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Revista mexicana de ciencias pecuarias
versión On-line ISSN 2448-6698versión impresa ISSN 2007-1124
Rev. mex. de cienc. pecuarias vol.11 no.3 Mérida jul./sep. 2020 Epub 05-Feb-2021
https://doi.org/10.22319/rmcp.v11i3.4828
Articles
Effect of follicular replacement (GnRH) and bovine somatotropin (bST) on the fertility of dairy cows exposed to heat stress
a Universidad Autónoma de Zacatecas. Unidad Académica de Medicina Veterinaria y Zootecnia. El Cordovel, General Enrique Estrada, Zacatecas, México.
b Universidad Autónoma de Ciudad Juárez. Instituto de Ciencias Biomédicas. Departamento de Ciencias Veterinarias. Ciudad Juarez, Chihuahua, Mexico.
c Universidad Autónoma de Baja California. Instituto de Ciencias Agrícolas. Mexicali, Baja California, Mexico.
d Universidad Nacional Autónoma de México. Facultad de Medicina Veterinaria y Zootecnia. Departamento de Reproducción. Ciudad Universitaria, Ciudad de México, México.
Three reproductive protocols were evaluated: 1) PG: injection of PGF2α on d-50 postpartum and insemination (AI) based on estrus detection. 2) OVS (Ovsynch: d 0, GnRH; d 7, PGF2α; d 9, GnRH; d 10, AI); 3) ROV (GnRH + Ovsynch: d- 7, GnRH; d 0, GnRH; d 7 PGF2α; d 9, GnRB; d 10, AI). In addition, the effect of somatotropin (bST) to AI, on fertility at first postpartum service (FERT), and pregnancy rate at 99 d postpartum (PP) FERT was similar in ROV and OVS (36.2 vs 36.6 %) (P>0.05); and higher than PG (27.3 %) (P<0.05). Likewise, FERT was similar with and without bST (36.2 vs 30.6 %, P>0.05). PG and without bST (22.5 %) was lower than OVS with (38.5 %) and without bST (33.7 %), as well as than ROV with (37.0 %) and without bST (36.1 %), and PG with bST (32.9 %). The pregnancy rate at 99 d was: OVS (60.6 %); ROV (54.3 %), higher than PG group (46.8 %) (P>0.05). OVS with (64.7 %) and without bST (56.5 %) and ROV without bST were higher than PG without bST (41.1 %, P<0.05). In conclusion, GnRH before Ovsynch (ROV) and bST at AI did not increase fertility at the first service in Holstein cows under heat stress. OVS and ROV increased fertility of first service postpartum and pregnancy rate to 99 d postpartum. Somatotropin increased fertility of first postpartum service only in PG treated cows.
Key words Dairy cow; Ovsynch; Somatotropin; heat stress; GnRH
Tres protocolos reproductivos fueron evaluados: 1) PG: inyección de PGF2α en el día 50 posparto e inseminación (IA) en base a detección del estro. 2) OVS (Ovsynch: día 0, GnRH; día 7, PGF2α; día 9, GnRH; día 10, IA); y 3) ROV (GnRH + Ovsynch: día- 7, GnRH; día 0, GnRH; día 7, PGF2α; día 9, GnRH; día 10, IA). Además, el efecto de la somatotropina (bST) a la IA, sobre la fertilidad al primer servicio posparto (FERT), y la tasa de preñez a 99 días posparto (PP). FERT fue similar en ROV y OVS (36.2 vs 36.6 %) (P>0.05); y mayor a PG (27.3 %) (P<0.05). Igualmente, FERT fue similar con bST y sin bST (36.2 vs 30.6 %, P>0.05). PG y sin bST (22.5 %) fue menor que OVS con (38.5 %), y sin bST (33.7 %); y que ROV con bST (37.0 %) y sin bST (36.1 %); y PG con bST (32.9 %) (P<0.05). La tasa de preñez a 99 días PP fue: OVS (60.6 %); ROV (54.3 %), superior al grupo PG (46.8 %) (P<0.05). OVS con bST (64.7 %), y sin bST (56.5 %), y ROV sin bST fueron mayores que PG sin bST (41.1 %, P<0.05). En conclusión, GnRH previo al Ovsynch (ROV) y la bST al momento de la IA no incrementaron la fertilidad del primer servicio en vacas Holstein en estrés calórico. OVS y ROV incrementaron la fertilidad del primer servicio posparto y la tasa de preñez a 99 días posparto. La somatotropina incrementó la fertilidad del primer servicio posparto solo en vacas tratadas con PG.
