Patterns of Alcohol Use Before and During Pregnancy and the Risk of Small-for-Gestational-Age Birth

Nedra Whitehead  and Leslie Lipscomb

From the Division of Reproductive Health, National Center for Chronic Disease Prevention and Health Promotion, Centers for Disease Control and Prevention, Atlanta, GA.

Received for publication December 5, 2002; accepted for publication April 17, 2003.


    ABSTRACT
 TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 ACKNOWLEDGMENTS
 REFERENCES
 
Few studies have examined the effect of binge drinking on human fetal growth. The authors studied the effect of binge drinking 3 months before pregnancy and during the last 3 months of pregnancy on small-for-gestational-age (SGA) birth, using data from the Pregnancy Risk Assessment Monitoring System (PRAMS). PRAMS is an ongoing US survey of women who recently delivered a liveborn infant. Data are collected 2–6 months after birth by using mailed, self-administered questionnaires, with telephone interviews conducted for nonresponders. This study included 50,461 women who delivered at term from 1996 to 1999. Overall, binge drinkers before pregnancy were less likely than nondrinkers to have an SGA birth, but moderate or heavy drinkers (>=4 drinks per week) who also binged were 2.2 times more likely to have an SGA birth. Moderate and heavy drinkers in late pregnancy were also more likely to have an SGA birth, but there were only 46 women in these categories, so estimates were imprecise. Vascular effects of alcohol or dietary differences between drinkers and nondrinkers may explain the lower risk of SGA birth among some drinkers. The relation of these areas with fetal growth needs more research.

alcohol drinking; birth weight; growth; infant, newborn; pregnancy

Abbreviations: Abbreviations: PRAMS, Pregnancy Risk Assessment Monitoring System; SGA, small for gestational age.


    INTRODUCTION
 TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 ACKNOWLEDGMENTS
 REFERENCES
 
The effect of chronic heavy alcohol consumption during pregnancy on fetal growth is well documented. Fetal growth restriction, with mental retardation and facial anomalies, is a defining characteristic of fetal alcohol syndrome (1, 2). Alcohol consumption may also be associated with growth restriction alone, especially if alcohol use persists into the last trimester of pregnancy (35).

The effects of light or moderate alcohol use are unclear. Lundsberg et al. (6) found low-to-moderate alcohol use to be protective against intrauterine growth restriction. Lazzeroni et al. (7) did not find any significant relation between light or moderate alcohol use and low birth weight, and Mills et al. (3) found that, compared with infants of nondrinkers, infants of light drinkers were 14-g lighter and at an 11 percent higher risk of low birth weight and that infants of moderate drinkers were 83-g lighter and at a 62 percent higher risk of low birth weight.

Researchers have become interested in whether occasional binge drinking, in the absence of chronic heavy drinking, affects pregnancy outcome. Gladstone et al. (8) recently reviewed the evidence for such effects. They reported that studies with rats suggest that peak alcohol concentration, rather than total amount of alcohol consumed, determines the effect of alcohol and that binge drinking early in pregnancy followed by abstinence in pigtailed macaques affect-ed fetal development as much as exposure throughout pregnancy.

We studied the effect of different patterns of drinking on term small-for-gestational-age (SGA) birth by using data from the Pregnancy Risk Assessment Monitoring System (PRAMS) on alcohol use before pregnancy and in late pregnancy, the time periods for which PRAMS collects information on alcohol use. We asked the following two questions:

1. Does the risk of SGA birth increase as reported alcohol consumption before pregnancy increases?

2. Among women whose average alcohol consumption is similar, do binge drinkers have a higher prevalence of SGA births than drinkers who do not binge?


    MATERIALS AND METHODS
 TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 ACKNOWLEDGMENTS
 REFERENCES
 
PRAMS
PRAMS is a US federal-state cooperative survey of women who recently delivered a liveborn infant (9, 10); the survey is designed to provide state-specific, population-based data for planning state public health programs. Participating states are selected through the Centers for Disease Control and Prevention’s objective review process. Currently, 31 states and one city participate in PRAMS. The PRAMS participating states, questionnaire, and methodology are available on the PRAMS Web site: http://www.cdc.gov/nccdphp/drh/srv_prams.htm.

A stratified, systematic sample of women who delivered a liveborn infant is drawn from a state’s birth certificate file. Sample design and sampling fractions differ by state and change over time. Birth weight, race, and geographic region are common stratification variables. Sampled women are mailed a self-administered questionnaire 2–6 months after delivery, with a telephone follow-up for those who do not respond to the mailed survey.

