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RESEARCH AND PRACTICE |
At the time of this study, Edith C. Kieffer and Wendy J. Carman were with the Department of Health Behavior and Health Education, University of Michigan, Ann Arbor. Bahman P. Tabaei and William H. Herman were with the Departments of Internal Medicine and Epidemiology, University of Michigan, Ann Arbor. George H. Nolan was with the Department of Obstetrics and Gynecology, Henry Ford Health System, Detroit, Mich. J. Ricardo Guzman was with Community Health and Social Services, Inc, Detroit.
Correspondence: Requests for reprints should be sent to Edith C. Kieffer, University of Michigan School of Social Work, South University, Room 3770, Ann Arbor, MI 48109-1106 (e-mail: ekieffer{at}umich.edu).
| ABSTRACT |
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Objectives. We assessed the influence of maternal anthropometric and metabolic variables, including glucose tolerance, on infant birthweight.
Methods. In our prospective, population-based cohort study of 1041 Latino motherinfant pairs, we used standardized interviews, anthropometry, metabolic assays, and medical record reviews. We assessed relationships among maternal sociodemographic, prenatal care, anthropometric, and metabolic characteristics and birthweight with analysis of variance and bivariate and multivariate linear regression analyses.
Results. Forty-two percent of women in this study entered pregnancy overweight or obese; at least 36% exceeded weight-gain recommendations. Twenty-seven percent of the women had at least some degree of glucose abnormality, including 6.8% who had gestational diabetes. Maternal multiparity, height, weight, weight gain, and 1-hour screening glucose levels were significant independent predictors of infant birthweight after adjustment for gestational age.
Conclusion. Studies of birthweight should account for maternal glucose level. Given the increased risk of adverse maternal and infant outcomes associated with excessive maternal weight, weight gain, and glucose intolerance, and the high prevalence of these conditions and type 2 diabetes among Latinas, public health professionals have unique opportunities for prevention through prenatal and postpartum interventions.
| INTRODUCTION |
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This focus has diverted research and program attention from other aspects of maternal and child health in this population. Obesity, impaired glucose tolerance, and type 2 diabetes are common among Latino women of childbearing age.15,16 Intrauterine metabolic abnormalities associated with these conditions are linked to increased risk for fetal overgrowth, developmental anomalies, birth injuries, and subsequent obesity and type 2 diabetes in childhood, youth, and later life.1722 Increased birthweight secondary to intrauterine overnutrition may be a marker of poor maternal and infant health in populations with a high prevalence of maternal obesity and diabetes. Our study assessed the combined influence of maternal weight and other anthropometric and metabolic characteristics on the birthweights of Latino infants.
| METHODS |
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All 1346 Latino women who entered prenatal care at CHASS between January 5, 1999, and February 28, 2001, were recruited to participate in this study. Nine women with twin pregnancies, 6 women who entered care in the final weeks of pregnancy, and 39 women who had participated during their previous pregnancy were excluded, which left 1292 eligible women. No consent was obtained for 104 women (8.0%) including 49 who refused, 39 who were younger than 18 years and could not obtain parent/guardian consent, 13 who changed provider, and 3 who miscarried before consent could be obtained. On average, these women were younger, thinner, and entered care later than did consenting women. Of the 1188 consenting women, 147 (12.4%) were subsequently excluded from analyses, including 10 who miscarried, 6 who had a stillbirth, 1 whose records were missing, and 130 who were lost to follow-up. They entered prenatal care a week earlier but were otherwise similar to the 1041 women who, with their infants, constituted the study population.
Data Collection
Standardized interviews, anthropometry, and medical record reviews were conducted by trained study staff. Blood was drawn by CHASS laboratory personnel and processed by the University of Michigans Michigan Diabetes Research and Training Center laboratories according to standard protocols. Maternal and family health history, obstetric history, last menstrual period, and medical complications since the last menstrual period were obtained at the first prenatal visit and abstracted from the medical record. Acculturation variables (birthplace inside or outside the United States, duration of US residence, primary language of Spanish or English, urban vs rural childhood environment) were obtained by interview with study staff at the first prenatal visit. Hispanic Health and Nutrition Survey questions about smoking before and during pregnancy were used to assess smoking behavior.23 An index of prenatal care adequacy, which was coded as adequate (yes/no), included the trimester prenatal care began and the number of prenatal care visits given the gestational age of the infant at birth.24
Maternal prepregnancy weight was assessed with a questionnaire. When prepregnancy weight was unknown or missing, and a weight was obtained within the first 10 weeks of pregnancy, predicted prepregnancy weight was estimated using procedures described by Siega-Riz.8 Height was measured with a stadiometer and weight was measured with a beam balance scale at the first prenatal visit. Blood pressure, measured with a sphygmomanometer, and weight measurements were obtained at each prenatal visit. Prepregnancy body mass index (BMI) (weight [kg]/height [m]2) was calculated and coded into 4 Institute of Medicinerecommended categories: underweight (<19.8), normal weight (19.826.0), overweight (>26.029.0), and obese (>29.0).25 Weight gain was calculated by subtracting prepregnancy weight from the last weight recorded during prenatal care if the last visit occurred within 7 days of delivery. Women without a reported or predicted prepregnancy weight nor a last weight recorded within 7 days of delivery, were excluded from analyses of pregnancy weight gain.