Palabras clave: Vaca lechera; Ovsynch; Somatotropina; Estrés calórico; GnRH
Introduction
Heat stress (HS) compromises the estrous non-return rates1,2 and conception rates of dairy cows1-6. Ovsynch protocols have increased the ovulation rate7,8, the diameter of the ovulatory follicle8, the fertility at first service8-13 and the accumulated pregnancy rate at 120 d post-partum in high production dairy cows9-11,14. Injection of a luteolytic (i.e. prostaglandin F2α or PG) prior to Ovsynch7,12 increases the ovulation rate of a follicle suitable for fertilization by more than 40 %7, and the percentage of cows with higher levels of circulating progesterone 3 d after beginning Ovsynch12. The intravaginal insertion of a progesterone releasing device (PRD) increased the conception rate compared to cows that only receive Ovsynch12,13. However, under environmental conditions of HS, reproductive programs may be less efficient than under thermal comfort8,12,14,15. Double Ovsynch treatment has increased fertility by 10 %16. Several studies have determined that even though the fertility of in vitro fertilized oocytes are similar in winter and in the summer17, the percentage of embryos that reached the blastocyst stage is compromised when using oocytes collected during the summer17,18, especially in repeating cows17. Holstein cows in full lactation19 and non-lactating cows20 exposed to heat stress during the summer19, or during a follicular cycle20, show a decrease in the number of healthy follicles20, in the quality of the ovarian cluster19, and in embryonic development18-20. Follicle replacement is important for eliminating developed and affected follicles and is promoted with repeated GnRH treatments or by frequent aspiration of follicles 3 to 7 mm19 or larger than 5 mm20, and for generating the development of better-quality follicles and a higher percentage of embryos developed in vitro to the blastocyst stage. Follicle exchange prior to Ovsynch21,22 did not improve fertility at the first service21,22, but it did improve fertility in cows with uterine problems and low body condition21.
On the other hand, bovine somatotropin (bST) has been used in Holstein cows for its beneficial effect in increasing milk production23-26. It was considered that this increase in milk production could have a detrimental effect on the reproduction of the dairy cows. Treatment with 500 mg bST from 61 to 63 ds in milk and with repeated applications of this hormone every 10 ds25 or 14 d24,26 does not compromise fertility, the pregnancy rate24-26 or the elimination of cows from the herd; the number of ds open; the number of mastitis cases, the incidence of follicular cysts and abortions26, or animal welfare or health27. Several authors have established that the use of bST at the onset of the estrus28 and 10 ds after AI in dairy cows29 has a positive effect on the pregnancy rate, improves the development of the corpus luteum and increases the production of progesterone28,29 in both repeating cows30,31 and embryo receptor cows32. This favorable effect of bST has also caused a higher percentage of transferable embryos and fewer unfertilized oocytes in superovulated cows29,32,33, and seems to be associated with insulin-like growth factor (IGF-I), and with final oocyte maturation, follicular development, and steroidogenesis30,34,35. Together, beginning Ovsynch and bST at d 69 PP increased fertility at first insemination28,36 and the accumulated pregnancy percentage at 120 and 365 d postpartum32, but decreased the detection of estrus in cows treated with bST37, and failed to increase the fertility of cows under heat stress24.
The purpose of the present work was to evaluate the effect of follicular replacement (GnRH d-7) and the administration of bovine somatotropin (bST) at the time of insemination on fertility at the first postpartum service and the pregnancy rate in high production dairy cows exposed to heat stress.
Material and methods
The study was conducted on Holstein dairy cows (n= 553) from two intensive-production commercial herds in the central highlands of Mexico (Aguascalientes, Mexico), during the warm season, with shade only in the pens of the cows in production and dry cows. After calving, the cows were divided into batches by number of lactations with a whole feed, according to their milk production level. The estimated milk production at 305 d from the herd was 8 493 ± 349.6, and 9 116.3 ± 307.02 kg, respectively, in primiparous and multiparous cows.