PRAMS has been approved by the Centers for Disease Control and Prevention and individual state institutional review boards. The mailing packet and telephone introductory script contain information on PRAMS, its purpose, and its goals and indicate that participation is voluntary. Informed consent is implied by completing the survey or agreeing to proceed with the interview.

The PRAMS data set contains questionnaire data, selected birth certificate information, and selected information on the timing and mode of data collection. The data are weighted to account for the sampling design, nonresponse, and noncoverage (Centers for Disease Control and Prevention, Atlanta, Georgia, 1996, unpublished data). We used data for births occurring from 1996 through 1999, the years for which data on binge drinking were available. We used data for states and years only when the response rate was at least 70 percent. The analysis includes 1–4 years of data from 19 states: Alabama, Alaska, Arkansas, Colorado, Florida, Georgia, Illinois, Louisiana, Maine, Michigan, New Mexico, New York, North Carolina, Ohio, Oklahoma, South Carolina, Utah, Washington, and West Virginia.

Subject characteristics
We limited our analysis to women who delivered singleton full-term infants because we thought that the etiology of SGA might differ for preterm and term infants. A term birth was defined as occurring at between 37 and 42 weeks of gestation, as calculated from the last menstrual period or clinical gestational age reported on the birth certificate by using the algorithm described by Alexander et al. (11). If gestational age could not be determined by the last menstrual period or clinical week, we calculated it from the infant’s date of birth and the due date reported on the questionnaire. Gestational age was based on last menstrual period for 77 percent of records, clinical estimate for 20 percent of records, and due date for 3 percent of records. Records that contained incompatible infant birth weight and gestational age, based on the criteria used by Adams et al. (12), were excluded. Gestational age or birth weight was missing for 2,577 (3.9 percent) records. SGA was defined as birth weight less than the 10th percentile for the infant’s gestational age according to the race- and parity-specific standards published by Zhang and Bowes (13). Birth-weight-for-gestational-age standards were available for only Black infants and White infants. A total of 65,969 sampled women met the study criteria—Black women and White women who delivered at term—and 50,461 respondents, a 76 percent response rate among the study population.

PRAMS asks a woman about her alcohol consumption during the 3 months before she became pregnant and the last 3 months of her pregnancy. For each time period, a woman is asked the number of drinks she consumed in an average week and the number of times she drank five or more drinks at one sitting. We categorized a woman as a nondrinker if she reported no alcohol use during the relevant time frame, a light drinker if she reported three drinks or less in an average week, a moderate drinker if she reported four to 13 drinks in an average week, and a heavy drinker if she reported 14 or more drinks in an average week. A woman was considered to have binged if she reported drinking five or more drinks in one sitting once or more during the relevant time period. If a woman reported more binges during the 3 months than was consistent with the number of drinks she reported having in an average week, average consumption was recoded to the higher level. For example, a woman who reported less than one drink per week in an average week but also reported 12 binges in a 3-month time period would be coded as drinking four to six drinks in an average week. Data were recoded in this way for 516 women. Information for women was missing on average alcohol consumption before pregnancy for 2.3 percent, on binge drinking before pregnancy for 6.8 percent, on average alcohol consumption in late pregnancy for 1.6 percent, and on binge drinking in late pregnancy for 2.0 percent.

The infant’s birth certificate was our source for maternal race, age, marital status, and weight gain during pregnancy. Data on smoking, source of income, and prepregnancy height and weight are collected by the PRAMS questionnaire. Prepregnancy weight was categorized according to body mass index (calculated as height (in meters) divided by weight (in kilometers) squared) as less than 19.8, underweight; 19.9–26.0, normal weight; and more than 26.0, overweight.

Statistical analysis
The study was designed as a retrospective cohort analysis. SUDAAN software (14) was used to compute the prevalence of SGA infants among women with different patterns of alcohol use. Logistic regression was conducted by using SAS software (15) to model the association between patterns of alcohol use and SGA while controlling for variables that have been shown to be associated with binge drinking and with alcohol consumption. We examined maternal race, age, marital status, parity, smoking in the last 3 months of pregnancy, prenatal care initiation, and income from public assistance (measure of socioeconomic status) as potential confounders because they previously were associated with alcohol consumption or binge drinking and with fetal growth (1619), and we also studied prepregnancy body mass index because it is associated with SGA birth (20, 21). Stratification variables and state of residence were included to control for the sampling designs. We examined interactions with prepregnancy weight and smoking to determine whether they modified the effect of binge drinking on SGA birth. Neither interaction was significant. We kept a variable in the model if its removal changed the estimated odds ratio for the association between alcohol use and SGA by more than 5 percent or if the variable improved the fit of the model. Maternal race and parity were controlled through the birth-weight-for-gestational-age standards. Including them in the model did not affect the estimated odds ratio and adversely affected model fit. The covariates included in the final model were maternal age, education, marital status, prepregnancy weight status, receipt of income from public assistance, state of residence, and smoking status before pregnancy.

