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Obstet Gynecol. Author manuscript; available in PMC 2017 May 01. Published in final edited form as: Obstet Gynecol. 2016 May ; 127(5): 884–892. doi:10.1097/AOG.0000000000001372.
Energy Intake and Energy Expenditure for Determining Excess Weight Gain in Pregnant Women L. Anne Gilmore, Ph.D.1, Nancy F. Butte, Ph.D.2, Eric Ravussin, Ph.D.1, Hongmei Han, M.S. 1, Jeffrey H. Burton, Ph.D.1, and Leanne M. Redman, Ph.D.1 1Pennington
Author Manuscript
2Baylor
Biomedical Research Center
College of Medicine
Abstract Objective—To conduct a secondary analysis designed to test whether gestational weight gain is due to increased energy intake or adaptive changes in energy expenditures.
Author Manuscript
Methods—In this secondary analysis, energy intake and energy expenditure of 45 pregnant women (BMI 18.5–24.9 kg/m2, n=33 and BMI ≥ 25, n=12) were measured preconceptionally 22, and 36 weeks of gestation. Energy intake was calculated as the sum of total energy expenditure measured by doubly labeled water and energy deposition determined by the 4-compartment body composition model. Weight, body composition, and metabolic chamber measurement were completed preconceptionally, 9, 22, and 36 weeks of gestation. Basal metabolic rate was measured by indirect calorimetry in a room calorimeter and activity energy expenditure by doubly labeled water. Results—Energy intake from 22 to 36 weeks of gestation was significantly higher in high gainers (n=19) (3437 ± 99 kcal/d) versus low + ideal gainers (n=26) (2687 ± 110 p< .001) within both BMI categories. Basal metabolic rate increased in proportion to gestational weight gain; however, basal metabolic rate adjusted for body composition changes with gestational weight gain was not significantly different between high gainers and low + ideal gainers (151 ± 33 vs. 129 ± 36 kcal/d; p=.66). Activity energy expenditure decreased throughout pregnancy in both groups (low + ideal gainers: −150 ± 70 kcal/d; p=.04 and high gainers: −230 ± 92 kcal/day; p=.01), but there was no difference between high gainers and low + ideal gainers (p=.49).
Author Manuscript
Conclusion—Interventions designed to increase adherence to the IOM guidelines for weight gain in pregnancy may have increased efficacy if focused on limiting energy intake while increasing nutrient density and maintaining levels of physical activity.
Address for correspondence: Leanne M. Redman, PhD, Pennington Biomedical Research Center, 6400 Perkins Rd, Baton Rouge, LA 70808, [email protected]. Financial Disclosure The authors did not report any potential conflicts of interest. Presented at Obesity Week November 11–16, 2013 in Atlanta, GA (T-79-OR).
Gilmore et al.
Page 2
Author Manuscript
Introduction Energy intake and energy expenditure are considered to be the two primary determinants of weight gain in humans. However, little is known regarding changes in energy intake and energy expenditure during pregnancy and the effect on gestational weight gain (GWG). Given that 48% percent of all pregnant women exceed the 2009 Institute of Medicine (IOM) recommendations for GWG (1), understanding the roles of energy intake and energy expenditure during pregnancy in relation to GWG is important for the development of successful weight management programs for this population.
Author Manuscript
Self-reported food intake is not different for women who achieved the recommended weight gain and those who had excessive weight gain (2). However, most individuals significantly under-report energy intake (3, 4) even during pregnancy (5). Objective assessments of energy intake are thereby critically important to enhance the fundamental understanding of how changes in energy intake contribute to weight gain in pregnant women. Many investigators believe compensatory changes in energy metabolism in response to increased food intake, contribute to the variability in weight gain (6–9). Furthermore, a low resting metabolic rate has been demonstrated to be a determinant of weight gain in nonpregnant adults (10). Quantifying the changes in energy metabolism during pregnancy in relation to GWG is needed to direct intervention strategies.