Anthropometry was performed at the first prenatal visit and no later than 25 weeks of gestation to reduce the influence of fetal growth on the measurement of waist circumference. Anthropometry was adjusted for duration of gestation at the measurement visit during data analysis. Circumferences were measured to the nearest 0.5 cm with a flexible tape. Waist circumference, a measure of body fat distribution, was calculated by measuring at the narrowest horizontal circumference in the area between the ribs and iliac crest. Hip circumference was measured at the level of maximal extension of the buttocks. Arm circumference was measured at the midpoint of the upper arm. Triceps skinfold thickness was measured to the nearest millimeter using a Lange skinfold caliper at the triceps at the same level where the arm circumference was obtained.
Women with random glucose levels 126 mg/dL or higher at the first prenatal visit received immediate diabetes screening or diagnostic testing. All women without a diagnosis of diabetes received a 1-hour, 50-g oral glucose screening test at approximately 26 weeks gestation. Assays for insulin and lipids were performed on blood samples drawn 1 hour after a drink containing 50 g of glucose was consumed. There are no reference standards for insulin or lipid levels during pregnancy. Women with glucose screening test results 130 mg/dL or higher received a 3-hour, 100-g oral glucose tolerance test. Gestational diabetes mellitus (GDM) was diagnosed with American Diabetes Association criteria, i.e., 2 or more glucose values 95 mg/dL or higher at fasting, 180 mg/dL or higher at 1 hour, 155 mg/dL or higher at 2 hours, and 140 mg/dL or higher at 3 hours.26 Women with 1 abnormal oral glucose tolerance test value were referred to the CHASS dietitian who provided nutrition counseling similar to that provided to women with GDM. Women with GDM were referred to the Henry Ford Hospital Endocrinology Department for diabetes management.
Gestational age was established by a single perinatologist who was blinded to the glucose and birth outcome status of the motherinfant pair. An initial ultrasound assessment was obtained immediately after the first prenatal visit. The last menstrual period date was used when the difference between that date and that estimated from ultrasound measurements was less than 8 days. In all other cases, the ultrasound data were used. Birthweight was measured in grams within an hour of birth on a Detecto recumbent scale (Cardinal Scale Manufacturing Co, Webb City, Mo). Birthweight was adjusted for gestational age with analysis of covariance and by including gestational age as a covariate in the linear regression models.
Statistical Analysis
All statistical analysis and test procedures were performed with SAS software version 6.12 (SAS Institute, Cary, NC). Descriptive statistics were obtained with mean and standard deviation for continuous variables and frequencies and proportions for categorical variables. Maternal sociodemographic, anthropometric, and metabolic characteristics by 1-hour glucose category (< 100 mg/dL, 100129 mg/dL,
130 mg/dL) and gestational diabetes status were assessed with 1-way analysis of variance using general linear models and the CochranMantelHaenszel
2 test. Differences within groups were assessed with the Tukey pairwise comparison procedure. Analysis of covariance was used to compare means between groups after adjustment for covariates. Bivariate and multivariate linear regression analyses were performed to assess the relationships among sociodemographic, biological, anthropometric, and metabolic characteristics as independent variables and birthweight as the dependent outcome variable after adjustment for gestational age.
The normality and linearity assumptions of linear regression models were assessed by univariate analyses and by categorizing each continuous variable into multiple dichotomous variables. Interaction terms between independent variables were also considered. None of the interaction effects was statistically significant. The coefficient of determination (R2) and adjusted R2 (for the multiple linear regression model) were used as a quantitative measure of how well the independent variables explained the outcome. Pearson correlation analyses and partial correlation analyses were performed to assess the strength of the relation between the outcome variable (birthweight) and the independent variables after adjustment for gestational age. Multicolinearity among anthropometric variables made it difficult to determine their independent effects if included in the multivariate linear regression model together. Therefore, to select the best possible multivariate model, a forward stepwise selection procedure was performed with maternal sociodemographic, health, prenatal care, and metabolic variables, and the anthropometric variables were forced into the stepwise model separately. A P value <.05 was defined as the level of statistical significance.
| RESULTS |
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On average, the women weighed 139 pounds before pregnancy and were 5 feet, 2 inches tall. The average prepregnancy BMI was 25.9 kg/m2. Only 7% of women were classified as underweight, whereas 42% were either overweight or obese before they became pregnant. The mean weight gain during pregnancy was 12.9 kg (28.4 pounds). Thirty-six percent of the women gained more than the recommended amount of weight during pregnancy, including more than half of overweight women and 38% of obese women. At the first prenatal visit, the mean waist, hip, and upper-arm circumferences were 90.7 cm, 102.8 cm, and 28.2 cm, respectively. The mean triceps skin-fold measurement was 27.2 mm.