Only the 39,709 women for whom data for all analysis variables were nonmissing were included in the modeling analyses. The distribution of the variables in the model for the represented population (i.e., residents of the included states who delivered a liveborn infant in that state during the included years) of sampled women, questionnaire respondents, and respondents for whom data were complete are given in table 1. The distribution in the represented population was calculated as the distribution of the variable among the questionnaire respondents, weighted to account for the sampling design, survey nonresponse, and frame noncoverage.


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TABLE 1. Distribution of study variables, Pregnancy Risk Assessment Monitoring System, United States, 1996–1999*
 

    RESULTS
 TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 ACKNOWLEDGMENTS
 REFERENCES
 
The majority of the 50,749 women in this study were White (75.7 percent), were aged 18–34 years (83.3 percent), had 12 or more years of education (75.4 percent), were married (62.2 percent), were not on public assistance (81.0 percent), and were nonsmokers in late pregnancy (82.2 percent) (table 1). Forty-nine percent were of normal weight before pregnancy, and 26 percent were overweight. Sixteen percent of study participants delivered an SGA infant, but these women represented only 8 percent of the study population, reflecting the oversampling of low birth weight infants by many states.

Alcohol use just before pregnancy was common: 44 percent of women reported drinking in the 3 months before they became pregnant; of these, 94 percent were light drinkers (table 1). By the last 3 months of their pregnancy, less than 6 percent were still drinking alcohol; of these women, 98 percent were light drinkers. Binge drinking was less common. In the 3 months before pregnancy, 14 percent of all women, 31 percent of light drinkers, 78 percent of moderate drinkers, and 84 percent of heavy drinkers reported at least one binge. During the last 3 months of pregnancy, less than 1 percent of all women, 8 percent of light drinkers, 9 percent of moderate drinkers, and 18 percent of heavy drinkers binged. Forty percent of women who binged before pregnancy and 47 percent of women who binged in late pregnancy did so only once in the 3-month time period.

SGA births were more common among moderate drinkers or heavy drinkers in the 3 months before pregnancy than among nondrinkers or light drinkers (table 2). Moderate and heavy drinkers during the last 3 months of pregnancy were not more likely than nondrinkers during this time to deliver an SGA infant; however, only 46 women reported moderate or heavy drinking in late pregnancy, so the estimates were very imprecise. Overall, women who binged during either time period were not significantly more likely to deliver an SGA infant; women who binged in late pregnancy were 20 percent more likely to deliver an SGA infant, but the increase was not significant. The risk of SGA birth was higher among bingers than nonbingers at all levels of alcohol use for both time periods and increased with higher alcohol use, but the difference was significant only for heavy drinkers. The number of binges a woman reported was not related to the risk of SGA birth.


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TABLE 2. Association of levels of alcohol use and binge drinking with small-for-gestational-age birth, Pregnancy Risk Assessment Monitoring System, United States, 1996–1999
 
After adjusting for confounding variables, light and moderate drinkers in the 3 months before pregnancy were somewhat less likely than nondrinkers to deliver an SGA infant, although the difference was not significant. The risk among heavy drinkers was not different from that of nondrinkers (table 3). The results were similar when we limited the analysis to women who did not binge. Light and moderate drinking during late pregnancy was not related to SGA birth, but heavy drinking was associated with a fourfold risk. As mentioned before, there were few heavy drinkers in late pregnancy. The estimate was unstable, and the effect was halved when any tobacco use during the last 3 months of pregnancy was included in the model instead of the number of cigarettes smoked. When the analysis was limited to women who did not binge, the results for light drinkers were similar. The effect of moderate or heavy drinking could not be estimated.


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TABLE 3. Adjusted odds ratios* for the effect of level of alcohol use{dagger} on small-for-gestational-age birth, Pregnancy Risk Assessment Monitoring System, United States, 1996–1999
 
Compared with women who did not drink or who drank but did not binge, women who binged at least once before pregnancy were 15 percent less likely to deliver an SGA infant (table 4). This protective effect disappeared when we limited the reference group to women who drank alcohol but did not binge. The effect of bingeing before pregnancy differed by level of alcohol consumption. Light drinkers who binged had the same risk of SGA birth as those who did not binge, but moderate and heavy drinkers who binged were more than twice as likely to deliver an SGA infant as drinkers who did not binge (table 4). There were not enough women who drank heavily for us to analyze this group independently. Binge drinking during late pregnancy did not affect the risk of SGA birth overall or among light drinkers (table 4), and there were too few moderate or heavy drinkers in late pregnancy to fit the model. The number of binges before pregnancy or in late pregnancy was not related to SGA birth overall, for any level of drinking, or among women who had binged at least once. Moderate and heavy drinkers before pregnancy who were still drinking by late pregnancy were more likely to have delivered an SGA infant than those who had quit drinking, and the risk increased with heavier alcohol consumption in late pregnancy. The power of this analysis was limited, however, and the difference was not statistically significant (table 5).