Author Manuscript
Using a unique dataset that includes prospective objective and highly reliable measures of energy intake and expenditure throughout pregnancy (11), we tested the hypothesis that when compared to those women who gain weight below or in accordance with the 2009 IOM guidelines for GWG, women will exceed the guidelines through the following mechanisms: 1) increased energy intake, 2) increased energy expenditure but less than expected for the changes in body composition, and 3) decreased physical activity.
Materials and Methods The parent study was approved by Institutional Review Board for Human Subject Research for Baylor College of Medicine and Affiliated Hospitals, funded by the United States Department of Agriculture and Department of the Army, and completed prior to 2007, and thus was not required to register with ClinicalTrials.gov. Individuals were recruited through local newspapers and community fliers. Informed written consent was obtained from each woman. LAG, LMR, ER, HH, JB received a dataset containing individual, de-identified data from NFB. The statistical analysis plan for this work was reviewed by the Institutional Review Board at Pennington Biomedical Research Center, but was exempt from approval.
Author Manuscript
This secondary analysis included 45 women with a body mass index of 18.5 – 35.4 kg/m2 who participated in a comprehensive study of changes in body composition and energy expenditure throughout pregnancy (11). The initial study included 63 women who were nonsmokers, nonanemic, normotensive, normoglycemic, and euthyroidic both at enrollment and throughout pregnancy. For this analysis, a priori criteria for exclusion included women with a BMI =30, these women were combined with the overweight women (BMI >=25); however, the respective BMI specific IOM recommendations were used to determine adherence. Those individuals who exceeded the IOM guidelines (n=19) were classified as “high gainers”. No women with a BMI ≥ 25 kg/m2 gained below the IOM recommendations, so individuals who gained below (n=12) or within (n=14) the IOM guidelines were combined into one group collectively classified as “low + ideal gainers”. Total GWG was calculated as weight gain between preconception and last measured study weight during pregnancy (36 weeks of gestation; Table 2).
Author Manuscript
The energy balance method provides a reliable estimation of energy intake during a period of weight change through the use of doubly labeled water to estimate total energy expenditure and quantification of the changes in body energy stores (i.e. fat mass and fat free mass). The energy balance theory relies on the assumption of linear weight gain, as does the IOM GWG recommendations in the second and third trimesters. Therefore, we used body composition changes between the second (week 22) and third trimester (week 36) to estimate energy intake during that period. Changes in fat mass and fat-free mass between the second and third trimester were converted to energy (kcal/d) using previously published energy coefficients for protein and fat deposition in pregnant women; 0.771 and 9.5 kcal/g, respectively (13). Total energy intake was the sum of total energy expenditure measured by doubly labeled water and the energy deposited as fat or fat free mass during that period (Table 2).
Basal metabolic rate was measured in a metabolic chamber (14) preconception, and at 9, 22 and 36 weeks of gestation. In brief, participants consumed meals at 0830, 1200, and 1730 with a snack at 1830. No food was allowed after 1900. Bedtime was at 2200. Participants were awakened at 0645, were asked to void, and returned to sleep. The participant was again awakened about 30 min later and basal metabolic rate was measured for 40 min while the
Obstet Gynecol. Author manuscript; available in PMC 2017 May 01.
Gilmore et al.
Page 4
Author Manuscript
participant remained motionless in bed. Basal metabolic rate was calculated by the Weir equation (15). Obligatory changes in basal metabolic rate were computed from the unadjusted data (absolute kcal/d). Adaptive changes in basal metabolic rateat the third trimester time point were determined as the difference between the measured basal metabolic rate and the basal metabolic rate predicted from a linear regression model for basal metabolic rate using fat mass and fat-free mass during the second trimester and maternal age at gestation as predictors (Table 2).
