1 Department of Epidemiology, University of Washington School of Public Health and Community Medicine, Seattle, WA.
2 Center for Perinatal Studies, Swedish Medical Center, Seattle, WA.
3 Obstetrix Medical Group, Seattle, WA.
4 Fred Hutchinson Cancer Research Center, Seattle, WA.
Received for publication January 8, 2004; accepted for publication March 12, 2004.
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ABSTRACT |
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hyperlipidemia; hypertriglyceridemia; leisure activities; pregnancy
Abbreviations: Abbreviations: CI, confidence interval; HDL, high density lipoprotein; MET, metabolic equivalent.
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INTRODUCTION |
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Many effects of physical activity in pregnancy have been hypothesized as being beneficial to the mother, and a smaller number have been documented in observational studies (59). Two case-control studies demonstrated significant reductions in risk of gestational hypertension and preeclampsia among women who engaged in recreational physical activity during pregnancy (5, 6). One study detected trends in pre-eclampsia risk reduction across groups categorized by flights of stairs climbed daily and intensity of physical activity (6). A prospective study demonstrated a reduced risk of pre-eclampsia among women who reported physical activity during the year before pregnancy and suggested a similar relation with physical activity performed in early pregnancy (7). One registry-based study reported a reduced risk of gestational diabetes mellitus among obese women (8). Additionally, a reduced risk of gestational diabetes mellitus among women performing physical activity during early pregnancy was observed in a prospective cohort study (9).
Thus, although not conclusive, available cross-sectional and prospective data suggest that recreational physical activity may reduce the risk of preeclampsia and gestational diabetes. Physical activity may do so through a variety of biologic pathways. Potential intermediate effects of exercise that may reduce the risk of these disorders include reduced blood pressure, improved insulin sensitivity, decreased concentrations of proinflammatory cytokines and C-reactive protein in peripheral circulation, reduced oxidative stress, and improved plasma lipid and lipoprotein concentrations (1014).
To date, we know of no studies that have evaluated the relation between habitual physical activity and the blood lipid profile in pregnant women. Lipid metabolism is dramatically altered during pregnancy. Notably, maternal serum or plasma cholesterol and triglyceride concentrations increase 1.5- and threefold, respectively, above nonpregnancy levels by the mid-third trimester (15). This pregnancy-associated hyperlipidemia is further exaggerated in women with preeclampsia (1618) and gestational diabetes (1921). To date, however, little is known about the correlates and determinants of maternal plasma lipids and lipoproteins in pregnancy. Given that 1) maternal participation in recreational physical activity is associated with reduced risks of preeclampsia (57) and gestational diabetes (89); 2) dyslipidemia in early pregnancy, particularly hypertriglyceridemia, appears to be predictive of these disorders (1621); and 3) habitual physical activity has been shown to improve lipid profiles in men and nonpregnant women (14, 22), we sought to assess the extent to which maternal plasma lipids in early pregnancy are associated with measures of recreational physical activity.
The specific objectives of this cross-sectional study were to measure the relations between maternal plasma triglyceride, total cholesterol, and high density lipoprotein (HDL) cholesterol concentrations in early pregnancy and maternal self-reported participation in recreational physical activity during the same time period. Detailed assessment of physical activity during early pregnancy allowed us to determine whether the amount, energy expenditure, and peak intensity of physical activity were differentially associated with plasma lipid concentrations.
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MATERIALS AND METHODS |
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Enrolled subjects were asked to participate in an interview regarding sociodemographic and lifestyle characteristics and medical and reproductive histories. Nonfasting blood and urine specimens were collected, processed, and stored during early pregnancy. Detailed information about maternal habitual dietary intake during the periconceptional period and early pregnancy was ascertained by using a self-administered, 121-item semiquantitative food frequency questionnaire (23). Food composition values were obtained from the University of Minnesota Nutrition Coding Center nutrient database (24). Pregnancy outcome information was abstracted from labor, delivery, and medical records after the estimated delivery date. All women were enrolled in the study through only one pregnancy.
The procedures used in this study were in agreement with the protocols approved by the institutional review boards of the Swedish Medical Center and Tacoma General Hospital. All participants provided written informed consent.
