Effect of Circadian Distribution of Energy and Macronutrients on Gestational Weight Gain in Chinese Pregnant Women

Optimal Gestational weight gain (GWG) is essential to ensure the health of both the mother and the baby. However, GWG above or below the recommended guidelines of the Institute of Medicine is related to adverse perinatal outcomes, including gestational hypertension, gestational diabetes, cesarean delivery, premature birth, macrosomia, and infant mortality, as well as long-term negative outcomes in the offspring, including childhood obesity and adiposity [1,2]. Abnormal GWG is currently a serious obstetric issue. For example, in the United States, weight gained is higher than the Institute of Medicine-recommended range in 48% of women giving birth to full-term singleton infants, with 21% gaining insufficient weight [3]. In China, inadequate and excessive weight gain account for 27.2% and 36.6%, respectively [4]. On average, maternal weight increases as pregnancy progresses. The fastest weight gain occurs in the second trimester, and the weight gain rate in the third trimester slightly decreases [5]. In the second and third trimesters, weight gained includes maternal fat accumulation, extravascular fluid, placenta, uterus, and fetus growth [6]. Therefore, it is necessary to simultaneously pay attention to the GWG during the second and third trimesters and explore the associated factors.

Emerging evidence suggests that the timing of food intake may affect weight gain. For instance, skipping breakfast, eating lunch late, and eating a large dinner have been associated with various indices of obesity [7]. Nevertheless, this subject has not been sufficiently studied in Chinese pregnant women, and one main methodological limitation is defining meal timing; conventional meal categories (i.e., breakfast, lunch, and dinner) and clock timing (external timing) to characterize meal timing may fail to accurately relate metabolic alterations in the context of the internal circadian rhythm [8]. Dim light melatonin onset is the recommended method for assessing the biological timing (internal circadian timing), which demands participants to stay in dim light conditions for a whole evening or more and undergo repeated blood or saliva collections to measure melatonin concentrations [9]. However, this method is unpractical for most epidemiological or clinical studies. A more practical approach to estimating the circadian time of food intake is to consider the timing of food intake relative to the sleep/wake cycle [10]. Moreover, changing an individual’s meal timing in a real-world setting may be difficult, but changing the daily distribution of energy or macronutrients may be achievable. Therefore, in the present study, we investigated dietary intake and sleep/wake timing in the second and third trimesters to define mealtimes relative to sleep/wake timing. We examined the associations between individual daily energy and macronutrient distribution, macronutrient intake in different time windows, and GWG.

Pregnant women were classified into mutually exclusive dietary patterns by latent profile analysis. Latent profile analysis could identify unobserved heterogeneity in multiple continuous response variables. The Akaike information criterion (AIC), Bayesian information criterion (BIC), and sample-size-adjusted BIC (aBIC) were used to determine the best-fitting latent profile model. Additionally, the Vuong, Lo, Mendell, and Rubin likelihood ratio test was used to determine whether adding an additional profile contributed to a significantly better-fitting model [19].

For continuous variables, the Shapiro–Wilk test was used to assess the distribution of variables. Data with parametric distribution are described as mean and standard deviation and were compared using the one-way analysis of variance or t-test. Data with nonparametric distribution are described as median and interquartile range and were compared using the Kruskal–Wallis or Mann–Whitney U tests. For categorical variables, data are described as numbers (percentages) and were compared using the chi-squared test or Fisher’s exact test. Multiple comparisons were conducted using the Bonferroni post hoc test when necessary.

The Sample Wilcoxon Signed Rank Test was used to evaluate the adequacy of GWG in pregnant women with different dietary patterns. Spearman’s correlation was used to explore correlations among macronutrient intake in different time windows and the GWG. Multiple Linear Regression Models (method = backward) were used to determine the effects of dietary patterns (independent variables) and macronutrient intake in different time windows (independent variables) on the adequacy of weight gain (dependent variable). Models were adjusted for age, educational level, employment status, household income, pregestational BMI, parity, the condition of gestational diabetes mellitus, gender of offspring, physical activity, daily sleep duration, time node of the time window, number of eating episodes, total energy intake, and gestational week of delivery. p < 0.05 was considered statistically significant. Statistical analyses were performed using SPSS version 24 and Mplus version 6.0.

To the best of our knowledge, the present study is the first to be conducted on Chinese pregnant women to investigate the effects of daily energy and macronutrient distribution on GWG during the second and third trimesters.

Our study findings showed that the proportion of pregnant women with an inadequate, adequate, or excessive trimester-specific mean rate of GWG (14.3%, 33.3%, 52.4% in the second trimester; 22.2%, 24.1%, 53.7% in the third trimester) and total GWG (23.9%, 45.7%, 30.4%) was approximately similar to some studies [4,20,21,22]. However, it differed from a large retrospective cohort study conducted with Chinese singleton pregnant women with gestational diabetes mellitus [23]. This large population-based study was conducted with Chinese singleton pregnant women who delivered between January 2011 and December 2017 in Beijing [24]. However, this could be due to the differences between populations, such as physical conditions and regional dietetic culture.

