Administration of human chorionic gonadotropin 7 days after fixed-time artificial insemination of suckled beef cows 1
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1 Published December 4, 2014 Administration of human chorionic gonadotropin 7 days after fixed-time artificial insemination of suckled beef cows 1 C. R. Dahlen,* S. L. Bird, C. A. Martel, KC Olson, J. S. Stevenson, and G. C. Lamb 2 *Northwest Research and Outreach Center, University of Minnesota, Crookston 56716; North Central Research and Outreach Center, University of Minnesota, Grand Rapids 55744; Department of Animal Sciences and Industry, Kansas State University, Manhattan ; and North Florida Research and Education Center, University of Florida, Marianna ABSTRACT: We determined the effects of administering hcg 7 d after a fixed-time AI (TAI) on ovarian response, concentrations of progesterone, and pregnancy rates in postpartum suckled beef cows. Cows at 6 locations received 100 µg of GnRH (Fertagyl, Intervet Animal Health, Millsboro, DE) and a controlled internal drug release (CIDR) device (CIDR EAZI-Breed, Pfizer Animal Health, New York, NY), followed in 7 d by 25 mg of PGF 2α (Lutalyse, Pfizer Animal Health) and CIDR removal. At 64 h after CIDR removal, cows received an injection of GnRH and AI (d 0), and then were stratified by days postpartum and parity and assigned randomly to 2 treatments administered 7 d after TAI: 1) 1 ml of saline (saline; n = 252); or 2) 1,000 IU of hcg (Chorulon, Intervet Animal Health; n = 254). Blood samples were collected on d 21, 10, and 33 relative to TAI (d 0) at all locations, on d 7 and 68 at 5 locations, and on d 14 at 1 location to determine concentrations of progesterone. Transrectal ultrasonography was used to determine pregnancy status on d 33 and 68 at all locations, to monitor response of follicles and corpora lutea (CL) in response to treatment at 1 location (n = 106) on d 7 and 14, and to determine the number of CL present in pregnant cows on d 33 in 3 locations (n = 130). Pregnant cows had greater (P < 0.05) concentrations of progesterone at the time of treatment (d 7) compared with nonpregnant cows (3.7 ± 0.1 vs. 2.6 ± 0.2 ng/ml, respectively). On d 14, hcg-treated cows had a greater (P < 0.05) volume of luteal tissue (12.1 ± 0.5 vs. 7.3 ± 0.5 cm 3, respectively) and greater concentrations of progesterone (6.8 ± 0.4 vs. 5.4 ± 0.5 ng/ml, respectively) compared with saline-treated cows. A greater (P < 0.01) percentage of hcg-treated cows (90.6%) had multiple CL on d 14 compared with saline-treated cows (0%), and a greater percentage of pregnant cows treated with hcg (74.6%) had multiple CL on d 33 compared with salinetreated cows (3.0%). Pregnancy rates of hcg-treated cows (56.3%) tended (P = 0.07) to differ from those of saline-treated cows (50.0%). Concentrations of progesterone in pregnant hcg-treated cows were greater (P < 0.05; 7.7 ± 0.3 vs. 5.8 ± 0.3 ng/ml, respectively) on d 33 than for pregnant saline-treated cows, but were similar between treatments on d 68 (7.2 ± 0.3 vs. 6.7 ± 0.4 ng/ml, respectively). We conclude that treatment with hcg increased the volume of luteal tissue on d 14 and concentrations of progesterone on d 14 and 33 after TAI. Treatment with hcg tended to increase pregnancy rates at 5 of 6 locations from 1.1 to 27 percentage points (average = 10.2) compared with saline, but cumulative pregnancy rates determined on d 68 after TAI were similar between treatments. Key words: beef cow, human chorionic gonadotropin, luteal function, ovulation synchronization 2010 American Society of Animal Science. All rights reserved. J. Anim. Sci : doi: /jas Sincere appreciation is expressed to Bethany Funnell (North Central Research and Outreach Center, University of Minnesota, Grand Rapids) and Jamie Gardner (Department of Animal Sciences and Industry, Kansas State University, Manhattan) for assistance in data collection and laboratory analyses. The authors thank Intervet Animal Health (Millsboro, DE) for their donation of hcg (Chorulon) and GnRH (Fertagyl), and Pfizer Animal Health (New York, NY) for their donation of PGF 2α (Lutalyse) and CIDR inserts (CIDR EAZI-Breed). 2 Corresponding author: gclamb@ufl.edu Received October 20, Accepted February 25,
2 2338 Dahlen et al. Table 1. Characteristics of cows at locations where the study was conducted Item Location Mean or total No. of cows State 1 KS KS MN KS KS KS Breed 2 AN HH AN HH AN AN, SM, HH AN, SM, HH AN HH Parity 3.3 ± 0.2 y 1.4 ± 0.3 w 3.5 ± 0.2 y 2.4 ± 0.2 x 2.6 ± 0.3 x 4.8 ± 0.2 z 3.2 DPP 3 66 ± 1.6 x 90 ± 1.7 z 64 ± 1.4 x 75 ± 1.6 y 63 ± 1.9 x 72 ± 1.3 y 71 BCS ± 0.05 z 5.4 ± 0.06 z 5.5 ± 0.05 z 5.2 ± 0.05 y 4.8 ± 0.06 x 5.2 ± 0.04 y 5.3 Cycling, 5 % 91.4 z 94.1 z 41.3 w 58.2 x 69.6 y 93.3 z 74.4 w z Means within a row lacking common superscripts differ (P < 0.10). 1 KS = Kansas; MN = Minnesota. 2 AN = Angus; HH = Hereford; SM = Simmental. 3 DPP = days postpartum at the time of controlled internal drug release device (CIDR; EAZI-Breed CIDR containing 1.38 g of progesterone, Pfizer Animal Health, New York, NY) insertion. 