Analytical population
The analytical population was derived from participants who enrolled in the Omega Study between 1996 and 2000. During this period, 1,219 eligible women were approached, and 1,000 (82 percent) agreed to participate. Fifty-two women with chronic hypertension and/or pregestational diabetes were excluded from the current analysis. Also excluded were 23 women for whom lipid concentration values were missing. Thus, 925 women remained for analysis.
Data collection and physical activity assessment
At the time of enrollment in the Omega Study (12.7 weeks gestation, on average), a 45- to 60-minute structured questionnaire was administered by a trained interviewer. Information on medical and reproductive histories and on sociodemographic and lifestyle characteristics was collected. After the interviewer read a script listing several examples of physical activities, women were asked, "What activities did you do during the last 7 days?" For each activity, women were asked to report the number of hours spent performing each activity on weekdays and weekend days, separately. Similar questions were asked to collect information on physical activity during the year before pregnancy. Questions were derived from the Stanford Seven-Day Physical Activity Recall and the Minnesota Leisure-Time Physical Activity Questionnaire, which have been validated among men and nonpregnant women (25, 26). Relevant sections of the questionnaire are available from the first author upon request.
Plasma lipid measurement and laboratory analytical procedures
Plasma lipid measurement procedures used for this study have been described elsewhere (27). Briefly, at or near the time of interview (13.2 weeks gestation, on average), a 20-ml nonfasting blood sample was collected. Blood was fractionated by using standard procedures and was stored at 80°C until analysis. Cholesterol and triglyceride concentrations were measured enzymatically by using assays standardized by the Lipid Standardization Program of the Centers for Disease Control and Prevention, Atlanta, Georgia. Analytical interassay coefficients of variation for cholesterol, tri-glyceride, and HDL cholesterol were 1.5 percent, 2.5 percent, and 3.0 percent, respectively.
Quantification of physical activity
We assessed the relation between plasma lipid concentrations and participation in recreational physical activity during a week in early pregnancy. Women were categorized into two groups: those who had performed any recreational activity during the assessment period (active) and those who had performed none (inactive). We also examined the relation between plasma lipid concentrations and the following measures of recreational activity: 1) amount of time engaged in physical activity in early pregnancy, 2) peak intensity of physical activity in early pregnancy, 3) energy expended during these activities, and 4) combined participation in physical activity before and during pregnancy.
To measure time engaged in physical activity in early pregnancy, the total numbers of hours spent performing each activity during the assessment period were summed and were expressed as hours/week. Inactive women were designated as the referent group. The remaining active women were divided into approximate tertiles according to hours spent engaged in recreational physical activity, resulting in four categories: none, <4.9 hours/week, 4.912.7 hours/week, and >12.7 hours/week.
Physical activity during the previous week was classified by intensity, and the score for the most intense exercise was used to measure peak intensity. Intensity of physical activity was quantified by using a standardized classification procedure that determines the energy costs of specific physical activities (28). Energy costs, expressed as metabolic equivalent (MET) scores, estimate energy expended on each activity. One MET is the ratio of work metabolic rate to a standard resting metabolic rate of 4.18 kJ x kg1 x hours1 (28). As the intensity of physical activity increases above that of the resting state, the energy expended in performing an activity (MET) increases. We defined light-intensity activities as those with MET scores of <3.0. Examples of light activities include croquet and horseback riding. Moderate-intensity activities (3.05.9 METs) include casual swimming and cycling. Vigorous activities (6.0 METs) include jogging and aerobic exercise. Using the MET scores, we classified physically active subjects according to the intensity of their most vigorous activity during the assessment period. We initially constructed four categories of peak intensity: no activity, light intensity, moderate intensity, and vigorous intensity. However, because only two women reported light peak intensity (<3.0 METs), we included them in the group reporting moderate peak intensity.
We measured the total amount of energy expended during recreational activity in the assessment period. Energy expenditure integrates the intensity with the amount of time spent performing each activity. Energy costs for each activity were calculated as described by Ainsworth et al. (28) and were expressed in METs. Energy expenditure, expressed as MET-hours/week, was calculated by summing the total number of hours spent on each activity in the assessment period, multiplying the result by the activity intensity score, and summing over all reported activities. Inactive women were designated as the referent group. The remaining active women were categorized into approximate tertiles of weekly energy expenditure, resulting in four categories: inactive, <20.4 MET-hours/week, 20.467.5 MET-hours/week, and >67.5 MET-hours/week.
