Negative energy balance and metabolic stress in relation to oocyte and embryo quality: an update on possible pathways reducing fertility in dairy cows

Abstract

A negative energy balance in metabolically compromised high producing dairy cows has been shown to influence oocyte and embryo quality. However, the possible involved pathways needed more attention to better understand specific deleterious effects. Oocyte maturation is the first process to be scrutinized. Because many possible metabolic factors might directly impact oocyte quality, systematic in vitro approaches were used to investigate the effects of oocyte maturation under elevated NEFA concentrations. Blastocysts originating from NEFA-exposed oocytes showed a lower cell number, an increased apoptotic cell index, signs of glucose intolerance, sensitive to oxidative stress and mitochondrial dysfunction. Defining these embryos' transcriptome and epigenome signatures revealed changes in DNA methylation patterns. Long-term exposure of developing murine follicles to elevated NEFA concentrations showed to impair oocyte developmental competence even more. While little is known on how the oviductal microenvironment can change as a consequence of a negative energy balance, a validated in vitro bovine oviduct model offered some valuable insights on how NEFAs disturb oviductal cell physiology. NEFA exposure reduces cell proliferation, cell migration, sperm binding capacity and monolayer integrity. In addition, oviductal cells seem to play an active role in regulating luminal NEFA-concentrations through increased permeability, intracellular lipid accumulation and fatty acid metabolism. This might favour early embryo development. The establishment of a successful pregnancy largely depends on the ability of the embryo to interact with a properly prepared endometrium. Because suboptimal physiological conditions influence oocyte maturation and embryo development to the extent that epigenetic consequences are unavoidable, the question arises if these changes hamper embryo implantation and subsequent development. Gene expression studies on epithelial endometrial cells brought in contact with in vitro embryos cultured for 4 days under suboptimal conditions reveal that the embryo-endometrial signaling is affected. Transfer of bovine embryos derived from compromised oocytes showed disturbed embryo development following recovery at day 14 with a negative impact on IFNt secretion and therefore suggesting carry-over effects from suboptimal culture conditions. The current paper will document the most important recent findings and comment on extrapolation possibilities from in vitro studies to field conditions in daily dairy practice. In addition, the possibility of remediating approaches will be discussed to see how this knowledge might generate insights on possible alleviating strategies.

Extended lactation in high-yielding dairy cows. I. Effects on reproductive measurements

“…The idea behind the extension of the VWP is that the onset of breeding takes place fairly after the high-risk period of puerperium and postpartal negative energy balance (NEB; Knight, 2005), which should result in improved herd fertility. This is crucial, as the genetic selection toward milk production has led to a high predisposition of dairy cows to NEB and NEBmediated diseases (Veerkamp et al, 2003;Leroy et al, 2017) associated with a reduced fertility (Lucy, 2007;Lucy, 2016).…”

Analysis of the transcriptome of bovine endometrial cells isolated by laser micro-dissection (2): impacts of post-partum negative energy balance on stromal, glandular and luminal epithelial cells

“…Despite that a more balanced selection is currently applied [ 5 ], high milk-yield cows still meet strong negative energy balance (NEB) during the early postpartum period due to the high nutrient and energy demand for body metabolism, milk production, and body weight maintenance [ 6 ]. Energy deficiency and excessive lipid mobilization during the postpartum period have been reported to be the cause of unfavorable reproductive performances such as delayed ovarian activity [ 7 ], prolonged uterine involution period [ 8 ], retained placenta [ 9 ], endometritis [ 10 ], increased early embryonic losses and decreased conception rates [ 11 ].…”

Classifying the fertility of dairy cows using milk mid-infrared spectroscopy

“…Multiple factors have been reported to be associated with variation in conception rate. Nongenetic factors include quality and quantity of bull semen (DeJarnette et al, 2004), age, body con-10461 dition, energy balance, RUP, milk yield, milk protein concentration, and health status of the cow (Roche et al, 2007;Shorten et al, 2015;Rodney et al, 2016;Leroy et al, 2017;Morton et al, 2017;Rearte et al, 2018), days postcalving (Clay et al, 2004), heat stress (Morton et al, 2007), lameness (Alawneh et al, 2011), and insemination season (Cornwell et al, 2006). Berry et al (2011) indicated that about 2.3% of the phenotypic variation in conception rate could be attributed to additive genetic effects.…”