Climate variables
During the study period from March to September, climate information regarding ambient temperature (°C) and relative humidity (RH) was recorded every 15 min at the INIFAP weather station in Aguascalientes, located at a distance of 5 km from the dairy herds where the study was conducted. The temperature-humidity index (THI) was calculated (Table 1) according to Ingraham et al37, and the maximum temperature and average relative humidity were recorded using the following equation: THI= ° F - (0.55 - (((HR / 100) x 0.55)) * (° F - 58)).
Reproductive management
The study included dairy cows that gave birth during the months of March and April. Reproductive management during early postpartum and the implementation of estrus synchronization programs took place during the warm months of the year, from May to June. The evaluation of uterine involution and clinical aspects of the reproductive system was performed around ds 20 and 40 postpartum (PP), and 500 μg of synthetic prostaglandin (Cloprostenol sodium, Virbac) were administered, approximately at d 50 PP. The voluntary waiting period and the target calving interval were 50 d and 13.8 mo, respectively.
The study included cows in full lactation (n= 553) that were clinically healthy, exhibiting no anatomical-pathological problems of the reproductive system, and which calved in the months of March and April, and the number of lactations of each cow was recorded. The experimental design is shown in Figure 1. At the beginning of the study (voluntary waiting period (VWP: approximately 50 d in milk), the days in milk (DIM) were recorded; and cows with an acceptable physical body condition (BCS) with an approximation of 0.25 points were used as described by Ferguson et al38.
The cows were randomly assigned to the following treatments (T):
Prostaglandin (PG) (n= 247 cows) Induction of estrus synchronization with prostaglandin (500 μg of cloprostenol sodium, Virbac); the cows were given artificial insemination service 12 h after estrus detection through visual observation.
OVS (n= 161 cows). Ovsynch: d 0, GnRH; d 7, PG; d 9, GnRH; d 10, FTAI). Estrus synchronization and fixed time artificial insemination (FTAI) program, in which cows were administered 100 μg of gonadotropin releasing factor (GnRH) (gonadorelin acetate, SYVA) on day zero (treatment start); subsequently, on ds seven and nine, the cows were given 500 μg of PG and 100 μg of GnRH, respectively. The artificial insemination was performed between 12 and 16 h after the last administration of GnRH.
ROV (n= 145 cows). GnRH + Ovsynch: Seven ds prior to the Ovsynch treatment (OVS), 100 μg of GnRH (i.e., d-7) were administered. Artificial insemination was performed between 12 and 16 h after the last GnRH administration.
For the evaluation of the fertility of the first postpartum service with similar ds in milk of this service, only the cows that presented estrus and were inseminated in the PG treatments, and all those with fixed time service (OVS and ROV), were considered. The cows in each treatment exhibiting estrus were randomly assigned to two groups: a) with bovine somatotropin (C-bST) (n= 221), i.e. the cows that received 500 μg of bovine somatotropin (bST) (Lactotropine, Elanco) at the time of insemination, and b) without bovine somatotropin (S-bST) (n= 235), i.e., cows not treated with bST at the time of insemination.
For the evaluation of the fertility of the first postpartum service with similar ds in milk of this service only the cows that presented estrus were inseminated in the PG treatments were considered, and all those with fixed time service (OVS and ROV). The cows of each treatment which exhibited estrus were randomly assigned to two groups: a) bovine somatotropin (C-bST) (n=221); cows received at the time of insemination 500 mg of bovine somatotropin (bST) (Lactotropine, Elanco). B) without bovine somatotropin (S-bST) (n=235). Cows not treated with bST at the time of insemination.
Based on the interaction of the main treatment effects and the administrations of bST at the time of the first service, six 3experimental groups were formed to be evaluated:
Estrus synchronization with PG without bST (PG / S-bST) (n=80)
Synchronization of the strobe with PG plus bST at service (PG / C-bST) (n = 70).
Ovsynch without bST (OVS / S-bST) (n=83).
Ovsynch with bST at service (OVS / C-bST) (n=78).
GnRH - Ovsynch without bST (ROV / S-bST) (n = 72)
GnRH - Ovsynch with bST at service (ROV / C-bST) (n = 73).
