Frequency of Eating During Pregnancy and Its Effect on Preterm Delivery
Anna Maria Siega-Riz1,2,
Tracy S. Herrmann1,
David A. Savitz3 and
John M. Thorp4
1 Department of Nutrition, University of North Carolina, Carolina Population Center, Schools of Public Health and Medicine, Chapel Hill, NC.
2 Department of Maternal and Child Health, University of North Carolina, Carolina Population Center, School of Public Health, Chapel Hill, NC.
3 Department of Epidemiology, University of North Carolina, Carolina Population Center, School of Public Health, Chapel Hill, NC.
4 Department of Obstetrics and Gynecology, University of North Carolina, Carolina Population Center, School of Medicine, Chapel Hill, NC.
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ABSTRACT
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Frequency of eating or meal patterns during pregnancy may be a component of maternal nutrition relevant to pregnancy outcome. To identify meal patterns of pregnant women and investigate the relation between these meal patterns and preterm delivery, the authors performed an analysis using data from the Pregnancy, Infection, and Nutrition Study (n = 2,065). Women recruited from August 1995 to December 1998 were categorized by meal patterns on the basis of their reported number of meals (breakfast, lunch, and dinner) and snacks consumed per day during the second trimester. An optimal pattern was defined according to the Institute of Medicine recommendation of three meals and two or more snacks per day. In this population, 72 percent of the women met this recommendation, and 235 delivered preterm. Women who consumed meals/snacks less frequently were slightly heavier prior to pregnancy, were older, and had a lower total energy intake. In addition, these women had a higher risk of delivering preterm (adjusted odds ratio = 1.30, 95 percent confidence interval: 0.96, 1.76). There was no meaningful difference in the risk by early versus late preterm delivery, but those who delivered after premature rupture of the membranes (adjusted odds ratio = 1.87, 95 percent confidence interval: 1.02, 3.43) had a higher risk than those who delivered after preterm labor (adjusted odds ratio = 1.11, 95 percent confidence interval: 0.64, 1.89). This study supports previous animal model work of an association between decreased frequency of eating and preterm delivery.
delivery; eating; pregnancy
Abbreviations:
BMI, body mass index; IOM, Institute of Medicine; PIN, Pregnancy, Infection, and Nutrition
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INTRODUCTION
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Frequency of eating or meal patterns during pregnancy may be a component of maternal nutrition relevant to pregnancy outcome. In 1990, the Institute of Medicine (IOM) convened a panel of experts to summarize the current literature on the nutritional status of women during pregnancy (1
). On the basis of this report, a subcommittee published a guide that provided practical information to health care providers in which it was recommended that pregnant women "eat small to moderate-sized meals at regular intervals, and eat nutritious snacks" (2
, p. 45) in order to meet the increased nutritional needs during pregnancy. However, to our knowledge, there are no published reports to substantiate this recommendation for nondiabetic women. Meal patterning during pregnancy may be important because pregnant women who sustain prolonged periods of time without food by skipping meals and/or snacks may be inducing a physiologic stress upon their pregnancy. Experimental evidence from animal studies suggests that as little as 24 hours without food may decrease the length of gestation (3

6
). In humans, spontaneous term delivery rates increased dramatically after 24 hours of fasting for Yom Kippur (7
). Prolonged periods of time without food can cause hypoglycemia, which stimulates a cascade of neuroendocrine events that may ultimately affect the health of the fetus (8
, 9
). Thus, meal patterns may have important implications on pregnancy outcomes, but no one has evaluated this association. The purposes of this study were to characterize the meal patterns of pregnant women and to examine the relation between these meal patterns and both early and late preterm delivery as well as the clinical presentations leading to prematurity.
