but also has to deal with the problem of nutritionally and suckling-induced anestrous. The incorporation of FTAI protocols, like those discussed above, may reduce the problem of estrus detection and provide the possibilities for the application of FTAI in postpartum cows. Results of studies presented in this review suggest that treatments using P4 releasing devices and EB may improve reproductive performance in suckled B. indicus cows due to their beneficial effect on LH pulse frequency, follicle growth and ovulation. Furthermore, the use of eCG at the time of P4 releasing device removal in a FTAI program improved the pregnancy rates, and its effect was more evident in cases with more pronounced anestrous condition. These treatments may facilitate the application of genetic improvement programs more efficiently in herds under tropical conditions. 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