4 BCS, 1 = emaciated, and 9 = obese (Whitman, 1975), was assessed at the time of GnRH (Fertagyl, Intervet Animal Health, Millsboro, DE) injection and CIDR insertion. 5 Percentage of cows cycling based on changes in concentrations of progesterone in blood serum collected at the time of CIDR insertion and 10 d prior. INTRODUCTION Research in the area of estrus and ovulation synchronization has produced programs that achieve pregnancy rates that meet the demands of most beef producers while handling cattle only 3 times (Lauderdale, 2009). The time and labor associated with implementing these programs and the resulting variable fertility are concerns that have limited adoption and application of AI by beef producers (National Animal Health Monitoring Service, 2009). Development of additional synchronization programs should identify methods that may further improve pregnancy rates obtained using the current protocols. Administration of hcg from 5 to 7 d after estrus or AI increased concentrations of progesterone in lactating dairy cows (Santos et al., 2001; Hanlon et al., 2005; Stevenson et al., 2007), dairy heifers (Diaz et al., 1998; Chagas e Silva and Lopes da Costa, 2005), beef cows (Nishigai et al., 2002; Machado et al., 2008), and beef heifers (Funston et al., 2005; Walker et al., 2005). Increased concentrations of progesterone have been associated with increased conceptus growth rates (Garrett et al., 1988). Interferon-τ (INF τ ), the factor associated with maternal recognition of pregnancy in cattle, is produced by the trophoblast of the growing conceptus (Demmers et al., 2001), and concentrations of INF τ are closely related (R 2 = 0.83) to embryo length (Mann et al., 2006). Increased concentrations of progesterone may result in increased conceptus growth rates and a greater proportion of pregnancies that are maintained to term. Administration of hcg has the potential to increase the fertility of cows when administered after AI by inducing formation of ancillary luteal tissue. Approximately 1 wk after estrus, a large percentage of firstwave dominant ovarian follicles ovulate in response to GnRH (Vasconcelos et al., 1999). Further, 1,000 IU of hcg was as effective as GnRH in ovulating follicles in suckled beef cows (Burns et al., 2008). The goal of this research was to determine whether administration of hcg to suckled beef cows 7 d after a fixed-time AI (TAI) could alter ovarian response, concentrations of progesterone, and increase pregnancy rates. MATERIALS AND METHODS All cows in this experiment were managed according to guidelines set forth in the Guide for the Care and Use of Agricultural Animals in Agricultural Research and Teaching (FASS, 1999), and all procedures were approved by the Institutional Animal Care and Use Committees at the University of Minnesota and at Kansas State University. Animals and Treatments Spring-bred cows from 6 locations in 2 midwestern states were used in this study. Herd size ranged from 57 to 119 cows. Mean BCS assessed at the onset of the ovulation synchronization program (scale of 1 to 9; 1 = emaciated, 9 = obese; Whitman, 1975) was 5.3, with a range of 4.0 to 7.0. Mean days postpartum was 71.3, with a range of 18 to 110 d. Mean parity was 3.2, with a range of 1 to 14. Differences existed among locations for all traits summarized except d 33 pregnancy rates (Table 1). Ovulation was synchronized in cows by administering 100 μg of GnRH intramuscularly (i.m.; 2 ml of Fertagyl, Intervet Animal Health, Millsboro, DE) and a controlled internal drug release device (CIDR; EAZI- Breed CIDR containing 1.38 g of progesterone, Pfizer Animal Health, New York, NY), followed in 7 d by 25 mg of PGF 2α i.m. (5 ml of Lutalyse, Pfizer Animal Health) and CIDR removal, followed in 64 h by TAI and a second injection of GnRH (CO-Synch + CIDR protocol; Larson et al., 2006). Cows were stratified by days postpartum, BCS, and parity before random as-
3 Human chorionic gonadotropin after artificial insemination 2339 Figure 1. Schematic diagram of the experimental protocol for suckled beef cows treated with hcg or saline 7 d after fixed-time AI (TAI). GnRH = 100 µg of intramuscular (i.m.) injection of GnRH (Fertagyl, Intervet Animal Health, Millsboro, DE); CIDR = treatment with a controlled internal drug release insert containing 1.38 g of progesterone (EAZI-Breed CIDR, Pfizer Animal Health, New York, NY); PG = 25 mg i.m. injection of PGF 2α (Lutalyse, Pfizer Animal Health); hcg = 1,000 IU i.m. injection of hcg (Chorulon, Intervet Animal Health); saline = 1 ml i.m. injection of physiological saline. signment to receive 1 of 2 treatments, 7 d after TAI: 1) 1 ml of physiological saline i.m. (n = 252), or 2) 1,000 IU of hcg i.m. (1 ml of Chorulon, Intervet Animal Health; n = 254; Figure 1). At locations 1, 2, 4, 5, and 6, exposure to live bulls (cleanup bulls) was not initiated until a minimum of 10 d after AI to ensure a detectable difference between pregnancies initiated by AI and those resulting from natural matings by cleanup bulls. At location 3, cows were visually observed a minimum of 3 times daily (at least 45 min each) for estrus beginning immediately after TAI until the completion of a 67-d breeding