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MATERIALS AND METHODS
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Study design and sample
The Pregnancy, Infection, and Nutrition Study (PIN) is a prospective cohort study of risk factors for preterm birth in North Carolina. The study recruits predominantly lower- to middle-income women from four prenatal care clinics in two settings: the University of North Carolina Resident and Private Physician Obstetrics Clinic and the Wake County Departmennt of Human Services and Wake Area Health Education Center Prenatal Care Clinics. Women were recruited into the study between 24 and 29 weeks gestation. Genital tract, blood, and urine specimens were collected at the time of recruitment. Several questionnaires were also self-administered at that time, including a food frequency questionnaire for dietary intake. Women were also interviewed by telephone regarding sociodemographic data, health habits, and their previous as well as current medical histories. Birth outcome information was obtained from hospital delivery logs. The procedures followed for this study were in accordance with the ethical standards of the Institutional Review Board of the University of North Carolina School of Medicine and Wake Area prenatal clinics.
The recruitment period reflected in this analysis is August 1995 to December 1998. During this time, 4,160 women were determined to be eligible, and 2,505 (60 percent) were successfully recruited into the PIN Study. Slightly more White than Black women were recruited into the PIN Study compared with women who refused to participate in the study. More notable differences were found when comparing the different study sites, with the health department clinics having a greater proportion of refusals and more women who could not be contacted than did the teaching hospital. The study had somewhat greater success recruiting highly educated (>16 years of education) and older (age >35 years) women. The risk of preterm birth was slightly higher among the successfully recruited women than among those who refused (10
).
Of these successfully recruited women, 2,247 (90 percent) completed the food frequency questionnaire, and 2,081 also had information available on sociodemographics, prenatal care, and health behaviors from the other questionnaires necessary for this analysis. Sixteen women did not have sufficient data to determine their meal patterns, leaving 2,065 women for the analysis.
Birth outcomes
Gestational age was assessed on the basis of a reliable, self-reported estimate of last menstrual period, when available (70.8 percent), or an ultrasound procedure performed early in pregnancy if the date of the last menstrual period was unknown (10 percent). When both were available and the two estimates were within 14 days of one another, the date of the last menstrual period was used (6.3 percent). When the disagreement exceeded 14 days, the ultrasound estimate was used (12.8 percent). Preterm birth was defined as a delivery prior to 37 completed weeks of gestation. The charts of all preterm deliveries were examined by a team of three obstetricians to determine whether the delivery was spontaneous or medically induced as well as the clinical presentations (preterm labor or premature rupture of the membranes). Thus, preterm deliveries were further subdivided into early (<34 weeks) and late (>3437 weeks) preterm as well as preterm labor, premature rupture of the membranes, or medical induction. Thirty-three women did not have gestational age data available and thus were not included in the multivariate analysis examining the risk of meal frequency on preterm birth (n = 2,032).
Primary exposure and selected covariates
On the food frequency questionnaire, women were asked to indicate how many meals and snacks they usually ate per day as well as the time that the meals and snacks were consumed (figure 1). The interpretation of what a meal or snack consisted of was left up to their discretion. Women were specifically requested to recall their dietary behaviors during the second trimester of pregnancy. This information was then used to create a meal pattern variable for the purpose of this analysis.

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FIGURE 1. Questions used to ascertain information concerning meal patterns during the second trimester of pregnancy, Pregnancy, Infection, and Nutrition Study, 19951998
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Information on potential confounders was obtained from questionnaires and medical records. During the telephone interview, women were asked whether they experienced nausea or vomiting during the first two trimesters, as well as their race, religious affiliation, work status, income, years of education, prenatal supplement use, and amount of time spent in recreational physical activities. Information concerning dietary intake was collected by using a modified National Cancer Institute-Block questionnaire with updated nutrient values based on data from the US Department of Agriculture 19941996 Continuing Survey of Food Intake by Individuals for women aged 1944 years. This questionnaire has been validated in numerous studies and in a variety of populations (11

14
). Slight modifications were made to include local foods, to focus on a 3-month time period (reflecting a trimester), to be specific for pregnancy, and to incorporate the latest recommendations for improving diet quality (15
). Information obtained from the medical record included age at time of conception as well as weight and height measurements for the determination of prepregnancy body mass index (BMI).
