NE1007: Ovarian and Environmental Influences on Embryonic/Fetal Mortality in Ruminants
Statement of Issues and Justification
Impaired reproductive performance is one of two major causes of reduced productivity for dairy cattle and represents the major cause of reduced profitability for meat animal species. Despite recent advances in estrous synchronization, overall fertility in dairy herds has declined during the past ten years, both nationally and internationally. Data from the 1996 NAHMS Dairy Study indicate that 11.6% of dairy cows are not pregnant 150 days after calving. The economic impact on dairy profitability is significant. The current NE-161 project has focused on endocrine manipulation of follicular development and luteal function. During the next 5 years, it is proposed to study mechanisms by which nutritional, management and environmental factors impact ovarian activity and the subsequent effect on pregnancy and calving rates.During the previous NE-161 project period, major progress was made in understanding that the duration of ovarian follicular development preceding ovulation is key to fertility in cattle. Persistent follicles develop under sub-luteal phase progesterone conditions such as during low dosage progestogen treatment for estrous synchronization (Kinder et al. 1996). However, through collaborative efforts of the NE-161 project, it was discovered that follicles that persisted for longer than the length of a normal follicular wave (12 days) resulted in decreased pregnancy rate after ovulation (Cooperative Regional Research Project, NE-161, 1996). The benefits to fertility of having a shorter duration of follicular development were reinforced by further collaborative work. Comparing dairy cows with three waves vs. two waves of follicular development in the cycle prior to ovulation and insemination, the ovulatory follicle was younger and smaller in three wave cows and resulted in a higher pregnancy rate (Cooperative Regional Research Project, NE-161, 2002). Similar differences were also noted in studies with beef cows (Ahmad et al., 1997).
The recognition that a shorter duration of preovulatory follicular development leads to enhanced fertility has made protocols for synchronized breeding more effective. For example, the development of persistent follicles during estrous synchronization can be corrected by recruitment and selection of a new ovulatory follicle by injection of gonadotropin-releasing hormone (Thatcher et al., 1996). This, in turn, has led to development of methods for both synchronization of follicular development and corpus luteum regression to effectively program insemination time (Ovsynch/TAI) without need for estrous detection (Burke et al., 1996; Pursley et al., 1997 a,b; Stevenson et al., 1996). Using this approach and comparing the expected size of the ovulatory follicle with fertility, Vasconcelos et al. (1999) found that pregnancy rates were higher from smaller, younger follicles ie. consistent with results of the previous NE-161 project. Most recently, pre-synchronization of lactating cows with prostaglandin F2a was applied to the Ovsynch/TAI protocol to optimize a short duration of follicular development and increased fertility (Moriera et al., 2001).
Although tools are now available to manage follicular development and allow timed insemination, several field studies have raised concerns about large early pregnancy losses in lactating cows. By using ultrasound imaging of embryos between days 25-32 days after AI, pregnancy losses ranged from 14-40 % before subsequent pregnancy diagnosis at 50-98 days (Vasconcelos et al., 1999; Cartmill et al., 2001; Moreira et al., 2001). Previously Vasconcelos et al. (1997) found that 10.5 % of lactating dairy cows that were pregnant at 28 days had lost the pregnancy by day 42. Based upon return intervals exceeding 27 days after breeding, Thatcher et al. (1994) estimated that late embryonic death rate was 10.6 % in heifers. Attachment of the embryo in the uterus is initiated around day 30 in the cow, with marked development of the placentomes between days 30 and 40 (Melton et al., 1951; King et al., 1982). Earlier authors have illustrated pregnancy losses occurring both before (Van Cleeff et al., 1991) and after day-25 of gestation (Schallenberger et al., 1989; Kastelic et al., 1991; Van Cleeff et al., 1991; Wolff, 1992; Smith and Stevenson, 1995).