season. Inseminations were performed using the morningevening rule and were performed 9 to 14 h after the first detected estrus. Blood Samples and RIA Blood samples were collected in 10-mL Vacutainer tubes (BD Worldwide, Franklin Lakes, NJ) that did not contain additive, via tail venipuncture on d 21 and 10, and on the day of treatment (d 7) at 5 locations (locations 1, 2, 4, 5, and 6), on d 14 at 1 location (location 3), on d 33 at all locations, and on d 68 at 5 locations (locations 1, 2, 4, 5, and 6). Blood was refrigerated for up to 24 h after collection and centrifuged at 1,500 g for 10 to 15 min at 3 C; serum was decanted into storage vials and stored at 20 C until analyzed for concentrations of progesterone. Concentrations of progesterone in blood samples collected on d 21 and 10 were used to determine the percentage of cows cycling before initiation of the ovulation-synchronization breeding program. When either of the 2 blood samples had concentrations of progesterone 1 ng/ml, the cow was considered to be cycling (Lamb et al., 2001). Concentrations of progesterone at locations 1, 2, 4, 5, and 6 were measured via RIA (Skaggs et al., 1986). Interand intraassay CV were 10.0 and 6.2%, respectively. Repeated pool samples averaged 3.96 ± 0.39 ng/ml in 16 assays (n = 48). Concentrations of progesterone at location 3 were analyzed by RIA using progesterone kits (Coat-A-Count, Siemens Medical Solutions Diagnostics, Los Angeles, CA). The assay kit was validated for bovine serum (Kirby et al., 1997) using an assay volume of 100 μl. Assay tubes for the standard curve contained 0.01, 0.025, 0.05, 0.2, 0.5, 1, 2, and 4 ng of progesterone/tube. Assay sensitivity for a 100-μL sample was 0.1 ng/ml. Pooled samples produced intra- and interassay CV of 9.3 and 10.5%, respectively. Ultrasound of Ovarian Structures and Pregnancy Diagnosis The ovaries of cows at location 3 were examined by transrectal ultrasonography (7.5-MHz linear array transducer, Aloka 900V, Corimetrics Medical Systems Inc., Wallingford, CT) before treatment and 7 d later (7 and 14 d after TAI), and all ovarian structures were mapped to monitor changes in corpora lutea (CL) and follicles in response to treatment. The vertical and horizontal diameter of the largest follicle on each ovary and all CL were measured on d 7, and the vertical and horizontal diameter and location of all CL were measured on d 14. Volume of CL tissue was calculated using the formula V = 4/3πr 3, where r was one-half the average value for vertical and horizontal CL measurements. In cases in which CL had fluid-filled cavities, the volume of the cavity was subtracted from the total volume of the CL, resulting in a value that reflected the estimated luteal tissue volume of each CL. Progesterone per cubic
4 2340 centimeter of luteal tissue on d 14 was calculated by dividing concentrations of progesterone (ng/ml) by the total volume of luteal tissue (cm 3 ) present at the time of ovarian scan and concurrent blood collection. Because ovulation in all cows had previously been synchronized, the majority were expected to have a CL present at the time of treatment. Ovulation occurred if a new CL was detected in either ovary 7 d after treatment in the same ovarian location where a follicle was previously identified before treatment, or when a single CL was detected 7 d after treatment when no CL was present at treatment. The ovulatory follicle was defined as the largest follicle present in either ovary at treatment that was subsequently replaced by a CL detected 7 d later on the same ovary. Transrectal ultrasonography (7.5-MHz linear array transducer, Aloka 900V, at location 3 or 5.0-MHz linear array transducer, Aloka 500, at locations 1, 2, 4, 5, and 6, Corimetrics Medical Systems Inc.) was used on d 33 and 68 to determine the presence of a viable conceptus at all locations and on d 33 and to determine the number of CL in pregnant cows at locations 3, 4, and 5 (n = 130). Statistical Analyses The GENMOD procedure (SAS Inst. Inc., Cary, NC) was used to analyze all binomial data, and the GLM procedure (SAS Inst. Inc.) was used to analyze noncategorical data. Means were separated by using the least significant difference in the GLM procedure when a protected F-test (P 0.05) was detected by ANOVA. Concentrations of progesterone at the time of treatment were analyzed using the GLM procedure. The model consisted of location, cycling status, pregnancy status determined on d 33, and all 2-way interactions. Days postpartum and BCS at initiation of the breeding program were regression covariables. Effects of treatment on volume of luteal tissue and concentrations of progesterone on d 14 at location 3 were analyzed using the GLM procedure. The model consisted of treatment (saline or hcg), cycling status, pregnancy status determined on d 33, and treatment interactions with cycling status and pregnancy status. In addition, days postpartum and BCS at initiation of the breeding program were regression covariables. Pregnancy rate on d 33 and 68, pregnancy loss from d 33 to 68, and incidence of multiple CL on d 33 were analyzed using the logistic regression procedures