The mean glucose level derived from the 1-hour, 50-g glucose screen test was 116 mg/dL; and 27% of the women had abnormal glucose values of greater than 130 mg/dL. The mean 1-hour insulin level was 96 µU/mL, and the mean insulinglucose ratio, a measure of insulin resistance, was 0.81. The mean 1-hour total cholesterol level was 223 mg/dL, the mean 1-hour high-density lipoprotein level was 64 mg/dL, and the mean 1-hour triglyceride level was 214 mg/dL. Women with 1-hour glucose levels of 130 mg/dL or higher were referred for 3-hour, 100-g oral glucose tolerance tests. Sixty-eight women (27% of women tested and 6.8% of the study population) had GDM.
The mean birthweight of infants born to study participants was 3408 g. Ninety-one infants (8.7%) weighed 4000 g or more. Among infants born to women with GDM, 13.2% weighed 4000 g or more compared with 8.8% among women without GDM. Only 3.6% of infants weighed less than 2500 g. The average gestational age of study infants was 39.3 weeks. Only 7.7% of infants were preterm (gestational age < 37 completed weeks). Preterm birth was much more frequent (19.1%) among infants of mothers with GDM than among infants of mothers without GDM (5.9%) (data not shown).
Maternal Glucose Category, Maternal Characteristics, and Infant Outcomes
Mean maternal age and the percentage of women with a family history of diabetes were significantly higher with each successive maternal glucose category at 26 weeks gestation, and were greatest in women with GDM (Table 2
). Maternal multiparity was not associated with significant differences in glucose category. There were no significant relations between maternal glucose category and parity, marital status, maternal education in years, any acculturation variable, prenatal care adequacy, smoking, or history of gestational hypertension (data not shown).
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There was a significant linear trend among maternal glucose category, gestational age, and mean birthweight. Among women without GDM, mean gestational age was slightly but significantly higher with successively higher glucose category. Women with GDM had shorter gestations than did women without GDM in all glucose-level categories. Birthweights that were unadjusted for gestational length followed a similar trend, with successively greater birthweights at each increase in glucose-level category for women without GDM. Infants born to mothers with GDM had lower unadjusted birth-weights than all mothers except those with glucose levels less than 100 mg/dL. After adjustment for gestational age, the significant linear increase in birthweight among infants of women without GDM persisted and continued among infants of GDM mothers, whose adjusted birthweights were the greatest. The significant linear increase in birth-weight with increasing glucose level was maintained after further adjustment for maternal age, parity, BMI, weight gain, hypertensive disorders, and family history of diabetes.
Maternal Characteristics and Birthweight, Adjusted for Gestational Age
In bivariate regression analyses, birth-weight was associated with multiparity and higher values of maternal age, as well as 7 anthropometric variables: BMI, weight gain, height, waist and hip circumference, triceps skinfold, upper-arm circumference, and upper-arm fat area after adjustment for gestational age (Table 3
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In the final multivariate model, significant independent predictors of birthweight were multiparity, BMI, height, weight gain, and 1-hour glucose value after adjustment for gestational age. Hip circumference was marginally significant. The maternal glucose value accounted for 16 g of increased birth-weight for each 10-mg/dL increase in glucose value, after adjusting for the other variables in the model (Table 4
).