As pointed out earlier, fewer data have been collected on embryonic death in beef cows after synchronization of estrus and fixed-time insemination. In the study reported by Bridges et al. (1999) only one of 71 cows pregnant at day 39 failed to calve. Four studies have been done in animals that were inseminated 12 hours after detection of estrus. In Brahman crossbred heifers, fertilization rate was 93% of intact ova, 78% had intact embryos on day 16 and 72% were pregnant on day 35 (Smith et al., 1982). Beal et al. (1992) diagnosed pregnancy by ultrasonography at 25, 45 and 65 days in 205 beef cows that initially had 138 viable embryos. Losses were 6.5% to day 45 and another 1.5% to day 65. Lamb et al. (1997) measured embryo mortality in Bos taurus heifers on three ranches with herds of 169 to 439 head. These heifers had been inseminated 12 hours after they were first detected in estrus in response to an injection of PGF2 17 days after withdrawal of MGA, which had been fed at 0.5 mg/day for 14 days. Conception rates as determined by ultrasonography at 29 to 33 days after insemination ranged from 44 to 67%. Of 525 pregnant heifers, 4.2% did not have viable embryos at palpation 60 to 90 days after the end of the breeding season. Dunne et al. (2000) measured embryo survival at slaughter on day 14 as 68%. By ultrasonography at day 30, their estimate was 76% pregnant, while at full term, 71.8% calved, so that the late embryonic and fetal loss was 4.2 percentage points. Thus they concluded that most losses occurred before day 14 and that losses after day 30 were approximately 5.5%. Clearly late embryonic losses are lower in beef cattle than in dairy cattle.
Drost et al. (1999) have used embryo transfer (ET) to attempt to overcome some of the effects of heat stress in lactating dairy cows in the summer in Florida. Conception rates at day 42 were improved from 21.4% for AI to 35.4% for ET from superovulated donors. Embryo mortality, as estimated from the difference in pregnancies at day 42 and cows with high progesterone on day 22, was 64.7% in cows bred AI and 41.3% in cows given ET.
There is evidence that late embryonic loss precedes luteolysis. In 7 of 8 heifers in which embryonic death was detected between days 25 and 40 post breeding, the onset of luteal regression, as detected by ultrasonography, began at least 3 days after embryonic death, as indicated by loss of heartbeat (Kastelic et al., 1991). In another study utilizing 70 pregnant cows, 7 pregnancies were lost between days 35 and 42 after breeding; embryonic death in each of these 7 cows preceded luteal regression, detected by ultrasonography and declining concentrations of progesterone in milk (Wolff, 1992). Schallenberger et al. (1989) observed an increased secretion of PGF2 between days 30 and 36 in pregnant heifers, one of which lost the pregnancy. However, from the magnitude and timing of secretion of PGF2 , or the luteal response to it, no firm conclusions could be drawn.
Lulai et al. (1994) induced new corpora lutea on day 36 to 40 of pregnancy, during progestogen treatment and after induced regression of the original corpora lutea. When present on the ovary adjacent to the pregnant uterine horn, but not contralateral, induced corpora lutea were maintained after progestogen withdrawal and supported the pregnancy. In research conducted at West Virginia, maintenance of pregnancy was examined after induction of new corpora lutea between days 27 and 54 post breeding (Wright et al. 1994). This was done in cows in which original corpora lutea had either regressed or been removed earlier and pregnancy had been maintained with an exogenous progestogen. After induction of new corpora lutea,, progestogen was withdrawn gradually and pregnancy was maintained only when the new corpus luteum was induced on the ovary adjacent to the embryo.
Bridges et al. (2000) removed original corpora lutea on day 26 of pregnancy, induced new corpora lutea between days 28 and 31 and examined patterns of secretion of PGF2 and estradiol during days 31 through 35. In cows with higher concentrations of PGF2 , more progesterone was secreted by the induced corpus luteum and maintenance of pregnancy tended to be higher. In addition, there was a tendency for more pregnancies to be maintained when concentrations of estradiol were lower.In the pooled data from this study and Wright et al.(1994), when a new corpus luteum was induced on the ipsilateral ovary later than day 36 after mating, 21 of 21 pregnancies were maintained. However, when the corpus luteum was induced on or before day-36 after mating, only 15 of 30 pregnancies were maintained. Further studies of the timing and nature of embryonic deaths after day 25 of pregnancy and the hormonal patterns with which they are associated are needed.
It is disturbing that treatment protocols have been designed to avoid the early embryonic death associated with persistent follicles in the dairy cow, but losses of pregnancy during the late embryonic and early fetal period appear unacceptably high. The degree of late embryonic loss varies widely among different studies and makes a large contribution to the overall low pregnancy rate to AI in dairy cattle that presently stands at less than 40 % ( Butler, 1998). These late embryo losses may be attributable to alteration in corpus luteum function at any point between maternal recognition of pregnancy through embryo attachment and further compromised by other factors such as heat stress (Cartmill et al., 2001).
Advantages of performing this work as a multi-state effort include the ability to commit larger numbers of animals under similar, but different management systems to the research effort, overlapping approaches with collaborative efforts and technologies can be directed toward several objectives simultaneously, and shared experience and data analysis make the interactions more beneficial.
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