GEN- MOD and GLM. The model included treatment (saline vs. hcg), cycling status before onset of the breeding program, location, treatment location, treatment cycling status, sire nested within location, AI technician nested within location, as well as BCS and days postpartum as regression variables. Three cows at location 3 were not included in models containing cycling status and BCS terms because 2 were missing data for cycling status and 1 was missing BCS data. Between Dahlen et al. Table 2. Pregnancy rates on d 33 and 68 after a fixedtime AI in suckled beef cows treated with saline or hcg on d 7 after AI Item d 33 and 68 after TAI, 4 cows were removed from the study and were excluded from any analyses performed using fertility data from d 68. The chi-squared analysis of SAS (FREQ procedure) was used to evaluate the effects of treatment on percentage of pregnant cows having 1 or 2 CL on d 33. Concentrations of progesterone on d 33 and 68 in pregnant cows were evaluated using the GLM procedure. The model included the effects of treatment (saline and hcg), cycling status, location, treatment interactions with location and cycling status, as well as BCS, and days postpartum as regression covariables. Fertility RESULTS Treatment, 1 % (total No. of cows) Saline hcg Pregnancy rate, d (252) x 56.3 (254) y Location (40) 51.2 (41) Location (35) 72.7 (33) Location (51) 50.0 (52) Location (41) 47.4 (38) Location (27) 62.1 (29) Location (58) 59.0 (61) Cumulative pregnancy rate, d (249) 80.2 (253) x,y Means within a row lacking common superscripts tended (P = 0.07) to differ. 1 Cows received either 1 ml of saline or 1,000 IU of hcg (Chorulon, Intervet Animal Health, Millsboro, DE) on d 7 after a fixed-time AI. Pregnancy rates on d 33 tended (P = 0.07) to be greater for cows treated with hcg (56.3%) compared with saline (50.0%; Table 2). In 5 of the 6 locations, pregnancy rates ranged from 1.1 to 27.0 percentage points (average = 10.2%) greater for cattle treated with hcg compared with saline. In contrast, no differences among treatments were detected when cumulative pregnancies were confirmed on d 68. For each whole unit increase in BCS (range 4 to 7), pregnancy rate on d 68 increased 9.9% (P < 0.05). Compared with cows that were cycling at the initiation of the breeding protocol, noncycling cows had similar pregnancy rates on d 33 but lesser pregnancy rates (P < 0.01) on d 68 (Figure 2). A treatment cycling status interaction (P < 0.05) was detected for pregnancy loss from d 33 to 68. Cows treated with hcg that were not cycling (8.8%; 3/34) had greater (P < 0.05) loss than cycling hcg-treated cows (0.9%; 1/109), whereas no difference in pregnancy loss was detected for cows treated with saline that were noncycling (3.4%; 1/29) and for salinetreated cows that were cycling (3.1%; 3/97).
5 Human chorionic gonadotropin after artificial insemination 2341 Figure 2. Pregnancy rates of cycling and noncycling cows on d 33 and 68 after fixed-time AI. x,y Means on d 68 differ (P < 0.01). Figure 3. Concentrations of progesterone on d 33 and 68 in pregnant cows treated with saline or hcg (Chorulon, Intervet Animal Health, Millsboro, DE) 7 d after fixed-time AI. x,y Means on d 33 differ (P < 0.01). Concentrations of Progesterone and CL At location 3, a total of 102 of 106 cows evaluated via ultrasound before treatment on d 7 had visible CL tissue (96.2%). Based on the appearance of new luteal structures on d 14, a greater (P < 0.01) proportion of cows ovulated in response to hcg (90.6%) than after saline (0%; Table 3). Of the cows treated with hcg that ovulated, accessory CL were present on d 14 on the ovary ipsilateral to the original CL in 56% (27/48) of cows, and on the ovary contralateral to the original CL in 44% (21/48) of cows. No differences (P = 0.11) were detected between treatments in volume of the largest CL present on d 14 on the ovary ipsilateral to the original CL observed on d 7. Although hcgtreated cows had greater (P < 0.05) total luteal tissue volume and concentrations of progesterone 7 d posttreatment, saline-treated cows had greater (P < 0.05) concentrations of progesterone per cubic centimeter of luteal tissue (Table 3). At location 3, all cows treated with hcg that developed accessory CL and became pregnant had accessory CL visible via ultrasound on d 33 (25 of 25 cows). Cows that were pregnant had greater (P < 0.01) concentrations of progesterone at the time of treatment than cows that were not pregnant. For every whole unit increase in BCS, concentrations of progesterone on d 7 increased (P < 0.05) by an average of 0.35 ± 0.15 ng/ ml. Of the cows that became pregnant, concentrations of progesterone were greater (P < 0.01) on d 33 for those treated with hcg compared with those treated with saline. This difference was no longer detectable on d 68 (Figure 3). Concentrations of progesterone in pregnant cows on d 33 were affected by BCS; for each whole unit increase in BCS, concentrations of progesterone increased by 0.66 ± 0.34 ng/ml. This relationship between BCS and progesterone, however, was not present on d 68. The proportion of pregnant cows with multiple CL