Controlled elevated temperatures during early-mid gestation cause placental insufficiency and implications for fetal growth in pregnant pigs

Abstract

It is known that pig offspring born from pregnant pigs exposed to elevated ambient temperatures during gestation have altered phenotypes, possibly due to placental insufficiency and impaired fetal growth. Therefore, the objective of this study was to quantify the effect of maternal heat exposure during early-mid gestation, when pig placentae grow heavily, on placental and fetal development. Fifteen pregnant pigs were allocated to thermoneutral (TN; 20 °C; n = 7) or cyclic elevated temperature conditions (ET; 28 to 33 °C; n = 8) from d40 to d60 of gestation. Following euthanasia of the pigs on d60, placental and fetal morphometry and biochemistry were measured. Compared to TN fetuses, ET fetuses had increased (P = 0.041) placental weights and a lower (P = 0.013) placental efficiency (fetal/placental weight), although fetal weights were not significantly different. Fetuses from ET pigs had reduced (P = 0.032) M. longissimus fibre number density and a thicker (P = 0.017) placental epithelial layer compared to their TN counterparts. Elevated temperatures decreased (P = 0.026) placental mRNA expression of a glucose transporter (GLUT-3) and increased (P = 0.037) placental IGF-2 mRNA expression. In conclusion, controlled elevated temperatures between d40 to d60 of gestation reduced pig placental efficiency, resulting in compensatory growth of the placentae to maintain fetal development. Placental insufficiency during early-mid gestation may have implications for fetal development, possibly causing a long-term phenotypic change of the progeny.

Figure 1

Physiological signs of thermal stress in pregnant pigs exposed to thermoneutral (TN) or elevated temperature (ET) conditions between d40 and 60 of gestation. (a) Respiration rate; (b) Skin temperature; (c) Rectal temperature. TN: n = 7 pigs; ET: n = 8 pigs. Data are expressed as means with average standard error of the difference (SED). Different letters indicate P < 0.05.

Figure 2

Placental mRNA relative expression of nutrient transporters of pregnant pigs exposed to thermoneutral (TN) or elevated temperature (ET) conditions between d40 to 60 of gestation. SLC2A1: solute carrier family 2 member 1; SLC2A3: solute carrier family 2 member 3; SLC7A1: solute carrier family 7 member 1; SLC7A2: solute carrier family 7 member 2; SLC7A7: solute carrier family 7 member 7. TN: n = 12 placentae; ET: n = 16 placentae. *P < 0.05.

Figure 3

Photomicrographs of representative placental epithelial layer from pregnant pigs exposed to thermoneutral (TN; a) or elevated temperature (ET; b) conditions. TN: n = 9 placentae; ET: n = 12 placentae.

Figure 4

Photomicrographs of representative cross-sectional areas of M. longissimus of fetuses from pregnant pigs exposed to thermoneutral (TN; a) or elevated temperature (ET; b) conditions. TN: n = 14 fetuses; ET: n = 16 fetuses.