Markers of inflammation such as C-reactive protein (CRP) have been associated with increased risk for cardiovascular disease (7). CRP has been shown to be higher in pregnant women compared with their nonpregnant counterparts, even in uncomplicated pregnancies (20). Throughout pregnancy, there is no consistent change in CRP in uncomplicated pregnancies (41); however, CRP levels may increase through pregnancy in women who subsequently develop preeclampsia (37). Although thresholds for identifying elevated CRP during pregnancy have not been defined, several studies have reported that women with the highest levels of CRP had an increased risk of adverse pregnancy outcomes relative to women with the lowest levels of CRP (34,42). A meta-analysis of 18 studies by Rebelo et al. (35) found that CRP was higher in women who developed preeclampsia compared with women who had uncomplicated pregnancies (weighted mean difference between groups = 2.30 mg·L−1). In addition, a nested case–control study by Smirnakis et al. (36) found that second trimester CRP was higher in cases of gestational diabetes mellitus (GDM) (n = 36) compared with controls with uncomplicated pregnancies (n = 73) (10.6 vs 6.1 mg·L−1, P > 0.05). Therefore, it is important to identify modifiable factors associated with lower levels of CRP, particularly during the early stages of pregnancy, to be able to better promote optimal maternal health.
In nonpregnant populations, physical activity, assessed both objectively and via self-report, has been associated with lower levels of CRP (1,3,5) with studies finding that physically active individuals had 19%–35% lower levels of CRP than inactive individuals (32). Objectively measured sedentary behavior has also been shown to be independently associated with elevated CRP in nonpregnant populations (18). This is concerning because physical activity levels are relatively low in pregnant women compared with their nonpregnant counterparts (8,33). According to cross-sectional data from National Health and Nutrition Examination Survey (NHANES) from 1999 to 2006, less than 25% of pregnant women in the United States reported meeting recommendations for moderate and vigorous physical activity (9).
To our knowledge, no prior studies have assessed whether physical activity or sedentary behavior are associated with CRP in pregnant women. Thus, the purpose of this study was to determine the association between objectively measured physical activity and sedentary behavior with CRP levels in the first, second, and third trimester of pregnancy.
Population and Study Design
NHANES is a cross-sectional observational study of noninstitutionalized U.S. residents conducted by the National Center for Health Statistics of the Centers for Disease Control. The NHANES design and sampling methodology has been described elsewhere (29). In brief, NHANES uses a stratified, multistage probability design to obtain a nationally representative sample of the U.S. population. It oversamples participants who are non-Hispanic black, Mexican American, persons 60 yr and older, and individuals of low income so that nationally representative estimates of health can be generated. The NHANES protocol was approved by the National Center for Health Statistics institutional review board. All participants provide written informed consent at the time of the household interview.
Health interviews were conducted in participants’ homes by trained technicians. During household interviews, women were asked if they were currently pregnant and, if so, the current trimester; urine pregnancy tests were not used to confirm these pregnancies. Physical examinations (including CRP assessment) were conducted in a mobile examination center (MEC), at which time a subset of participants were provided an accelerometer to measure physical activity during the 2003–2004 and 2005–2006 study cycles. For the purposes of the current analysis, the study sample was limited to women in the 2003–2006 study cycles who self-reported currently being pregnant, were 16 yr or older (a lower age bound consistent with previous reports) (9,10), and who had available data on CRP, physical activity, and sedentary behavior.
Physical Activity and Sedentary Behavior Assessment
Physical activity was measured objectively with the ActiGraph AML-7164 accelerometer (27). The accelerometer measures the duration and intensity of physical activity by determining the magnitude of acceleration (intensity) and summing those magnitudes (counts) within a specified time interval (epoch). A 1-min epoch was used in this analysis. In the MEC, participants were provided with an accelerometer and asked to wear the monitor on the right hip for 7 d, removing it only for bathing or water activities. Nonwear time was defined as any block of time greater than or equal to 60 min of consecutive zero counts. For our primary analysis, individuals were included if they had at least four valid days of accelerometer data (>10 h of wear). As a sensitivity analysis, we repeated the analysis among individuals with at least 1 d of valid data.