present on d 33 was greater (P < 0.01) for cows treated with hcg (74.6%) compared with cows treated with saline (3.0%; Table 4). One hcg-treated pregnant cow (1.6%) evaluated on d 33 had 3 CL, and thus may have experienced a double-induced ovulation in response to hcg. In addition, a treatment location interaction was present (P < 0.05); a greater (P < 0.05) proportion of pregnant cows from location 3 (92.3%) that were treated with hcg had multiple CL compared with cows from location 4 (66.7%) and location 5 (55.5%) that were treated with hcg. Of cows treated with hcg that Table 3. Effects of treating suckled beef cows with saline or hcg 7 d after AI on ovarian dynamics and concentrations of progesterone 7 d posttreatment (d 14) Treatment 1 Item Saline hcg No. of cows Volume of luteal tissue on d 7, cm ± ± 0.51 Induced ovulation, 2 % 0.0 x 90.6 y No. of corpora lutea on d ± 0.03 x 1.9 ± 0.03 y Largest corpus luteum volume on d 14, cm ± ± 0.44 Total corpus luteum volume on d 14, cm ± 0.51 x 12.1 ± 0.48 y Progesterone on d 14, ng/ml 5.4 ± 0.46 x 6.8 ± 0.43 y Progesterone per unit of luteal tissue, 3 (ng/ml)/cm ± 0.05 x 0.58 ± 0.05 y x,y Means within a row lacking common superscripts differ (P 0.05). 1 Cows received either 1 ml of saline or 1,000 IU of hcg (Chorulon, Intervet Animal Health, Millsboro, DE) on d 7 after fixed-time AI. 2 Ovulation resulting from treatment administration 7 d after AI; includes 3 cows treated with hcg that did not have corpora lutea present at the time of treatment. 3 Concentration of progesterone on d 14 divided by total volume of luteal tissue determined via transrectal ultrasound at the time of blood collection.
6 2342 Table 4. Location and number of corpora lutea (CL) present in pregnant, suckled beef cows on d 33 after treatment with saline or hcg on d 7 after fixed-time AI No. of CL ovulated, accessory CL were present at d 14 on the ovary ipsilateral to the original CL in 56% (27/48) of cows, and on the ovary contralateral to the original CL in 44% (21/48) of cows. Fertility Treatment, 1 % (total No. of cows) Saline DISCUSSION hcg One 97.0 x (65) 25.4 y (16) Right ovary 70.1 (47) 9.5 (6) Left ovary 26.9 (18) 15.9 (10) Two or more 3.0 x (2) 74.6 y (47) Right ovary 0.0 (0) 38.1 (24) 2 Left ovary 0.0 (0) 6.3 (4) Both ovaries 3.0 (2) 30.2 (19) x,y Means within a row lacking common superscripts differ (P < 0.01). 1 Cows received either 1 ml of saline of 1,000 IU of hcg (Chorulon, Intervet Animal Health, Millsboro, DE) on d 7 after fixed-time AI. 2 One cow had 3 CL. Dahlen et al. Pregnancy rates on d 33 of the current study tended to be greater for cows treated with hcg on d 7 compared with those treated with saline. Effects of administration of hcg after AI on pregnancy rates have varied. Increased 28-, 45-, and 90-d pregnancy rates were observed when lactating dairy cows were treated with hcg on d 5 after estrus (Santos et al., 2001). In addition, administration of hcg between d 4 and 9 after AI increased conception rates, but only in 3 of 5 herds (Stevenson et al., 2007). When administered on d 6 of the estrous cycle to Japanese Black beef cattle, 1,500 IU of hcg increased pregnancy rates of frozen-thawed embryos transferred on d 7 (68 vs. 45%, respectively; Nishigai et al., 2002). In contrast, treating lactating dairy embryo transfer recipients with hcg 5 d after ovulation failed to increase d 28 conception rates of embryos transferred on d 7 (Galvão et al., 2006). No differences in pregnancy rates were observed after hcg treatment of anestrous dairy cows or beef heifers after AI compared with untreated females (Breuel et al., 1990; Funston et al., 2005; Hanlon et al., 2005). Pregnancy rates in the current study also were variable, with improvements occurring at 5 of 6 locations. Pregnancy rates of cycling and noncycling cows were similar at d 33 but were greater for cycling cows on d 68. In our previous reports (Thompson et al., 1999; Stevenson et al., 2000; Lamb et al., 2001; Larson et al., 2006), we determined that ovulation synchronization protocols that include progestogens, GnRH, or both initiate the induction of estrous cycles in noncycling females that result in pregnancies. As a result, pregnancy rates of noncycling cows after ovulation synchronization with progestogens and GnRH are similar between cycling and noncycling cows (Larson et al., 2006; Wilson et al., 2010). A large percentage of the cows that fail to become pregnant to TAI are likely noncycling cows that were not induced to resume estrous cycles, that fail to return to estrous during the subsequent 30 d, and that fail to conceive to cleanup bulls. Induction of cyclicity by the CO-Synch + CIDR protocol may also be related to BCS at initiation of the breeding season. For every unit increase in BCS, pregnancy rate on d 68 increased by 9.9%. In our previous reports we noted that an increase in BCS of a single unit resulted in an 11.5% (Larson et al., 2006) and 23% (Lamb et al., 2001) increase in the proportion of cows pregnant to AI after ovulation synchronization. In addition, the impact of inclusion of a CIDR into ovulation synchronization induced a greater percentage