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TABLE 4. Adjusted odds ratios* for the effect of binge drinking{dagger} on small-for-gestational-age birth, Pregnancy Risk Assessment Monitoring System, United States, 1996–1999
 

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TABLE 5. Adjusted odds ratios* for patterns of prepregnancy and late pregnancy alcohol use{dagger},{ddagger} on small-for-gestational-age birth among women who drank moderately or heavily before pregnancy, Pregnancy Risk Assessment Monitoring System, United States, 1996–1999
 

    DISCUSSION
 TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 ACKNOWLEDGMENTS
 REFERENCES
 
Only moderate and heavy drinking, combined with binge drinking in the 3 months before pregnancy and heavy drinking in late pregnancy, were significantly associated with an increased risk of SGA birth. Binge drinking overall was associated with a decreased risk of an SGA birth. Moderate or heavy drinkers prepregnancy who continued to drink in late pregnancy were more likely than those who did not to have delivered an SGA infant, and light drinkers were less likely than nondrinkers to deliver an SGA infant, but neither association was statistically significant.

Less than 5 percent of women reported drinking alcohol in the last 3 months of their pregnancy, and only 46 of them were moderate or heavy drinkers, so only strong effects of heavy alcohol use (odds ratios >=3.9) could be detected. Our results are consistent with studies finding that heavy alcohol use during the late pregnancy period increased the risk of SGA birth (3, 22), but our results were very sensitive to the coding of tobacco use in the analysis.

We know of only a few studies of binge drinking and pregnancy outcome among humans. A longitudinal study of patterns of alcohol consumption and its effects found that maternal binge drinking in the period before pregnancy recognition was the best predictor of infant neurobehavior deficits (18). Binge drinking has also been associated with developmental changes in infant electroencephalograms (23), longer infant hospital stays (17), and decreased infant head circumference (24), but a study of occasional binge drinking among moderate drinkers found no association with mean infant birth weight, length, head circumference, gestational age, intrauterine growth restriction, or Apgar scores (25).

The time periods for which we measured alcohol use differed from those in the other studies that have examined binge drinking, so comparisons are difficult in this respect. However, none of the studies that examined the effect of binge drinking just before or during pregnancy found a difference in the birth weights of infants of women who binged compared with women who drank but did not binge (25), nondrinkers (17, 24), or prepregnancy drinkers who abstained during pregnancy (26). Our results are consistent with those of Passero et al. (26), who found that women who binged and drank one to two drinks per day in early pregnancy delivered infants of lower birth weights than those born to women who drank the same amount but did not binge. Our finding that the number of binges was not related to SGA birth suggests that peak alcohol consumption may have a stronger effect on fetal growth than total alcohol consumption, which may also explain why binge drinking increased SGA birth among only moderate and heavy drinkers. These women may binge more heavily or have higher alcohol concentrations before they binge, so a binge is more likely to raise alcohol concentrations enough to affect fetal growth. Such a relation would be consistent with animal studies (8), but it needs more investigation in humans.

Our finding of a small protective association between low levels of alcohol use and SGA birth is not unusual; it has been demonstrated in several European (7, 26) and US populations (6, 22, 27). One review (28) found that, in a majority of the 55 studies reviewed, women who consumed less than one drink per day during pregnancy, compared with nondrinkers, delivered infants of higher birth weights.

Few attempts have been made to explain this effect, but the similar relation between low-level alcohol use and cardiovascular disease, and the evidence of a vascular etiology for SGA birth, suggests a shared pathway. One mechanism for the effect of moderate alcohol use on cardiovascular disease may be stimulated production of vascular endothelial growth factors, resulting in increased angiogenesis (29). Decreased levels of vascular endothelial and placental growth factors have been associated with fetal growth restriction (30). If alcohol drinking near conception and in early pregnancy increases production of these growth factors, it could lead to improved placental development and a lower risk of SGA birth. This mechanism may also explain why the protective effect occurs in early pregnancy only.