Author Manuscript
Details regarding the doubly labeled water method to determine total energy expenditure can be found in the parent study publication (11). In brief, after a baseline saliva sample was collected, the women received an oral dose of 100 ml of 2H2O and 125 mg H218O (Cambridge Isotope Laboratories) per kg body weight. A daily saliva sample was then taken for 13 days. Saliva samples were analyzed for hydrogen and oxygen isotope ratio measurements by gas-isotope-ratio mass spectrometry (16). Turnover rates of 2H and 18O were converted to total energy expenditure using the Weir equation (15) and a food quotient of 0.86, the value traditionally used based on the standard American diet (23). Adaptive changes in total energy expenditure at the third trimester were determined as the difference between the measured total energy expenditure and the predicted total energy expenditure. Predicted total energy expenditure was calculated from a linear regression model for total energy expenditure using fat mass and fat-free mass during the second trimester and maternal age at gestation as predictors (Table 2).
Author Manuscript
The energy expenditure of activity was estimated from non-basal energy expenditure where the thermic effect of food was assumed to be 10% of total energy expenditure for all individuals. The physical activity level was estimated as the ratio between total energy expenditure and basal metabolic rate.
Author Manuscript
Data in the text and tables are provided as mean ± SE. All calculations and data analyses were performed using SAS Version 9.4 (SAS Institute, Cary, NC). The changes in variables across pregnancy were analyzed by fitting linear models for repeated measures with adherence to the 2009 GWG Guidelines (low + ideal vs. high gainers) and BMI classification as covariates. Differences in these changes between groups were investigated by comparing least squares means via two-sample t-tests. Multiple linear regression models were used to generate equations for predicting Total energy expenditure and basal metabolic rate by utilizing data observed during the second trimester (n=45). Third trimester total energy expenditure and basal metabolic rate were predicted by plugging observed third trimester fat-free mass and fat mass values into the predictive equations. The differences between measured and predicted total energy expenditure and basal metabolic rate values were calculated and analyzed using linear models. Fisher’s exact test was used to assess relation of preconception BMI class and adherence to the IOM GWG Guidelines. P
Obstet Gynecol. Author manuscript; available in PMC 2017 May 01. Published in final edited form as: Obstet Gynecol. 2016 May ; 127(5): 884–892. doi:10.1097/AOG.0000000000001372.
Energy Intake and Energy Expenditure for Determining Excess Weight Gain in Pregnant Women L. Anne Gilmore, Ph.D.1, Nancy F. Butte, Ph.D.2, Eric Ravussin, Ph.D.1, Hongmei Han, M.S. 1, Jeffrey H. Burton, Ph.D.1, and Leanne M. Redman, Ph.D.1 1Pennington
Author Manuscript
2Baylor
Biomedical Research Center
College of Medicine
Abstract Objective—To conduct a secondary analysis designed to test whether gestational weight gain is due to increased energy intake or adaptive changes in energy expenditures.
Author Manuscript
Methods—In this secondary analysis, energy intake and energy expenditure of 45 pregnant women (BMI 18.5–24.9 kg/m2, n=33 and BMI ≥ 25, n=12) were measured preconceptionally 22, and 36 weeks of gestation. Energy intake was calculated as the sum of total energy expenditure measured by doubly labeled water and energy deposition determined by the 4-compartment body composition model. Weight, body composition, and metabolic chamber measurement were completed preconceptionally, 9, 22, and 36 weeks of gestation. Basal metabolic rate was measured by indirect calorimetry in a room calorimeter and activity energy expenditure by doubly labeled water. Results—Energy intake from 22 to 36 weeks of gestation was significantly higher in high gainers (n=19) (3437 ± 99 kcal/d) versus low + ideal gainers (n=26) (2687 ± 110 p< .001) within both BMI categories. Basal metabolic rate increased in proportion to gestational weight gain; however, basal metabolic rate adjusted for body composition changes with gestational weight gain was not significantly different between high gainers and low + ideal gainers (151 ± 33 vs. 129 ± 36 kcal/d; p=.66). Activity energy expenditure decreased throughout pregnancy in both groups (low + ideal gainers: −150 ± 70 kcal/d; p=.04 and high gainers: −230 ± 92 kcal/day; p=.01), but there was no difference between high gainers and low + ideal gainers (p=.49).