Statistical analysis
Crude risk ratios of the effect of meal pattern on the birth outcomes of interest were calculated. For this comparison, we considered women who ate three meals and two or more snacks per day as the referent group, since this meal pattern best represents the IOM recommendation. Descriptive statistics were generated, and a Student t test or a chi-square test was used to evaluate the statistical significance (p < 0.05) of various sociodemographic as well as health behavior characteristics of the women between the two meal pattern groups. Logistic regression was used to control for multiple covariates in the analysis. Selection of potential confounders was determined from findings reported in the literature on factors that may affect meal patterns as well as preterm birth (16


20
). These included maternal age, nausea and vomiting, smoking, pregravid BMI, height, total energy intake, prenatal supplement use, and income as a percentage of poverty. All potential confounders were entered into the model, and only those that changed the beta coefficient of the meal pattern variable by greater than 10 percent were retained. The adjusted odds ratios and 95 percent confidence intervals were then calculated. SAS software (SAS version 6.12, Cary, North Carolina,1996) was used for the data management, and STATA (STATA version 6.0, 1999, Stata Corporation, College Station, Texas) was used for statistical calculations.
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RESULTS
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The PIN Study population represents a mix of African-American (42 percent) and Caucasian (51 percent) pregnant women as well as 7 percent from other races. The age distribution of the women was as follows: ages 1517 years, 7 percent; ages 1824 years, 44 percent; ages 2534 years, 41 percent; and age 35 years and over, 8 percent. Twenty-one percent had not completed high school, and 53.6 percent were not currently married. Twenty-nine percent of the women were nulliparous, 62.5 percent were below 185 percent of the poverty index (the cutoff used for welfare and food and nutrition assistance programs), and 79 percent were employed at the time of the telephone interview. The prevalence of preterm birth in this population was 11.4 percent.
Numerous meal patterns were reported and initially aggregated into seven distinct categories as shown in table 1. The majority of women reported consuming three meals plus two or more snacks per day. The small number of women who consumed only three meals without snacks or one meal with or without snacks per day had the highest rates of preterm birth (table 1).
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TABLE 1. Distribution of women in the Pregnancy, Infection, and Nutrition Study according to meal patterns and the prevalence of preterm birth for each pattern (n = 2,065), 19951998
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Meal pattern categories were further collapsed into two groups for analysisthose who came closest to meeting the IOM recommendation of three meals plus two or more snacks versus all others. Women who consumed meals less frequently were, on average, slightly heavier prior to pregnancy, older, and less compliant with taking their prenatal supplement than were those who met the IOM recommendation (table 2). The total energy intake of women who met the IOM recommendation was significantly higher than that of women with less than the optimal frequency of food intake.
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TABLE 2. Selected characteristics of women from the Pregnancy, Infection, and Nutrition Study according to meal patterns, 19951998
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The crude relative risk of delivering preterm for women with less than optimal meal frequencies compared with the recommended IOM meal pattern was 1.27 (95 percent confidence interval: 0.98, 1.63). The risk for delivering very early, at less than 34 weeks, was higher than that of delivering later in gestation (table 3). Examination of the clinical presentations of preterm birth revealed a significantly higher risk for delivering after premature rupture of the membranes compared with no increased risk for preterm labor among women with less than optimal meal frequencies.
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TABLE 3. The effect of not following the Institute of Medicine recommendation for the number of meals and snacks (3 meals and ±2 snacks) on preterm delivery for women in the Pregnancy, Infection, and Nutrition Study (n = 2,032),* 19951998
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Of all the potential confounders considered for this analysis, only pregravid BMI, total energy intake, and supplement use remained in the model. Results from the logistic regression analysis (table 3) showed very little change in the magnitude of risk for all outcomes examined. When we excluded medically induced preterm deliveries, the risk for early preterm birth decreased slightly, whereas the risk for preterm birth in general and for late preterm birth increased. The confidence intervals widened, reflecting the imprecision due to the small number of cases.
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DISCUSSION
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This study demonstrates that the majority of pregnant women in this biracial population met the IOM recommendation to consume three meals and two or more snacks per day. Women who consumed food at a less optimal frequency were at a slightly higher risk for delivering preterm in general and were more likely to deliver after premature rupture of the membranes. This effect was independent of total energy intake, pregravid BMI, and supplement use.