An alternative explanation for the protective association is dietary, nutritional, or behavioral differences between light drinkers and nondrinkers. A recent study of Frenchwomen found that women who drank more alcohol consumed more calories from meat, eggs, and cheese but ate fewer fruits, vegetables, and carbohydrates (31). The effect may also be due to misclassification or categorization of tobacco use. In our study, the protective effect was weakened when we controlled for number of cigarettes smoked per day instead of smoking status.

Our study had several limitations that might have affected our results. Alcohol use is difficult to measure. The amount of alcohol a women reports drinking may differ depending on how and when she is asked to report the information. da Costa et al. (32) found that fewer women reported alcohol use when asked about daily use than when asked about weekly use and that reported preconceptional alcohol use changed over the course of pregnancy. Our review of women’s volunteered comments indicated differing interpretations of the phrase "drank in an average week." Some women calculated the mean number of drinks per week over the entire 3 months, while others seemed to report the mode (the number of drinks they usually consumed in a week). The timing of alcohol consumption, relative to the time of conception, can be difficult to determine. Although we asked about alcohol use in the 3 months before pregnancy, the use reported probably included use in early pregnancy, before pregnancy recognition. Women asked about alcohol consumption before pregnancy often report alcohol use before pregnancy recognition instead (16).

In addition, women may underreport alcohol use during pregnancy if they believe that they should not be drinking. Very few women reported drinking moderately or heavily in late pregnancy, which limited our ability to find effects of late-pregnancy alcohol consumption. Data collection occurred after delivery, and over- or underreporting may have been higher among women whose infants were low birth weight or were born with other problems.

We did not have information on the types of alcoholic drinks consumed, which may be related to pregnancy outcome (6). We also did not have information on several potentially important confounding variables, including illegal drug use and nutrition. Prepregnancy weight status was missing for a large proportion of women, which may have introduced selection bias. Our results were not substantially different when this variable was removed from the model, however.

The persistently higher birth weights and lowered risk of SGA birth among infants of women who drank small amounts of alcohol just before pregnancy (or during early pregnancy) deserves more examination. Term SGA birth is not associated with the severe morbidity of preterm births (33), but it has been associated with neonatal morbidity (34), respiratory failure (35), and death. A well-designed prospective study examining the relations between nutrition, alcohol use, prepregnancy weight, pregnancy weight gain, and fetal growth would be valuable in determining what advice about diet and alcohol consumption is appropriate for women planning to become pregnant.


    ACKNOWLEDGMENTS
 TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 ACKNOWLEDGMENTS
 REFERENCES
 
The authors acknowledge the statistical assistance provided by Brian Morrow of the Division of Reproductive Health, Centers for Disease Control and Prevention. They also acknowledge the contribution of the participating PRAMS states, represented by the PRAMS Working Group: Alabama—Rhonda Stephens; Alaska—Kathy Perham-Hester; Arkansas—Gina Redford; Colorado—Dr. Alyson Shupe; Florida—Dr. Steven Wiersma; Georgia—Tonya Johnson; Hawaii—Limin Song; Illinois—Theresa Sandidge; Louisiana—Joan Wightkin; Maine—Martha Henson; Maryland—Dr. Diana Cheng; Michigan—Yasmina Bouraoui; Minnesota—Dr. Ron Campbell; Mississippi—Linda Pendleton; Montana—JoAnn Dotson; Nebraska—Dr. Debbi Barnes-Josiah; New Jersey—Dr. Lakota Kruse; New Mexico—Dr. Ssu Weng; New York—Anne Radigan-Garcia; New York City, New York—Dr. Fabienne Laraque; North Carolina—Dr. Paul Buescher; North Dakota—Sandra Anseth; Ohio—Adriana Pust; Oklahoma—Dick Lorenz; Oregon—Dr. Ken Rosenberg; Rhode Island—Sam Viner-Brown; South Carolina—Mary Kate Dillard; Texas—Dr. Ramdas Menon; Utah—Lois Bloebaum; Vermont—Peggy Brozicevic; Washington—Linda Lohdefinck; West Virginia—Melissa Baker; Centers for Disease Control and Prevention PRAMS Team, Applied Sciences Branch, Division of Reproductive Health.


    NOTES
 
Reprint requests to Dr. Nedra Whitehead, Division of Reproductive Health, National Center for Chronic Disease Prevention and Health Promotion, Centers for Disease Control and Prevention, 4770 Buford Highway, NE, MS-K-22, Atlanta, GA 30341 (e-mail: nsw1{at}cdc.gov). Back


    REFERENCES
 TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 ACKNOWLEDGMENTS
 REFERENCES
 

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