Though neither daily energy intake nor physical activity differed significantly across all dietary patterns in the present study, we found that pregnant women with the high late afternoon–early evening distribution in the second and third trimesters appeared to have excessive GWG rates; macronutrient (carbohydrate, fat, and protein) intake in the late afternoon–early evening time window of the second trimester was associated with greater GWG rates. Moreover, pregnant women who had a relatively high average energy and macronutrient distribution in late afternoon–early evening time window exhibited a greater GWG rate and a greater total GWG than in the morning time window during the third trimester. These findings are consistent with other studies conducted in pregnant women [15,25] and non-pregnant adults [8,26,27], which supported that higher intake in the evening was associated with a higher risk of weight gain. A potential mechanism may be associated with circadian changes in total energy expenditure, including resting metabolic rate and the thermic effect of food [28]. Randomized crossover trials reported that the endogenous circadian rhythm in the total energy expenditure of healthy adults peaked in the biological morning or early afternoon and was lower in the biological evening [29,30]. If the total energy expenditure was reduced, coupled with high energy-dense food intake, it might cause a positive energy balance in pregnant women as a contributing factor for excessive weight gained.

Additionally, we found that pregnant women with high late morning–early afternoon distribution in the second trimester with high morning distribution in the second and third trimesters experienced excessive GWG rates or excessive total GWG. Protein intake in the late morning–early afternoon time window of the second trimester, carbohydrate intake in the morning time window of the second trimester, carbohydrate intake in the late morning–early afternoon time window of the third trimester, and carbohydrate and fat intake in the morning time window of the third trimester was associated with greater GWG rates or greater total GWG. This finding is inconsistent with other studies conducted on pregnant women [15,25] and non-pregnant adults [8,26,27,31], which supported that higher morning or lunch intake was associated with a lower risk of weight gain. One possible reason is the difference between Chinese and Western food cultures. Taking breakfast as an example, nearly 90% of Chinese ingested cereals and tubers products (rich in carbohydrates), approximately 50% ingested vegetables, fruits, meat, fish, eggs, and milk, and only approximately 30% ingested beans and nuts [32]. In our study, participants with high morning distribution or high late morning–early afternoon distribution did not have a better diet quality for fruit components, milk, and nuts [33,34]. There is no significant difference in micronutrient intake across four dietary patterns (shown in Table S2). Much deep-fried food (rich in carbohydrates and fat) belongs to traditional Chinese breakfasts, such as dough sticks [35]. A previous study showed 4–8 weeks of overfeeding healthy adults with a high-fat breakfast resulted in 2–4 kg of weight gain [36], and a high-fat breakfast did not change satiety a few hours after breakfast [37]. Additionally, an increase of 1 g of carbohydrates was related to an increment of 17 g in weight during pregnancy. In comparison, 1 g of sugar was associated with an increase of 26 g of weight during pregnancy [38].

Interestingly, we found protein intake in the morning time window of the second trimester, protein intake in the late afternoon–early evening and morning time window of the third trimester, and fat intake in the late morning–early afternoon time window of the third trimester were negatively associated with the GWG rates or total GWG. This could be because foods high in protein are typically less energy dense. In healthy women, high-protein intake has a greater effect on satiety and appetite control and less subsequent food intake [39]. Though there is no significant difference in micronutrient intake across four dietary patterns, participants in our study were accustomed to eating food rich in monounsaturated and polyunsaturated fatty acids as snacks in the late morning–early afternoon time window. For instance, in nuts and yogurt, monounsaturated and polyunsaturated fatty acids have been found to contribute to weight loss and obesity prevention [40]. The total GWG was related more closely to eating behavior during the third trimester. This could be due to nonmonotonic fetal growth. However, the biparietal diameter and head circumference show an accelerated increase in the second trimester, while the abdominal circumference and estimated fetal weight velocity peak in the third trimester [41]. Another possible cause was the dietary counseling [42] after BMI monitoring in the second trimester; some pregnant women (65.2%, not shown in the result) in our study changed their dietary patterns after the second trimester.

This study has many strengths. First, we concurrently collected data about sleep timing and meal timing, which enabled us to establish an index indicating the circadian time of food intake. Second, we used a prospective design to assess multiple time points of sleep timing and dietary recalls, which reduced the potential effect of seasonal fluctuations in sleep timing and meal timing. Third, we considered the relationship between relative and absolute energy and macronutrient intake and GWG, since this is achievable in weight management during pregnancy. This study also has several limitations. The study was conducted on relatively healthy women in early pregnancy; therefore, the results of this study cannot be generalized to all pregnant women, especially those with high-risk pregnancies. A small sample size of pregnant women with higher night distribution hinders the observation of the association between the night distribution of energy and macronutrients and GWG. Moreover, a more detailed classification of nutrient consumption was not considered, such as saturated fatty acids, monounsaturated fatty acids, and polyunsaturated fatty acids. Future studies with more comprehensive investigations of sleep status and diet conditions in a larger population of pregnant women are needed.

Excessive GWG of Chinese pregnant women was related closely to eating behavior focused on the late afternoon–early evening time window and carbohydrate and fat intake in the morning during the second and third trimesters. Our findings emphasize that it is necessary to pay attention to Chinese pregnant women with high energy and macronutrient distribution in the late afternoon–early evening and adjust the macronutrient intake based on internal circadian timing for GWG management. Additionally, clinicians should provide more well-directed nutritional advice for pregnant women in different trimesters.