There are no established accelerometer cut points for defining intensity of physical activity in pregnant women. Thus, we defined intensity using two commonly used cut points (11,25). Using Matthews’s cut points, light-intensity physical activity (LPA) and moderate-to-vigorous–intensity physical activity (MVPA) were defined as 100 to <760 and >760 counts per minute, respectively, (25). Using Freedson’s cut points, LPA and MVPA were defined as 100 to <1952 and >1952 counts, respectively (11). Sedentary behavior was defined as any minute with <100 counts, a commonly accepted cut point (39). In addition, sedentary behavior was presented as a proportion of monitor wear time (sedentary proportion = sedentary time minutes per day / wear time minutes per day). Total accelerometer counts were divided by the total wear time to calculate total counts per minute. Each minute of MVPA, LPA, and sedentary activity and total counts per minute were summed separately and divided by the number of valid days of wear time to obtain daily averages.
Subjective physical activity assessment
Physical activity was also assessed by self-report. The NHANES Physical Activity Questionnaire assesses leisure time physical activity (LTPA) by collecting detailed information about the frequency and duration of 47 specific activities of moderate or vigorous intensity (e.g., walking, running, swimming, yoga, and tennis). Frequency was multiplied by the duration in minutes and divided by 4.3 to obtain minutes of LTPA per week. To calculate MET-minutes per week, we multiplied each activity by its MET level as recommended by NHANES (31). Women were then categorized into three groups. The reference group was women who reported no LTPA. Among those who reported any LTPA, two groups were created above and below median levels of MET-minutes per week.
High-sensitivity CRP was measured in the MEC using latex-enhanced nephelometry (Dade Behring, Deerfield, IL) on a BN II nephelometer. Serum samples were collected in the MEC on all NHANES participants throughout the day with no special dietary requirements with respect to fasting. Stored samples were maintained at a temperature of −20° and shipped to the University of Washington Medical Center, Seattle, Washington, for testing as described elsewhere (30). Day-to-day coefficients of variation ranged from 4.93 to 7.84.
Information on age, race/ethnicity, education, and income were collected through self-report during the household examination. Self-reported trimester of pregnancy was categorized as first, second, and third. Race/ethnicity was self-reported as non-Hispanic white, non-Hispanic black, Mexican American, or other. Current smoking was defined as a serum cotinine level >3 mg·dL−1. Weight was measured using a digital scale in pounds and then converted to kilograms. Height was measured on a fixed stadiometer with a vertical backboard and moveable headboard. Body mass index (BMI) was calculated as measured weight in kilograms over height in meters squared (4). Normal weight, overweight, and obesity were defined as follows: <25 kg·m−2, 25 to <30 kg·m−2, and >30 kg·m−2, respectively. Annual household income was categorized as <$35,000, $35,000 to <$65,000, >$65,000, or unknown/missing. Education level was categorized as less than high school, high school diploma or GED, and greater than high school. Women were asked the number of pregnancies that resulted in a live birth (twin births were counted as one live birth). Parity was categorized as having 0, >1, or an unknown/missing number of live births. Because history of adverse pregnancy outcomes are related to risk of adverse outcomes in current pregnancy (19,40), we collected information on this variable. History of adverse pregnancy outcomes was determined by self-reported history of low birth weight babies (<5.5 g) or preterm births (<37 wk gestation) and categorized as 0, >1, or unknown/missing. Likewise, a family history of diabetes has been associated with an increased risk for GDM (2). To assess family history of diabetes, we asked the women if a blood relative (grandparent, parent, or sibling) had ever been diagnosed with diabetes.