The fertility of the first postpartum service (FERT) was the ratio of pregnant cows to the number of cows served. The date of the first service and conception was recorded. The calving at first service (FERT) and calving to conception intervals (CCI) were calculated. Regardless of the treatment received, all cows that were not pregnant at the first service were served again when a new natural estrus was observed; those that were empty at the time of the gestation diagnosis (approximately 30%) were resynchronized with a Re-synch protocol to provide a new artificial insemination service.
A frequency distribution of the calving to conception interval of cows that responded to synchronization with prostaglandins and were inseminated, and of those with fixed time insemination, was carried out to determine the number of classes and the amplitude of this interval39. The cumulative percentage of pregnant cows (CPPC) for each defined class was estimated thus: 1. Less than 100 d in milk 2. 101 to 150 d in milk. 3. 151 to 201 d of milk. 4. 2020 to 253 d in milk. 5. More than 253 d in milk.
Likewise, the percentage of pregnant cows at the first, second, third or fourth or more services was determined by treatment, bST administration, and their interaction. The calving to conception interval and the number of services per conception were calculated for all cows in the study, including those that did not respond to estrus synchronization with prostaglandin treatment without administration of bovine somatotropin at the time of service.
Variables to be evaluated
The variables evaluated were the number of lactations; days in milk (DIM) and body condition (BC) at the beginning of the study; interval from calving to first service postpartum (CFSI); fertility of first postpartum service (FERT); cumulative percentage of pregnant cows in different postpartum periods (CPPC); distribution of calving-to-conception interval of cows with response to synchronization up to 150 d in milk; as well as, the number of services per conception (NSC) and calving-to-conception interval (CCI), including in these last two parameters the cows with response to synchronization with prostaglandin and that were not treated with bST at the time of insemination.
Statistical analysis
The variables number of lactations (NL), ds in milk (DIM), body condition (BPC), calving to first service interval (CFSI), calving to conception interval (CCI) and number of services per conception (NSC) were analyzed by means of a randomized block analysis of variance. The cumulative percentage of pregnant cows in different postpartum periods and by number of services were analyzed by Chi-square. The expected value of the percentage of fertility of the first postpartum service was analyzed with a first-order multiple logistic regression model. The model was adjusted by the maximum likelihood method considering the effects: Treatment (T); the administration of bST (S); the interaction between treatment and bovine somatotropin (T x S); and the dairy herd was taken as a block39.
Results
The ds in milk at the beginning of the treatment (BT= 56.6 ± 0.3), the body condition (BCS=3.1 ± 0.4), the number of lactations (NL= 2.7 ± 0.1), and the calving to first service interval (CFSI= 59.7 ± 0.3) were similar between treatment groups (P>0.05) (Table 2). The fertility at the first postpartum service of the Ovsynch (OVS, 36.6) and GnRH-Ovsynch (ROV, 36.2) treatments was higher than that observed in the Prostaglandin treatment (27.3 %) (P<0.05) (Figure 2).
Table 2 Body physical condition, days in milk at baseline, number of lactations and interval from birth to postpartum service per treatment
| Treatments | |||
|---|---|---|---|
| Variables | PG | OVS | ROV |
| Number of observations | 150 | 161 | 145 |
| Initial fisical condition | 3.1 ± 0.03 | 3.0 ± 0.03 | 3.1 ± 0.03 |
| Lactation days | 55.3 ± 0.3 | 57.6 ± 0.3 | 56.8 ± 0.3 |
| Number of lactations | 2.6 ± 0.1 | 2.8 ± 0.1 | 2.6 ± 0.1 |
| Calving to first service interval | 58.8 ± 0.3 | 60.5 ± 0.3 | 59.9 ± 0.3 |
(P>0.05).
No single effect of bST (P>0.05) on fertility was detected at the first postpartum service of the dairy cows (36.2 vs 30.6 %, with and without bST, respectively). PG without bST presented a lower fertility rate at the first postpartum service (22.5 %) than the rest of the treatments (P<0.05) (Figure 3).
a/b Different literals between columns indicate differences (P<0.05).
Figure 3 Fertility rate at first service postpartum (FERT) by treatment (PG - OVS - ROV) with (C-bST) or without (S-bST) somatotropin administration
The percentage of pregnant cows at 99 d postpartum was higher with Ovsynch (60.6 %) and ROV (54.3 %) than with Prostaglandin (46.8 %) (P<0.05). Later, between days 100 and 150 postpartum, 28.8 % of the cows treated with Prostaglandin calved; this percentage is superior to those observed with the Ovsynch (17.5 %) and ROV (17.3 %) (P<0.05) treatments (Figure 4). No simple effect of bST (P>0.05) was detected on the percentage of pregnant cows at 99 d postpartum (P>0.05).