Author Manuscript
Conclusion—Interventions designed to increase adherence to the IOM guidelines for weight gain in pregnancy may have increased efficacy if focused on limiting energy intake while increasing nutrient density and maintaining levels of physical activity.
Address for correspondence: Leanne M. Redman, PhD, Pennington Biomedical Research Center, 6400 Perkins Rd, Baton Rouge, LA 70808, [email protected]. Financial Disclosure The authors did not report any potential conflicts of interest. Presented at Obesity Week November 11–16, 2013 in Atlanta, GA (T-79-OR).
Gilmore et al.
Page 2
Author Manuscript
Introduction Energy intake and energy expenditure are considered to be the two primary determinants of weight gain in humans. However, little is known regarding changes in energy intake and energy expenditure during pregnancy and the effect on gestational weight gain (GWG). Given that 48% percent of all pregnant women exceed the 2009 Institute of Medicine (IOM) recommendations for GWG (1), understanding the roles of energy intake and energy expenditure during pregnancy in relation to GWG is important for the development of successful weight management programs for this population.
Author Manuscript
Self-reported food intake is not different for women who achieved the recommended weight gain and those who had excessive weight gain (2). However, most individuals significantly under-report energy intake (3, 4) even during pregnancy (5). Objective assessments of energy intake are thereby critically important to enhance the fundamental understanding of how changes in energy intake contribute to weight gain in pregnant women. Many investigators believe compensatory changes in energy metabolism in response to increased food intake, contribute to the variability in weight gain (6–9). Furthermore, a low resting metabolic rate has been demonstrated to be a determinant of weight gain in nonpregnant adults (10). Quantifying the changes in energy metabolism during pregnancy in relation to GWG is needed to direct intervention strategies.
Author Manuscript
Using a unique dataset that includes prospective objective and highly reliable measures of energy intake and expenditure throughout pregnancy (11), we tested the hypothesis that when compared to those women who gain weight below or in accordance with the 2009 IOM guidelines for GWG, women will exceed the guidelines through the following mechanisms: 1) increased energy intake, 2) increased energy expenditure but less than expected for the changes in body composition, and 3) decreased physical activity.
Materials and Methods The parent study was approved by Institutional Review Board for Human Subject Research for Baylor College of Medicine and Affiliated Hospitals, funded by the United States Department of Agriculture and Department of the Army, and completed prior to 2007, and thus was not required to register with ClinicalTrials.gov. Individuals were recruited through local newspapers and community fliers. Informed written consent was obtained from each woman. LAG, LMR, ER, HH, JB received a dataset containing individual, de-identified data from NFB. The statistical analysis plan for this work was reviewed by the Institutional Review Board at Pennington Biomedical Research Center, but was exempt from approval.
Author Manuscript
This secondary analysis included 45 women with a body mass index of 18.5 – 35.4 kg/m2 who participated in a comprehensive study of changes in body composition and energy expenditure throughout pregnancy (11). The initial study included 63 women who were nonsmokers, nonanemic, normotensive, normoglycemic, and euthyroidic both at enrollment and throughout pregnancy. For this analysis, a priori criteria for exclusion included women with a BMI =30, these women were combined with the overweight women (BMI >=25); however, the respective BMI specific IOM recommendations were used to determine adherence. Those individuals who exceeded the IOM guidelines (n=19) were classified as “high gainers”. No women with a BMI ≥ 25 kg/m2 gained below the IOM recommendations, so individuals who gained below (n=12) or within (n=14) the IOM guidelines were combined into one group collectively classified as “low + ideal gainers”. Total GWG was calculated as weight gain between preconception and last measured study weight during pregnancy (36 weeks of gestation; Table 2).