The complex survey design used for NHANES data collection was incorporated into all data analysis using the “svy” command in STATA 12.0 (StataCorp LP, College Station, TX). Detailed information on the procedures to select the appropriate survey weight has been described elsewhere (29). We used the “wtmec2yr” survey weight for all analyses because we used data collected during the MEC visit. All analyses were considered significant at an alpha of 0.05. Descriptive statistics are presented as means or medians for continuous data and percentages for categorical data. Chi-square tests were used to evaluate association of pregnancy trimester with sociodemographic and health characteristics. ANOVA was used to assess differences in CRP, physical activity (objective and self-report), and sedentary time by trimester. Finally, multivariable linear regression was used to determine the relationship between physical activity (total counts per minute, LPA, MVPA, and LTPA) and sedentary behavior with high-sensitivity CRP by trimester. Each physical activity variable was analyzed in independent models. CRP was log transformed (log-CRP) to conform to the assumptions of the linear regression model. LPA and sedentary behavior were divided by 30 to show linear associations with CRP per 30-min increments. Because average time spent in MVPA is relatively low in this population, we show linear associations with CRP per 1-min increments. Model 1 examined the unadjusted association between physical activity and sedentary behavior with log-CRP. Model 2 examined this relationship adjusted for potential confounders. To assess confounding, we entered covariates into the model one at time, and beta coefficients of the adjusted and unadjusted models were compared. We considered factors as potential confounders if they resulted in a changed in the beta coefficients of >10%. We decided a prior included additional factors (e.g., history of pregnancy complications) based on previous studies that examined the association between CRP and pregnancy complications. Using these criteria, dietary factors such as fiber, folate, and total calories were not confounders in this data set and therefore were not included in multivariable models.
A total of 6367 women age >16 yr were in the NHANES 2003–2006 study cycles, of which 566 reported currently being pregnant. Among this sample, 496 (87.6%) were provided with an accelerometer and 304 (61.3%) had at least 4 d of valid accelerometer data. The final sample included 294 (51.9%) pregnant women with at least 4 d of accelerometer data who also had data on CRP. Most women were in their second trimester (42.9%, n = 126), with 17.3% (n = 51) in the first trimester and 39.8% (n = 117) in the third trimester (Table 1).
Women were similar across trimesters with respect to all descriptive characteristics except household income (Table 1). A greater proportion of women in their third trimester of pregnancy had an annual household income greater than or equal to $65,000 compared with women in their first or second trimester.
Objectively measured MVPA was higher among women in the first and second trimester compared with women in the third trimester using Freedson’s cut points (median = 11.5, 11.2, and 7.3 min·d−1, respectively; P < 0.01), but not Matthews’s cut points (Table 2). Total counts per minute, LPA, and sedentary behavior were similar across each trimester of pregnancy. Self-reported levels of LTPA followed a similar pattern to objectively measured MVPA, with higher levels among women in the second trimester of pregnancy; however, this difference failed to reach statistical significance (P = 0.24) (Table 2).
CRP levels were slightly higher among women in the second and third trimester of pregnancy compared with women in the first trimester, a pattern observed in previous studies (12); however, the difference failed to reach statistical significance (4.4, 5.8, and 5.5 mg·dL−1, respectively; P = 0.28) (Table 2).
The relationship between physical activity and sedentary behavior with log-CRP differed by trimester of pregnancy (Table 3). Physical activity (total counts per minute, MVPA, and LPA) or sedentary behavior was not significantly associated with log-CRP among women in the first trimester of pregnancy. However, among women in the second trimester, after adjusting for age, BMI, current smoking status, and history of adverse pregnancy outcomes, LPA but not total counts per minute or MVPA was inversely related to log-CRP (β = −0.0701, P = 0.05) using Freedson’s cut points. This translates to an approximately 0.4 mg·L−1 decrease in CRP with every 30-min increase in LPA. Using Matthews’s cut points, LPA also showed an inverse relationship which bordered on significance (β = −0.086, P = 0.06). In unadjusted analyses, sedentary behavior expressed as both mean sedentary time and proportion of total wear time among women in the second trimester was positively associated with log-CRP (β = 0.048, P = 0.02 and β = 2.36, P = 0.03, respectively). After adjusting for age, BMI, smoking status, and history of adverse pregnancy outcomes, these relationships were attenuated and no longer significant (β = 0.033, P = 0.20 and β = 1.96, P = 0.08, respectively). Physical activity (total counts per minute, MVPA, and LPA) and sedentary behavior were not significantly associated with log-CRP among women in the third trimester of pregnancy.