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| DISCUSSION |
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More than a quarter of the study population had some degree of glucose intolerance, including 27% with an abnormal (
130 mg/dL) 1-hour screening glucose value. Similar to our previous study, we found that among women without GDM, the highest birthweights occurred among infants of mothers whose screening glucose values were 130 mg/dL or higher.22 Among women without GDM in our study, each 10-mg/dL increase in 1-hour glucose level was associated with a 16-g increase in birthweight, after adjusting for gestational age, parity, maternal BMI, height, pregnancy weight gain, and hip circumference. These variables attenuated but did not fully explain the effect of maternal glucose on birthweight. All women with an abnormal glucose screen were referred for further testing.16,22
Gestational diabetes was diagnosed in 6.8% of the women, which is higher than that found in a recent study of non-Hispanic White and African American women that used the same diagnostic criteria.30 The percentage of women with 1 abnormal oral glucose tolerance test value was 3.3%. This condition, which has been defined as impaired glucose tolerance, has been associated with increased birthweight and macro-somia in African American women.30 The number of women with impaired glucose tolerance in our study was too small to assess this relation. Women with GDM or impaired glucose tolerance received dietary and weight management counseling according to clinic protocol. This practice may have reduced the impact of higher glucose levels on birthweight compared with those previously reported.22,31
We found no statistically significant independent associations between several other metabolic fuels and birthweight. A previous study found that the 1-hour triglyceride value was a significant predictor of birth-weight among women with or at high risk for GDM but not among women with normal glucose status.27 Another found a significant association between 1-hour triglyceride value and birthweight independent of BMI and weight gain, but glucose status was not included in their model.32 In our study, when the glucose category was included, this relationship was attenuated and was not significant in our multivariate model.
Factors commonly used in perinatal research, policy, and practice, such as maternal age, education, marital status, and adequacy of prenatal care, showed no association with birthweight in our multivariate model after adjustment for gestational age.1,2,21 We also found no association between any measure of acculturation and birthweight. Because more than 90% of our study participants were born in Mexico, and because their duration of US residence was short, there may have been insufficient variation in birthplace and acculturation levels to find significant associations. Others have found that low levels of acculturation and increased length of time in the United States were associated with higher infant birthweights.13 Mexican-born women had significantly lower risks than did US-born Mexican women and non-Latino White women, whose risks of low birthweight were similar.14
Several limitations apply to this study. Our results may not apply to all US Latino women because a greater percentage of women in this study were Mexican and recent immigrants, and their levels of education and prenatal care were lower than US Latino women overall.2 Nonetheless, our participants were representative of pregnant women in a growing number of communities throughout this country. Lack of first-trimester anthropometry, and more sensitive measures of metabolic status such as the fasting and 2-hour postglucose values of glucose, insulin, and lipids from the oral glucose tolerance test were not suitable for most women. This may have reduced our ability to detect the full influence of maternal anthropometric and metabolic characteristics on birthweight.
Overweight, obesity, abnormal glucose tolerance, and GDM were prevalent among Latino women in this study. Their infants birthweights were influenced by these conditions and by maternal weight gain. These results suggest that research related to birth outcomes, including assessments of ethnic disparities in fetal growth, should include measures of glucose tolerance during pregnancy, maternal weight, and weight gain in addition to more commonly used sociodemographic, prenatal care, and behavioral variables. This work should not be limited to mothers with diabetes, but should include the whole range of glucose tolerance. Longitudinal studies that include anthropometry and metabolic measures from early until late in pregnancy are also needed to better assess the influence of the intrauterine metabolic environment on subsequent maternal, infant, and child health among Latino children, given their increased risk of early onset type 2 diabetes.33
Almost half of the women in this study entered pregnancy overweight or obese. More than a third of the women exceeded the Institute of Medicine weight gain recommendations, particularly if they were already overweight or obese. These percentages are similar to those for Latinas nationally.34 However, these estimates are conservative. Calculating BMI using current standards for nonpregnant adults would increase the prevalence of both excessive prepregnancy weight and pregnancy-associated weight gain. Excessive maternal weight, weight gain, and glucose intolerance are each associated with adverse maternal and newborn outcomes and with increased risk for GDM and subsequent type 2 diabetes in both mothers and infants.1721,33,3537
Dietary modifications and increased physical activity during pregnancy may reduce excessive weight gain, improve maternal glucose status and decrease associated maternal and infant complications.26,3841 Similar lifestyle modifications and breastfeeding, along with postpartum glucose testing and diabetes education, may also reduce morbidity associated with undetected or untreated impaired glucose tolerance and type 2 diabetes.20,26,39 Because most women have repeated contact with either public health or private health care systems during pregnancy and immediately after, public health professionals and prenatal care providers have unique opportunities to promote healthy outcomes among mothers and infants at risk for obesity and type 2 diabetes.
| Acknowledgments |
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The authors thank Cathy Zavala Sanborn, Marilyn Lugo, and the staff and patients of Community Health and Social Services Center in Detroit.
Human Participant Protection
This study was approved by the University of Michigans institutional review board.
| Footnotes |
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Contributors
E. C. Kieffer led the study design and implementation and the writing of the article. B. P. Tabaei and W. J. Carman contributed to the analysis plan and conducted the statistical analysis. B. Tabaei also contributed to writing the article. G. H. Nolan and J. R. Guzman assisted with study design and interpretation. W. H. Herman contributed to study design and implementation and to writing the article. All authors helped to conceptualize ideas, interpret findings, and review drafts of the manuscript.
Accepted for publication December 20, 2005.
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