Author Manuscript
The energy balance method provides a reliable estimation of energy intake during a period of weight change through the use of doubly labeled water to estimate total energy expenditure and quantification of the changes in body energy stores (i.e. fat mass and fat free mass). The energy balance theory relies on the assumption of linear weight gain, as does the IOM GWG recommendations in the second and third trimesters. Therefore, we used body composition changes between the second (week 22) and third trimester (week 36) to estimate energy intake during that period. Changes in fat mass and fat-free mass between the second and third trimester were converted to energy (kcal/d) using previously published energy coefficients for protein and fat deposition in pregnant women; 0.771 and 9.5 kcal/g, respectively (13). Total energy intake was the sum of total energy expenditure measured by doubly labeled water and the energy deposited as fat or fat free mass during that period (Table 2).
Basal metabolic rate was measured in a metabolic chamber (14) preconception, and at 9, 22 and 36 weeks of gestation. In brief, participants consumed meals at 0830, 1200, and 1730 with a snack at 1830. No food was allowed after 1900. Bedtime was at 2200. Participants were awakened at 0645, were asked to void, and returned to sleep. The participant was again awakened about 30 min later and basal metabolic rate was measured for 40 min while the
Obstet Gynecol. Author manuscript; available in PMC 2017 May 01.
Gilmore et al.
Page 4
Author Manuscript
participant remained motionless in bed. Basal metabolic rate was calculated by the Weir equation (15). Obligatory changes in basal metabolic rate were computed from the unadjusted data (absolute kcal/d). Adaptive changes in basal metabolic rateat the third trimester time point were determined as the difference between the measured basal metabolic rate and the basal metabolic rate predicted from a linear regression model for basal metabolic rate using fat mass and fat-free mass during the second trimester and maternal age at gestation as predictors (Table 2).
Author Manuscript
Details regarding the doubly labeled water method to determine total energy expenditure can be found in the parent study publication (11). In brief, after a baseline saliva sample was collected, the women received an oral dose of 100 ml of 2H2O and 125 mg H218O (Cambridge Isotope Laboratories) per kg body weight. A daily saliva sample was then taken for 13 days. Saliva samples were analyzed for hydrogen and oxygen isotope ratio measurements by gas-isotope-ratio mass spectrometry (16). Turnover rates of 2H and 18O were converted to total energy expenditure using the Weir equation (15) and a food quotient of 0.86, the value traditionally used based on the standard American diet (23). Adaptive changes in total energy expenditure at the third trimester were determined as the difference between the measured total energy expenditure and the predicted total energy expenditure. Predicted total energy expenditure was calculated from a linear regression model for total energy expenditure using fat mass and fat-free mass during the second trimester and maternal age at gestation as predictors (Table 2).
Author Manuscript
The energy expenditure of activity was estimated from non-basal energy expenditure where the thermic effect of food was assumed to be 10% of total energy expenditure for all individuals. The physical activity level was estimated as the ratio between total energy expenditure and basal metabolic rate.
Author Manuscript
Data in the text and tables are provided as mean ± SE. All calculations and data analyses were performed using SAS Version 9.4 (SAS Institute, Cary, NC). The changes in variables across pregnancy were analyzed by fitting linear models for repeated measures with adherence to the 2009 GWG Guidelines (low + ideal vs. high gainers) and BMI classification as covariates. Differences in these changes between groups were investigated by comparing least squares means via two-sample t-tests. Multiple linear regression models were used to generate equations for predicting Total energy expenditure and basal metabolic rate by utilizing data observed during the second trimester (n=45). Third trimester total energy expenditure and basal metabolic rate were predicted by plugging observed third trimester fat-free mass and fat mass values into the predictive equations. The differences between measured and predicted total energy expenditure and basal metabolic rate values were calculated and analyzed using linear models. Fisher’s exact test was used to assess relation of preconception BMI class and adherence to the IOM GWG Guidelines. P
