Efficient fat storage in premenopausal women and in early pregnancy: a role for estrogen

Abstract

There is a sexual dimorphism in body fat in humans. Adipose tissue increases with puberty and early pregnancy in women, suggesting gonadal steroids can influence body fat. Previously, we have observed that oral estrogen, compared with transdermal estrogen, reduced postprandial lipid oxidation and increased body fat, possibly due to suppressed hepatic lipid oxidation. If estrogen effects lipid oxidation, we predicted that subjects with significantly different endogenous estrogen production would oxidize lipids at different rates. The aim of this study was to compare energy metabolism in 12 pregnant (19 wk gestation, 29 ± 1 yr, 1.66 ± 0.02 m, 73.5 ± 2.4 kg), 11 nonpregnant premenopausal (29 ± 2 yr, 1.68 ± 0.02 m, 63.1 ± 1.8 kg), and 28 postmenopausal (58 ± 1 yr, 1.62 ± 0.01 m, 69.9 ± 1.0 kg) women who were not receiving estrogen, and to relate these findings to endogenous estrogen concentrations. All women underwent indirect calorimetry under identical situations in the basal and postprandial state following a standard mixed meal. Basal (5998 ± 184 vs. 5712 ± 184 vs. 5800 ± 121 kJ·24 h, respectively) and postprandial energy expenditure (7172 ± 239 vs. 6964 ± 210 vs. 6955 ± 147 kJ·24 h) was similar among groups. However, basal lipid oxidation was reduced in pregnant (45.3 ± 6.1 mg/min, P < 0.05) and nonpregnant women (44.5 ± 6.3 mg/min, P < 0.05) compared with postmenopausal women (58.4 ± 2.9 mg/min). Postprandial lipid oxidation differed among groups, being least in pregnant women (8.8 ± 6.2 mg/min) compared with nonpregnant (28.9 ± 6.4 mg/min, P < 0.04) and postmenopausal (48.1 ± 4.0 mg/min, P = 0.0001) women. There was a significant reciprocal increase in postprandial carbohydrate oxidation. Mean postprandial glucose levels were slightly but nonsignificantly higher in pregnant women. Insulin levels were significantly higher in postmenopausal compared nonpregnant, but not pregnant, women. In a multiple regression analysis, serum estradiol (log transformed) correlated negatively with postprandial lipid oxidation (r = -0.66, P = 0.0001) and positively with postprandial nonesterified free fatty acid levels, whereas no correlation was found with postprandial insulin, glucose, fat free mass, and fat mass. In summary, postprandial lipid oxidation is reduced in pregnancy compared with that in healthy nonpregnant women, who in turn have lower postprandial lipid oxidation than postmenopausal women. This implies that the premenopausal years and early pregnancy are states of efficient fat storage, possibly mediated through reduced lipid oxidation due to estrogen, therefore increasing body fat for reproduction, thus supporting the notion that fat mass can be regulated.