The joint effect of exercise before and during pregnancy was also assessed. We categorized women into four groups based on their reported activity during a week in early pregnancy and the year before pregnancy, resulting in the following categories: inactive during both periods, active before pregnancy only, active during pregnancy only, and active during both periods.
Statistical analyses
We examined the distributions of maternal sociodemographic, reproductive, and medical characteristics. We then examined distributions of plasma triglyceride, total cholesterol, and HDL cholesterol concentrations and found them to be approximately normal. We therefore reported mean lipid concentrations across categorical levels of maternal characteristics. We examined linear relations between mean lipid concentrations and ordered categorical covariates by using tests of linear trend. All reported p values are two sided and were deemed significant at the = 0.05 level.
We calculated mean lipid concentrations across levels of physical activity measures. We then fit linear regression models to estimate the associations between physical activity measures and lipid concentrations. To assess confounding, we entered covariates into a model sequentially, comparing the unadjusted and adjusted regression coefficients for physical activity (29). Final models included covariates that altered unadjusted physical activity coefficients by 10 percent or more. The following covariates were considered as possible confounders: maternal age; race/ethnicity; marital status; years of education; parity (nulliparous vs. parous); use of prenatal vitamins; smoking before and during pregnancy; first-degree family history of diabetes; prepregnancy body mass index (weight (kg)/height (m)2); body mass index at the time of blood draw (hereafter referred to as early pregnancy body mass index); employment during pregnancy; annual household income; total dietary caloric intake during the periconceptional period (calories/day); percentage of calories from fat, carbohydrates, and protein; dietary fiber intake (g/day); dietary fruit and vegetable intake (servings/day); gestational age at blood draw; days between interview and blood draw; and, at blood draw, hours since eating.
Using logistic regression models, we examined the risks of elevated triglyceride (>150 mg/dl) or total cholesterol (>200 mg/dl) concentrations and reduced HDL cholesterol (<60 mg/dl) concentrations according to energy expended during physical activity. Cutpoints were determined a priori by using mean lipid concentrations in the study population. Odds ratios and 95 percent confidence intervals were calculated.
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RESULTS |
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Energy expended during early pregnancy was associated with decreased risks of both elevated triglyceride (>150 mg/dl) and elevated total cholesterol (>200 mg/dl) concentrations (table 5). Women reporting the highest energy expenditure were 55 percent less likely than inactive women to have elevated triglyceride concentrations (adjusted odds ratio = 0.45, 95 percent CI: 0.27, 0.76) and 45 percent less likely to have elevated total cholesterol concentrations (adjusted odds ratio = 0.55, 95 percent CI: 0.35, 0.88). Similar reductions in risk of elevated triglyceride and total cholesterol concentrations were detected across increasing levels of time performing physical activity and peak intensity (data not shown). There was no clear evidence of associations between physical activity variables and reduced HDL cholesterol concentration.
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DISCUSSION |
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To our knowledge, this is the first examination of the relation between lipid concentrations and habitual physical activity during pregnancy. Two studies demonstrated acute increases in maternal plasma triglyceride concentrations (approximately 4555 mg/dl) immediately after 2030 minutes of moderate exercise at 1533 weeks gestation (30, 31). Neither study design permitted determination of long-term changes in lipids associated with habitual exercise.
Potential limitations of the current analysis should be noted. Our measurements of physical activity were likely affected by misclassification due to recall error and variability in physical activity during the early weeks of pregnancy. Particularly, our method of estimating energy expenditure during the previous week has not been validated among pregnant women. One study demonstrated that 2-day energy expenditure was overestimated when using hourly physical activity records compared with heart-rate telemetry at 20 and 32 weeks gestation (32). While our estimates of physical activity may suffer from misclassification, the consistency of results across diverse measures (particularly the less complex measure of any vs. none) suggests that such potential misclassification cannot wholly explain the observed associations. The similarity in estimated coefficients of energy expenditure and time spent participating in physical activity suggests that intensity contributes little to the relation between early pregnancy physical activity and lipid concentrations. This similarity may be due to the observation that women tend to shift toward lower-intensity activities during pregnancy as compared with their prepregnancy habits (33).