of noncycling cows to initiate estrous cycles and enhanced pregnancy rates when those noncycling cows were in greater body condition or had longer postpartum intervals (Lamb et al., 2001). Cows with multiple CL had greater d 28 conception rates than those having a single CL (Santos et al., 2001). Moreover, hcg-treated heifers with an accessory CL had greater pregnancy rates than those without an accessory CL (Chagas e Silva and Lopes da Costa, 2005). Ovarian Dynamics and Concentrations of Progesterone: d 7 to 14 Our hypothesis was that post-ai administration of hcg would increase concentrations of progesterone either through induction of an accessory CL or stimulation of the original CL present at the time of hcg treatment. Concentrations of progesterone in cows monitored on d 14 were 1.4 ng/ml greater in cows treated with hcg than in those treated with saline in our experiment. Increased concentrations of progesterone have been observed when hcg was administered 5 to 7 d after estrus or AI in lactating dairy cows (Santos et al., 2001; Hanlon et al., 2005; Stevenson et al., 2007), dairy heifers (Diaz et al., 1998; Chagas e Silva and Lopes da Costa, 2005), beef cows (Nishigai et al., 2002; Machado et al., 2008), and beef heifers (Funston et al., 2005; Walker et al., 2005). As expected, more cows treated with hcg had multiple CL on d 14 than those treated with saline. Two cows (3%) treated with saline having multiple CL may have double ovulated in response to the GnRH injection administered concurrent with the TAI. Likewise, a similarly small proportion of hcg-treated cows may have double ovulated before treatment. Lactating dairy cows that received hcg on d 5 after estrus had a greater number of CL present between d 11 to 16 (86%) compared with those treated with saline (23%;
7 Human chorionic gonadotropin after artificial insemination 2343 Santos et al., 2001). Accessory CL developed in 11 of 12 recipient cows treated 7 d after embryo transfer on d 7 postestrus (Nishigai et al., 2002). Lactating dairy cattle used as embryo transfer recipients were treated 5 d after GnRH-induced ovulation with hcg, resulting in 93% of cows with accessory CL compared with 1.5% of untreated cows (Galvão et al., 2006). In the present experiment, none of the cows evaluated on d 7 and 14 developed multiple induced luteal structures in response to treatment. In contrast, multiple induced luteal structures were identified in 24% of lactating dairy cows ovulating in response to treatment with GnRH or hcg between d 4 to 9 after AI (Stevenson et al., 2007) and in 25% of lactating dairy cows treated with hcg on d 5 after estrus (Galvão et al., 2006). Frequency of multiple induced ovulations after treatment with hcg on d 5 were greater in lactating dairy cows having dominant follicles 10 mm (9/17; 53%) at the time of treatment compared with cows having dominant follicles >10 mm in diameter (22/108; 20%; Galvão et al., 2006). In the current study, 7 of the cows monitored on d 7 had dominant follicles 10 mm at the time of treatment (range 8 to 10 mm), 6 cows ovulated a follicle, and none had double ovulations. Discrepancies among reports regarding the incidence of multiple ovulations may result from a greater incidence of codominant follicles and corresponding multiple ovulations in lactating dairy cattle compared with suckled beef cows. Alternatively, it could be due to the larger dose of hcg administered (3,300 IU) compared with that in the current report (1,000 IU). Total volume of luteal tissue was greater in cows treated with hcg than in cows treated with saline. Accessory CL induced with hcg were smaller than the original CL on the ovary in the study by Fricke et al. (1993). In the present study, no difference in volume of the largest CL on d 14 was detected between treatments. Dairy cows treated with hcg between d 4 and 9 after AI had greater total luteal volume and a greater change in diameter of the original CL 7 d after treatment with hcg than untreated controls (Stevenson et al., 2007). Area and volume of the largest CL and original CL area also were increased by treatment with hcg on d 5 after estrus (Santos et al., 2001) or induced ovulation (Galvão et al., 2006). In addition, diameter of the original CL, induced CL, and concentrations of progesterone were greater in crossbred beef heifers treated with hcg than in those treated with GnRH or LH (Binelli et al., 2001). Although the total volume of luteal tissue and concentrations of progesterone were increased in the current study, progesterone production per unit of luteal tissue (ng per ml/cm 3 ) was less in cows treated with hcg than with saline. Although not reported by Santos et al. (2001), calculations made using their data indicated that both primiparous (3.2 vs. 3.8 ng per ml/cm 3, for hcg and saline-treated cows, respectively) and multiparous (1.3 vs. 1.6 ng per ml/cm 3, for hcg and saline-treated cows, respectively) dairy cows treated with hcg had decreased concentrations of progesterone per unit of luteal tissue compared with saline-treated cows. Therefore, although hcg may induce an increased quantity of luteal