RESUMO
The overarching aim was to examine the relationship of rectal temperature at fixed time artificial insemination (FTAI) on pregnancy outcomes in a typical breeding season with expected pregnancy rates approaching 50% using Bos indicus and Bos taurus cattle. This represents a continuum of steps to test the hypothesis that elevated body temperature at or around insemination is functionally important to maximize pregnancy outcomes. Rectal temperature of Bos indicus cattle at FTAI ranged from 37.0 to 40.9 °C; 60.6% were hyperthermic. Positive factors impacting pregnancy outcomes were rectal temperature at FTAI, body condition, and estrus patch scores. Rectal temperature at FTAI was positively associated with pregnancy outcomes (P < 0.0001); per each 1 °C increase pregnancy odds increased 1.9 times (95% CI: 1.4 to 2.6). Highest pregnancy outcomes occurred with rectal temperatures exceeding 40 °C (P = 0.0004). Rectal temperature before FTAI in Bos taurus cattle ranged from 37.8 to 41.8 °C; 43.3% were hyperthermic. Factors impacting pregnancy were rectal temperature at FTAI, estrus activity, parity, and ambient conditions on day of FTAI. Rectal temperature of Bos taurus cattle at FTAI was positively associated with pregnancy (P = 0.0286); odds increased 1.45 times (95% CI: 1.0 to 2.0) per each 1 °C increase. Highest pregnancy outcomes occurred with rectal temperatures at FTAI exceeding 40 °C (P = 0.057). Moreover, positive relationship of rectal temperature at FTAI to pregnancy persisted in estrual females (71.25% of total; P = 0.0408; OR 1.5; 95% CI: 1.0 to 2.2). Mindful that 1) elevated temperatures observed in Bos indicus and Bos taurus cattle directly promote meiotic resumption of the oocyte in vitro and that 2) in vivo hyperthermia alters intrafollicular components which others have shown to potentiate ovulation and promote meiotic resumption, it is biologically plausible that an acute elevation in body temperature at or around time of insemination is functionally important to maximize pregnancy outcomes.
Reproductive efficiency remains a major challenge for beef producers with 35% to 55% of females failing to become pregnant after a single insemination. While basis for failure is multi-factorial, heightened estrus activity matters for pregnancy outcomes, even when synchronizing ovulation for fixed time artificial insemination. Body temperature increases of 1.5 °C+ are common during estrus. We hypothesize that higher estrous-associated temperatures (HEAT) at/near insemination are functionally important to maximize pregnancy outcomes. Elevated temperatures equivalent to what is observed in females exhibiting HEAT have been shown to induce oocyte meiotic resumption. An acute episode of hyperthermia after the LH surge alters intrafollicular components known to potentiate ovulation and affect the oocyte. Effort to examine the relationship of rectal temperature at fixed time artificial insemination with pregnancy outcomes in a breeding season with expected pregnancy rates >50% represents a next step in the continuum of hypothesis testing. The positive relationship of rectal temperature at insemination with pregnancy outcomes that was discovered adds to foundational knowledge. Because the degree of hyperthermia is related to highest pregnancy outcomes, a case is made for HEAT to be biologically and functionally important to maximize pregnancy outcomes in cattle.
Assuntos
Sincronização do Estro , Resultado da Gravidez , Animais , Bovinos , Detecção do Estro , Feminino , Inseminação Artificial/veterinária , Gravidez , Resultado da Gravidez/veterinária , Taxa de Gravidez , Progesterona , TemperaturaRESUMO
Cows acutely heat stressed after a pharmacologically induced luteinizing hormone (LH) surge had periovulatory changes in the follicular fluid proteome that may potentiate ovulation and impact oocyte developmental competence. Because the cellular origins of differentially abundant proteins were not known, we have examined the cumulus and granulosa cell transcriptomes from the periovulatory follicle in cows exhibiting varying levels of hyperthermia when occurring after the LH surge. After pharmacological induction of a dominant follicle, lactating dairy cows were administered gonadotropin releasing hormone (GnRH) and maintained in thermoneutral conditions (~67 temperature-humidity index [THI]) or heat stress conditions where THI was steadily increased for ~12 h (71 to 86 THI) and was sufficient to steadily elevate rectal temperatures. Cumulus-oocyte complexes and mural granulosa cells were recovered by transvaginal aspiration of dominant follicle content ~16 h after GnRH. Rectal temperature was used as a continuous, independent variable to identify differentially expressed genes (DEGs) increased or decreased per each 1 °C change in temperature. Cumulus (n = 9 samples) and granulosa (n = 8 samples) cells differentially expressed (false discovery rate [FDR] < 0.05) 25 and 87 genes, respectively. The majority of DEGs were upregulated by hyperthermia. Steady increases in THI are more like the "turning of a dial" than the "flipping of a switch." The moderate but impactful increases in rectal temperature induced modest fold changes in gene expression (<2-fold per 1 °C change in rectal temperature). Identification of cumulus DEGs involved in cell junctions, plasma membrane rafts, and cell-cycle regulation are consistent with marked changes in the interconnectedness and function of cumulus after the LH surge. Depending on the extent to which impacts may be occurring at the junctional level, cumulus changes may have indirect but impactful consequences on the oocyte as it undergoes meiotic maturation. Two granulosa cell DEGs have been reported by others to promote ovulation. Based on what is known, several other DEGs are suggestive of impacts on collagen formation or angiogenesis. Collectively these and other findings provide important insight regarding the extent to which the transcriptomes of the components of the periovulatory follicle (cumulus and mural granulosa cells) are affected by varying degrees of hyperthermia.
Approximately 70% of the world's cattle population reside under ambient conditions experiencing some level of heat stress. Heat-stressed cows chronically exposed to elevated ambient temperatures have difficulty getting pregnant. Although the underlying basis for poor fertility during bouts of chronic heat stress remains unclear and is likely because of many different factors, when ambient conditions are sufficient to increase cow body temperature, different ovulatory follicle components are affected (i.e., mural granulosa cells that line the ovulatory follicle, the intrafollicular fluid and or the cumulus-oocyte complex while it matures in preparation for fertilization while resident within). To test this hypothesis, we have examined the cumulus and granulosa cell transcriptomes from the periovulatory follicle in cows. Using steady increases in THI to induce varying levels of elevated body temperature after the luteinizing hormone surge we discovered certain genes in the cumulus cells that may have indirect but impactful consequences on the oocyte as it undergoes meiotic maturation. We also noted changes in gene expression in granulosa cells that may impact ovulation and corpus luteum formation.