On the basis of studies conducted by Fowden and others (2

5
), we hypothesized that women who skipped meals or had no snacks during the day would be causing a physiologic stress on their bodies by extending the time period without food. Khatun et al. (21
) found elevated levels of corticotrophin-releasing factor, epinephrine, norepinephrine, and insulin in pregnant rats that were fasted for 12 hours, demonstrating the plausibility of this pathway. If skipping meals is similar to other types of stressors studied previously, such as psychologic stress, then the cascade of events that lead to preterm birth would be triggered (22
24
). In this respect, meal patterning would then be an antecedent of preterm birth and not a marker of this outcome. This study is the first step in demonstrating this causal pathway to preterm delivery. The fact that the risk was higher for those women who delivered after premature rupture of the membranes and not after preterm labor does not refute this pathway. Studies by those who examine amniochorionic membrane properties have found that repeated stretching of the amniochorionic membranes, as in the case of cyclic uterine contractions, can increase the likelihood of the membranes rupturing (25
, 26
).
To our knowledge, there are no published data examining the frequency of eating during pregnancy in humans or its effect on birth outcomes outside of the diabetic state. Research on the metabolic effects of eating frequency in general have demonstrated that increasing the frequency of eating may be related to positive physiologic adaptations such as the lowering of blood cholesterol and improved blood glucose control (27

30
).
Some of the issues that are important to consider when examining eating patterns in humans are the definition used to describe the eating occasions as well as the method used to collect the information on frequency of eating. The use of self-defined meals is common in the field of nutrition. An alternative approach is to create a definition of a meal or snack based on the caloric or food content of the eating occasion. There are many flaws with this approach as well, and to date, there is no consensus about the best method for defining meals and snacks. Classification of eating occasions as meals and snacks by the subject is open to individual and cultural interpretation. The time interval between food intake and the quantity of food intake may also impact the way an individual chooses to describe an eating occasion. Hence, inaccurate reporting may also be a source of error when quantifying eating frequency. In this study, we used a self-report of the number of meals and snacks that a woman usually consumed during her second trimester of pregnancy. This pattern may have changed throughout the course of pregnancy. Thus, future studies should examine changes in meal patterns and/or critical time windows during pregnancy for when meal patterns may have the most detrimental effect on birth outcomes.
Other limitations worthy of acknowledgment include uncertain gestational age estimation and selective participation. This study used an algorithm that synthesizes information on the reported date of the last menstrual period with an ultrasound taken before 20 weeks gestation to ascertain the gestational age at delivery. In addition, the charts of all preterm deliveries were examined by three obstetricians to determine the certainty of the gestational age and the clinical presentation at delivery. Despite our attention to how preterm birth was ascertained, misclassification of gestational age is still a possibility. The recruitment period of the study excludes women who enter into prenatal care late and those without prenatal care from participating. Thus, higher-risk women are likely to be excluded. As a result, our findings may not be generalizable to other populations.
Biologic markers of stress are needed to better examine the relation between frequency of food consumption and preterm birth. However, if our results are corroborated by others, measuring the frequency of a woman's meal and snack intake may be a simple and useful public health tool for evaluating the adequacy of the prenatal diet and identifying women at increased risk of preterm delivery.
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ACKNOWLEDGMENTS
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Supported by a grant from the National Institute of Child Health and Human Development, National Institutes of Health (grant HD28684), by the Institute of Nutrition, and by funds from the Wake Area Health Education Center, Raleigh, North Carolina.
The Pregnancy, Infection, and Nutrition Study is a joint effort of many investigators and staff members whose work is gratefully acknowledged.
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NOTES
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Reprint requests to Dr. Anna Maria Siega-Riz, Carolina Population Center, CB # 8120 University Square, University of North Carolina at Chapel Hill, Chapel Hill, NC 275163997 (e-mail: am_siegariz{at}unc.edu).
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Received for publication March 27, 2000.
Accepted for publication July 18, 2000.