tissue, progesterone secretion did not increase at the same rate. Similarly, luteal tissue from cows treated with hcg had less basal hormone and LH-induced in vitro secretion of progesterone than produced by luteal tissue from untreated cows (Veenhuizen et al., 1972; Fricke et al., 1993). Of the cows treated with hcg that ovulated, accessory CL were present on d 14 on the ovary ipsilateral to the original CL in 56% (27/48) of cows and on the ovary contralateral to the original CL in 44% (21/48) of cows. These proportions are similar to those found in dairy heifers when 56% (52/93) developed CL ipsilateral to the original CL and 44% (41/93) developed accessory CL contralateral to the original CL after treatment with hcg (Chagas e Silva and Lopes da Costa, 2005). The proportion of lactating dairy cattle receiving hcg or GnRH 4 to 9 d after AI that had accessory CL develop on the ovary ipsilateral to the original CL was 32%, the proportion contralateral was 41%, and 28% developed accessory CL on both ovaries (Stevenson et al., 2007). Cows from 5 locations that were pregnant on d 7 (n = 213) had greater concentrations of progesterone than those that were not pregnant (n = 190). Concentrations of progesterone were greater on d 6 or 7 in pregnant, lactating dairy cows than in those that were not pregnant (Mann et al., 1999; Demetrio et al., 2007). In contrast, beef heifers that were not pregnant had greater concentrations of progesterone on d 7 compared with those that were pregnant; moreover, pregnant heifers had greater concentrations of progesterone compared with nonpregnant heifers beginning only on d 17 (Breuel et al., 1989). CL Dynamics and Concentrations of Progesterone: d 33 to 68 Cows that became pregnant and were treated with hcg 7 d after AI had greater concentrations of progesterone on d 33 compared with those treated with saline; however, the effects of treatment were temporary because differences did not persist to d 68. Effects of hcg stimulation of luteal cells, the additional progesterone production, or both of the induced accessory CL that were first observed on d 7 after treatment apparently diminished between d 33 and 68 of pregnancy. Pregnant Japanese Black embryo recipients that were treated with 1,500 IU of hcg on d 6 had greater concentrations of progesterone when evaluated between d 40 to 50 after embryo transfer (Nishigai et al., 2002). Treatment of lactating dairy cows with hcg at the time of positive pregnancy (d 29 to 42 after AI) determination failed to have greater concentrations of progesterone compared with those treated with saline (Stevenson et al., 2008).
8 2344 Although concentrations of progesterone were greater in cows with induced luteal structures during the first 2 wk after treatment at pregnancy determination (d 29 to 42), no differences were present 4 wk after treatment (Stevenson et al., 2008). Administration of 100 mg of progesterone from d 1 to 4 of pregnancy increased concentrations of blood progesterone and fetal development compared with untreated females (Garrett et al., 1988). In addition, supplemental progesterone via CIDR insert increased embryo development and INF τ secretion when administered from d 5 to 9 after AI, but not when administered from d 12 to 16 (Mann et al., 2006). Previous reports indicated that concentrations of progesterone were elevated within 2 d of hcg administration and were initially ascribed to the effects of hcg on existing luteal tissue and later to supplemental progesterone from the induced CL (Lewis et al., 1990; Fricke et al., 1993). In the current study, concentrations of progesterone were elevated after treatment with hcg from at least d 14 after AI until d 33, but not until d 68 after TAI. This sustained increase in concentrations of progesterone that occurred from maternal recognition of pregnancy until early postimplantation stages of pregnancy may result in increased pregnancy survival. Of the cows at location 3 treated with hcg that developed accessory CL and became pregnant, accessory CL were visible by transrectal ultrasound on d 33 in all cases monitored (25 of 25 cows). When lactating dairy cattle received hcg 5 d after estrus and had double ovulations in response to treatment (determined on d 14), 7% regressed 1 CL by d 28 (Santos et al., 2001). In addition, when lactating dairy cows were treated with hcg at the time of pregnancy diagnosis (29 to 42 d), 39% experienced regression of induced luteal structures by 4 wk posttreatment (57 to 70 d; Stevenson et al., 2008). From d 28 to 42, a total of 62% (18 of 29) of Holstein heifers that developed accessory CL contralateral to the original CL after treatment with hcg experienced regression of the induced CL, whereas no heifers experienced regression of the accessory CL during this period that developed on the ovary ipsilateral to the original CL (Chagas e Silva and Lopes da Costa, 2005). In the present study, concentrations of progesterone were increased in pregnant cows after treatment with hcg, and treatment with hcg tended to increase pregnancy rates. Pregnant cows had greater concentrations of progesterone on d 7 after AI than cows