Early pregnancy symptoms such as fatigue and nausea may have confounded the measured association between lipid concentrations and physical activity. In a cross-sectional study of 98 healthy pregnant women, those experiencing early pregnancy nausea and/or vomiting demonstrated significantly lower serum HDL cholesterol concentrations than nonemetic pregnant women did (34). Differences in serum total cholesterol or triglyceride concentrations were not detected. We did not assess early pregnancy nausea during the interview. However, we abstracted information on hyperemesis and nausea from medical records after pregnancy completion. Adjustment for indication of nausea and hyperemesis at or before gestational age at maternal interview did not change the observed associations between physical activity and lipid concentrations (data not shown). We were unable to assess fatigue during early pregnancy.
Variation in lipid measurements may have been introduced by aspects of the study design. Blood draws and interviews were not always conducted on the same day but were performed within a 4-day span, on average. Additionally, because subjects were pregnant, they were not asked to fast before blood draws. However, women, at the blood draw, were questioned regarding elapsed time since eating. Pairwise correlations between elapsed time since eating and each of the plasma lipids in this population were small, ranging from 0.01 to 0.04 (0.29 < p < 0.75). Adjustment for elapsed time since eating as well as time between interview and blood draw did not meaningfully change estimated coefficients. In addition, strong correlations between fasting and postprandial plasma lipids have been reported, ranging from 0.90 to 0.99 in at least one study (p < 0.001) (35).
Our study population was uncommonly active. Only 9 percent reported no recreational physical activity during the year before pregnancy, and 16 percent reported none during early pregnancy. These distributions are similar to those observed in the 2000 Behavioral Risk Factor Surveillance System Survey, in which 18 percent of Washington State women reported no participation in recreational physical activity during the previous month (36). However, in a 1998 national survey, 59 percent of US women aged 1844 years reported never engaging in physical activity lasting 10 minutes or more per week (37). Our study population also differed from pregnant US women in general with regard to characteristics such as race/ethnicity, obesity, and smoking during pregnancy. The associations observed here should be examined in more sedentary and demographically diverse populations.
Because of the cross-sectional study design, we are unable to infer that physical activity reduces triglyceride and total cholesterol concentrations during pregnancy. Future prospective studies of pregnant women are needed to more conclusively demonstrate this potential causal relation. Furthermore, we did not measure occupational physical activity in addition to recreational activity during pregnancy or in the previous year. Studies of occupational activity in pregnant populations are warranted to more fully characterize the relation between total physical activity and plasma lipids in early pregnancy.
Beneficial relations between physical activity and the plasma lipid profile in men and nonpregnant women have been demonstrated in numerous studies (14, 22). On the whole, data from cross-sectional studies suggest that physical activity does not seem to affect total cholesterol concentration. In a review of published literature, Durstine et al. (14) reported that most sedentary persons can experience elevations of 46 mg/dl in HDL cholesterol and decreases of 720 mg/dl in triglyceride concentrations by increasing energy expenditure to 1,5002,200 kcal/week. Similar changes in the lipid profile were observed during a randomized trial of exercise among sedentary, overweight men and nonpregnant women (22). Exertion of 1,5002,200 kcal/week equates to roughly 20 miles (32 km)/week of jogging or brisk walking or, for a person weighing 65 kg, about 2334 MET-hours/week. Our results are consistent with this estimated triglyceride reduction. However, we did not observe differences in HDL cholesterol according to physical activity. Physical activity may be unrelated to HDL cholesterol concentration during pregnancy; alternatively, our study may not have had enough statistical power to detect relatively small differences in HDL cholesterol across groups.
We have shown consistent, positive, and statistically significant relations between several measures of physical activity and plasma triglyceride and total cholesterol concentrations among healthy women during pregnancy. These results, when taken into consideration with other studies of men and nonpregnant women (14, 22), suggest that habitual physical activity performed during pregnancy may mitigate pregnancy-associated dyslipidemia. This study also provides impetus to more thoroughly examine the relations among physical activity, lipid concentrations, and disorders of pregnancy such as preeclampsia and gestational diabetes. Prospective studies are needed to replicate these results, as are studies designed to describe the potential differences in lipid-altering effects of aerobic exercise and strength training. Results from this and future studies will contribute to our understanding of the role that alterations in modifiable factors (such as the type, frequency, and duration of physical activity and energy expenditure) may play in influencing maternal lipid concentrations.
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ACKNOWLEDGMENTS |
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The authors are grateful for the technical expertise contributed by the Center for Perinatal Studies staff.
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NOTES |
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REFERENCES |
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