The percentage of pregnant cows at d 99 postpartum under treatment with Ovsynch with or without bST (64.7 and 56.5 %, respectively) and ROV without bST (61.7 %) was higher than that observed in PG treatment without bST (41.1 %) (P<0.01). On ds 100 to 150 postpartum, , 34.2 % of the cows treated with PG but without bST were pregnant; this value was higher than that observed with the OVS treatment with bST (13.2 %) and the ROV treatment without bST (11.7 %) (P<0.05) (Figure 5).
Figure 5 Distribution of pregnant cows during postpartum (DIM) by effect of treatment interaction with (C-bST) or without (S-bST) somatotropin administration
Figure 6 shows the percentage of pregnant cows accumulated in the first 150 d postpartum by effect of the synchronization treatment, in the OVS and ROV treatments from d 62 exhibited a cumulative percentage of pregnant cows (29.2 and 33.8 %) which is higher than that observed in the PG treatment (23.0 %) (P<0.05). This difference increased substantially towards d 65 in the OVS (38.7 %) and ROV (41.7 %) treatments, compared with the PG treatment (28.0 %) (P<0.05); the OVS and ROV treatments maintained this significant difference until the 109th and 145th ds in milk, respectively (P<0.05). After 150 d in milk, the cumulative pregnancy rate was similar for all three treatments (P>0.05).
Table 3 shows a higher calving to conception interval in cows treated with PG without bST (144.6 d) than in those that were subjected to the rest of the treatments (P<0.05); fewer services per conception were observed in the groups of cows treated with Ovsynch and with PG plus bST at the time of service (2.2 and 2.3, respectively) compared to those observed in cows treated only with PG without bST at service (2.8), in those of the ROV group with bST (2.7) (P<0.05).
Table 3 Effect of treatment on calving-to-conception interval (CCI) and number of services per conception (NSC)
| Treatment | n | IPC | NSC |
|---|---|---|---|
| PG witout bST | 73 | 144.6 ± 6.7 a | 2.8 ± 0.1 a |
| PG with bST | 66 | 108.4 ± 9.4 b | 2.3 ± 0.2 b |
| OVS without bST | 69 | 115.4 ± 9.2 b | 2.4 ± 0.2 ab |
| OVS with bST | 68 | 106.4 ± 9.3 b | 2.2 ± 0.2 b |
| ROV without bST | 60 | 118.3 ± 9.9 b | 2.4 ± 0.2 ab |
| ROV with bST | 67 | 125.3 ± 9.4 b | 2.7 ± 0.2 a |
bST: Injection of somatotropin at the time of artificial insemination (AI)
OVS: [d 0, GnRH; d 7, PG; d 9, GnRH; d 10, AI]
ROV: [d -7, GnRH; plus Ovsynch].
a,b Different letters per column indicate significant statistical difference (P<0.05).
Discussion
Estrus synchronization and fixed-time artificial insemination (FTAI) programs improved first postpartum fertility in dairy cows under heat stress; thus, these programs show their goodness in overcoming the negative effect of dairy cow productivity on first postpartum fertility40,41, and even as an additive negative effect to heat stress1-6.