that were not pregnant. Therefore, we conclude that treatment with hcg increased the volume of luteal tissue on d 14 and concentrations of progesterone on d 14 and 33 after TAI. Treatment with hcg tended to increase pregnancy rates, improving pregnancy rates at 5 of 6 locations from 1.1 to 27 percentage points (average = 10.2) compared with saline; however, cumulative pregnancy rates determined on d 68 after TAI were similar between treatments. Dahlen et al. LITERATURE CITED Binelli, M., W. W. Thatcher, R. Mattos, and P. S. Baruselli Antiluteolytic strategies to improve fertility in cattle. Theriogenology 56: Breuel, K. F., J. C. Spitzer, and D. M. Henricks Systemic progesterone concentration following human chorionic gonadotropin administration at various times during the estrous cycle in beef heifers. J. Anim. Sci. 67: Breuel, K. F., J. C. Spitzer, C. E. Thompson, and J. F. Breuel First-service pregnancy rate in beef heifers as influenced by human chorionic gonadotropin administration before and/or after breeding. Theriogenology 34: Burns, M. G., B. S. Buttrey, C. A. Dobbins, C. A. Martel, K. C. Olson, G. C. Lamb, and J. S. 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9 Human chorionic gonadotropin after artificial insemination 2345 gonadotropin-releasing hormone, prostaglandin F 2α, and progesterone. J. Anim. Sci. 84: Lauderdale, J. W Contributions in the Journal of Animal Science to the development of protocols for breeding management of cattle through synchronization of estrus and ovulation. J. Anim. Sci. 87: Lewis, G. S., D. W. Caldwell, C. E. Rexroad Jr., H. H. Dowlen, and J. R. Owen Effects of gonadotropin-releasing hormone and human chorionic gonadotropin on pregnancy rate in dairy cattle. J. Dairy Sci. 73: Machado, R., M. A. Bergamaschi, R. T. Barbosa, C. A. de Oliveira, and M. Binelli Ovarian function in Nelore (Bos taurus indicus) cows after post-ovulation hormonal treatments. Theriogenology 69: Mann, G. E., M. D. Fray, and G. E. Lamming Effects of time of progesterone supplementation on embryo development and interferon-τ production in the cow. Vet. J. 171: Mann, G. E., G. E. Lamming, R. S. Robinson, and D. C. Wathes The regulation of interferon-τ production and uterine hormone receptors during early pregnancy. J. Reprod. Fertil. Suppl. 54: National Animal Health Monitoring Service Part II. Reference of beef cow-calf management practices in the United States, Pages Natl. Anim. Health Monit. Serv., Fort Collins, CO. Nishigai, M., H. Kamomae, T. Tanaka, and Y. Kaneda Improvement of pregnancy rate in Japanese Black cows by administration of hcg to recipients of transferred frozen-thawed embryos. Theriogenology 58: Santos, J. E. P., W. W. Thatcher, L. Pool, and M. W. Overton Effects of human chorionic gonadotropin on luteal function and reproductive performance of high-producing lactating Holstein dairy cows. J. Anim. Sci. 79: Skaggs, C. L., B. V. Able, and J. S. Stevenson Pulsatile or continuous infusion of luteinizing hormone-releasing hormone and hormonal concentrations in prepubertal heifers. J. Anim. Sci. 62: Stevenson, J. S., M. A. Portaluppi, D. E. Tenhouse, A. Lloyd, D. R. Eborn, S. Kacuba, and J. M. DeJarnette Interventions after artificial insemination: Conception rates, pregnancy survival, and ovarian response to gonadotropin-releasing hormone, human chorionic gonadotropin, and progesterone. J. Dairy Sci. 90: Stevenson, J. S., K. E. Thompson, W. L. Forbes, G. C. Lamb, D. M. Grieger, and L. R. Corah Synchronizing estrus and (or) ovulation in beef cows after combinations of GnRH, norgestomet, and prostaglandin F 2α with or without timed insemination. J. Anim. Sci. 78: Stevenson, J. S., S. M. Tiffany, and E. Inskeep Maintenance of pregnancy in dairy cattle after treatment with human chorionic gonadotropin or gonadotropin-releasing hormone. J. Dairy Sci. 91: Thompson, K. E., J. S. Stevenson, G. C. Lamb, D. M. Grieger, and C. A. Löest Follicular, hormonal, and pregnancy responses of early postpartum suckled beef cows to GnRH, norgestomet, and PGF 2α. J. Anim. Sci. 77: Vasconcelos, J. L. M., R. W. Silcox, G. J. M. Rosa, J. R. Pursley, and M. C. Wiltbank Synchronization rate, size of the ovulatory follicle, and pregnancy rate after synchronization of ovulation beginning on different days of the estrous cycle in lactating dairy cows. Theriogenology 52: Veenhuizen, E. L., J. F. Wagner, and L. V. Tonkinson Corpus luteum response to 6-chloro Δ 6-17 acetoxyprogesterone and hcg in the cow. Biol. Reprod. 6: Walker, R. S., P. D. Burns, T. E. Engle, G. E. Sides, and D. D. Zalesky Effects of human chorionic gonadotropin administration on artificial insemination pregnancy rates in beef heifers. Prof. Anim. Sci. 21: Whitman, R. W Weight changes, body condition and beef-cow reproduction. PhD Diss. Colorado State Univ., Fort Collins. Wilson, D.J., D. A. Mallory, D. C. Busch, N. R. Leitman, J. K. Haden, D. J. Schafer, M. R. Ellersieck, M. F. Smith, and D. J. Patterson Comparison of short-term progestin-based protocols to synchronize estrus and ovulation in postpartum beef cows. J. Anim. Sci. 88: doi: /jas
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