Maternal nutrient restriction alters uterine artery hemodynamics and placentome vascular density in Bos indicus and Bos taurus

Abstract

The objective was to examine uterine artery blood flow (UBF) as well as macroscopic and microscopic placentome vascular density in nutrient-restricted Angus and Brahman heifers. Angus (n = 6) and Brahman (n = 6) heifers were bred to a single sire and pregnancy confirmed at 30-d postbreeding. Heifers were randomly assigned to 1 of 2 dietary treatments consisting of 100% (control-fed; CON; n = 6) or 60% (total nutrient-restricted; RES; n = 6) based from net energy requirements for gestating heifers. Nutritional treatments were imposed from days 50 to 180 of gestation. On day 175 of gestation, UBF was collected ipsilateral and contralateral to the conceptus via Doppler ultrasonography. Heifers underwent Cesarean sections for collection of 2 adjacent placentomes on day 180 of gestation. The primary cotyledonary artery of 1 placentome was perfused with Alexa Fluor 647 Con A conjugate to examine macroscopic cotyledonary vascular density via an in vivo imaging system. The second placentome was fixed for microscopic immunofluorescence labeling of capillaries and separated into maternal (caruncle) and fetal (cotyledon) components for determination of angiogenic factor mRNA expression. Main effects of nutritional treatment and breed are reported in the absence of a significant nutritional treatment by breed interaction. Ipsilateral UBF was decreased (P < 0.05) by 48% in RES vs. CON, whereas breed did not influence ipsilateral UBF. Contralateral UBF was not different between nutritional treatments; however, contralateral UBF was decreased (P < 0.05) by 63% in Brahman vs. Angus cattle. Macroscopic cotyledonary vascular density was increased (P < 0.05) by 36% in RES vs. CON and 82% in Brahman vs. Angus heifers. Percent capillary area and capillary perimeter were increased (P < 0.05) in RES vs. CON and increased (P < 0.05) in Brahman vs. Angus heifers. Dietary treatments did not alter angiogenic factor expression; however, transcript abundance of caruncle and cotyledon ANGP1, FLT1, and KDR was increased (P < 0.05) in Brahman vs. Angus heifers. In summary, these data indicate compensatory responses in macroscopic and microscopic placentome blood vessel density during maternal nutrient restriction-induced reductions in UBF. Moreover, a greater macroscopic density of cotyledonary blood vessels was observed in Brahman vs. Angus heifers.

Maternal Vitamin and Mineral Supplementation and Rate of Maternal Weight Gain Affects Placental Expression of Energy Metabolism and Transport-Related Genes

“…The fetomaternal interface provided by the placenta acts as a nutrient sensor to coordinate maternal nutrient supply and fetal metabolic requirements [ 5 , 6 ]. Thus, proper fetal development and nutrition are supported by an adequate nutrient supply through the placenta [ 7 , 8 ]. The placenta has many functions that include nutrient and waste product transport and hormone synthesis [ 6 ].…”

Applied Use of Doppler Ultrasonography in Bovine Reproduction

“…Doppler ultrasonography has been used as a non-invasive technique in reproductive research to quantify UBF and to make inferences on how different management strategies may affect offspring development or pregnancy outcomes (Bollwein et al, 2002;McCarty et al, 2018;Gard Schnuelle et al, 2021). For example, differences in UBF were detected by color Doppler between cows exposed to nutrient restriction during early and mid-gestation and control cows (Camacho et al, 2014;Lemley et al, 2018). These differences in UBF were supported by histological differences in post-harvest placentome capillaries and differences in macroscopic vascular density of placentomes (Lemley et al, 2018), indicating that color Doppler can be used to provide insights into uterine and placental vascular adaptation in response to environmental insults (Lemley, 2017).…”

“…Doppler ultrasonography has been utilized extensively in research settings to evaluate changes in uterine blood flow (UBF) during the estrous cycle (Bollwein et al, 2000;Honnens et al, 2008;Bollwein et al, 2016), fetal and placental development (Camacho et al, 2014;Brockus et al, 2016;Lemley et al, 2018), and changes in blood flow associated with postpartum uterine involution (Heppelmann et al, 2013). The technique used to estimate UBF is relatively simple and has been well documented and described by others (reviewed by Bollwein et al, 2016).…”

“…For example, differences in UBF were detected by color Doppler between cows exposed to nutrient restriction during early and mid-gestation and control cows (Camacho et al, 2014;Lemley et al, 2018). These differences in UBF were supported by histological differences in post-harvest placentome capillaries and differences in macroscopic vascular density of placentomes (Lemley et al, 2018), indicating that color Doppler can be used to provide insights into uterine and placental vascular adaptation in response to environmental insults (Lemley, 2017). Research using color Doppler to estimate UBF during pregnancy is ongoing and will continue to contribute to our understanding of placental development and prenatal programming of offspring (Bollwein et al, 2002;Panarace et al, 2006;Sharma et al, 2021).…”

Melatonin Supplementation Alters Maternal and Fetal Amino Acid Concentrations and Placental Nutrient Transporters in a Nutrient Restriction Bovine Model

“…Furthermore, nutrient transport across the placenta is imperative for proper growth, development, and survivability of the fetus [2]. Maternal nutrient restriction during gestation has been shown to decrease uterine blood flow and fetal body weight in sheep and cattle [3][4][5]. Furthermore, maternal nutrient restriction reduces amino acid transporter abundance in placental tissue of sheep and cows [6,7].…”