The fertility rates observed in the first postpartum service in the FTAIs coincide with those reported by other studies7-16,20, which may be related to a higher ovulation rate of a follicle that is suitable for fertilization7, and to a higher circulating concentration of the hormone progesterone12,15, compared to schemes where cows were not pre-synchronized. However, other studies conducted in dairy cows under heat stress found a less efficient reproductive response than that observed in cows in thermal comfort12,14,15. An established effect of heat stress on dairy cows is that it reduces the quality of follicles and oocyte competence16-20,42, the ovulation rate7,8, and the diameter size of the ovulatory follicles8. Some studies determined that administering gonadotropin releasing factor (GnRH)19 or replacing dominant follicles20 in dairy cows during the summer season improved oocyte competence for fertilization and resulted in a higher percentage of embryos that would reach the blastocyst stage in in vitro studies, and concluded that oocyte competence has also been reported by other authors17,18 under heat stress conditions, especially in the case of repeating cows17,31, even though the fertility of in vitro fertilized oocyte was similar in winter and in the summer17. This emphasizes the importance of minimizing the effect of heat stress and shows that the FTAI schemes may have had a beneficial effect, improving the follicular quality and oocyte competence. The administration of gonadotropin release factor (GnRH: i.e., ROV treatment) prior to the Ovsynch program with the intention of generating follicular replacement did not improve the fertility rate of the first postpartum service, which was similar to the one observed in cows of the OVS group (Ovsynch). These results may indicate that the latter scheme of fixed-time artificial insemination was in itself sufficient to improve the follicular quality and oocyte competence, and they agree with those observed in other studies21,22, and that alone the follicular exchange prior to the start of the Ovsynch program can improve fertility in cows that exhibited uterine problems in the early postpartum period and in those with a low body condition21.
It has been determined that the loss of the cow’s physical body condition and the depth of the negative energy balance affect the fertility of the first postpartum service43,44 by affecting oocyte competence45,46; and given the acceptable health and physical body condition of the cows in this study, it may be inferred that these negative effects were controlled. On the other hand, the fertility rate of the first postpartum service of over 36% obtained in the fixed-time artificial insemination programs observed by the present study under heat stress is excellent, compared to the fertility reported in cows with a high productive potential40,41,47 and under heat stress1-6. On the other hand, the administration of bovine somatotropin (bST) at the moment of the fixed-time artificial insemination did not have a determining effect as a main variable to improve fertility in the first postpartum service, as reported by Jousan et al.24; therefore, it is possible that estrus synchronization and fixed-time artificial insemination programs were sufficient to eliminate the damaged follicle due to heat stress, induce the emergence of new follicles, and improve the quality of the ovulatory follicle and the competence of the oocyte as described in other studies19,20. However, the fact that the group of cows treated only with prostaglandin without administration of somatotropin at the time of service had a fertility rate 10.4 to 16 percentage points lower in the first postpartum service than that observed in cows treated with somatotropin significantly indicates a positive effect of somatotropin on fertility in the first postpartum service, as documented in other studies with bST treatments from 61 to 63 ds in milk with repeated applications of this hormone every 1025,48,49 or 14 d26,35,36, having improved the development of the corpus luteum and increased its production of progesterone28,29, both in repeating cows30,31, and in embryo receptor cows32. Furthermore, it has been inferred that this beneficial effect involves insulin-like growth factor type I (IGF-1), which appears to be associated with the process of final oocyte maturation, follicular development, and steroidogenesis34,50,51 and which, in in vitro studies, increases the pregnancy rate of transferred embryos52.
On the other hand, in programs in which bST is administered every 14 ds to dairy cows in order to increase their milk production24-26, the expression of the estrus has been observed to be negatively affected25,36; therefore, it has been suggested that the use of bST should be accompanied by fixed-time insemination protocols in order to ensure insemination of 100% of the cows36. Thus, although the application of bST as the main variable does not have a relevant effect on the fertility rate of the first postpartum service under heat stress, at least with the FTAI the risk of not detecting cows in heat is eliminated.
Consequently, an increase of 15.4 to 23.6 % in the percentage of pregnant cows in the first third of lactation in fixed-time insemination programs compared to traditional management, as confirmed in other studies9-11,14, ensures a new production cycle and reduces the risk of eliminating cows from the herd due to reproductive causes. On the other hand, pregnant cows using estrus synchronization treatments with prostaglandins without bST at service exhibited between 19.3 and 38.6 more open ds than with the other treatments; this implies the loss of at least one to two lost estrus cycles, which entails extra costs in the reproductive cycle of the dairy cows.
Conclusions and implications
The administration of gonadotropin releasing factor (GnRH) prior to the Ovsynch program (ROV) and the administration of bovine somatotropin (bST) at the time of insemination did not improve the fertility rate of the first postpartum service. Fixed-time artificial insemination schemes improved the fertility rate of the first postpartum service and increased the number of pregnant cows in the first 99 d postpartum. Under heat stress, bovine somatotropin increases the fertility rates at first service postpartum in cows treated with prostaglandin, but not in cows in fixed-time insemination programs.
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Received: March 28, 2018; Accepted: September 18, 2019
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