As a sensitivity analysis, we then repeated our analyses among individuals with at least 1 d of accelerometer data (Table 4). This sample included 393 women (79.2%) with a trimester distribution similar to the main analysis. Unlike the primary findings, we observed statistically significant associations between sedentary behavior and LPA with log-CRP during first trimester of pregnancy. In the fully adjusted models, the proportion of total wear time spent in sedentary behavior was positively associated with log-CRP (β = 1.39, P = 0.04). LPA was inversely associated with log-CRP when using the Matthews’s cut points (β = −0.084, P = 0.03), but not Freedson’s cut points. We also observed an inverse association between total counts per minute and log-CRP in this group (β = −0.001, P = 0.05). For women in the second trimester, both sedentary time and proportion of total wear time spent sedentary were positively associated with log-CRP (β = 0.03, P = 0.05 and β = 1.73, P = 0.03, respectively). MVPA was inversely associated with log-CRP when using Matthews’s cut points (β = −0.004, P = 0.02), but not Freedson’s (−0.015, P = 0.08). LPA was inversely associated with CRP when using Freedson’s cut points (β = −0.0522, P = 0.05). Total counts per minute was inversely associated with log-CRP (β = −0.003, P = 0.01). Neither physical activity nor sedentary behavior was associated with CRP during the third trimester of pregnancy.
Lastly, we examined the association between self-reported measures of physical activity and CRP by trimester of pregnancy (Table 5). In the first trimester of pregnancy, women who reported the highest levels of LTPA had a lower CRP than women who reported no LTPA (β = −0.58, P = 0.02). In the third trimester of pregnancy, women who reported the highest levels of LTPA had a lower CRP than women who reported no LTPA (β = −0.51, P = 0.03). In the second trimester of pregnancy, there were no differences in CRP levels across groups of LTPA.
In this population-based survey of NHANES pregnant participants, LPA was associated with lower levels of CRP among women in the second trimester of pregnancy. There was the suggestion that sedentary behavior was positively associated with higher CRP among women in the second trimester pregnancy, but this was not statistically significant. Neither physical activity nor sedentary behavior was associated with CRP among women in the first or third trimester of pregnancy when including participants with at least 4 d of accelerometer data. However, when using a less restrictive criterion for compliance (>1 d of accelerometer data), we found that sedentary behavior was positively, and total counts per minute and LPA were inversely, associated with CRP among women in the first trimester of pregnancy. In the second trimester of pregnancy, total counts per minute, LPA, and MVPA were inversely associated with CRP. We also observed that total sedentary time and the proportion of total wear time spent in sedentary behavior was positively associated with CRP in this group. Finally, self-reported LTPA was associated with lower CRP levels in women in their first and third trimester of pregnancy.
To our knowledge, the current study is the first to examine the relationship between physical activity and sedentary behavior with CRP in pregnant women. However, our findings are consistent with those of previous studies conducted in nonpregnant women. These studies have consistently found that physical activity is inversely, and sedentary behavior is positively, associated with CRP levels in nonpregnant populations (17,22,23). For example, Lynch et al. (24) examined the relationship between objectively measured physical activity and sedentary behavior with biomarkers of breast cancer in 1024 postmenopausal women from the NHANES 2003–2006 data set. The authors found that compared with women in the lowest quartile, women in the highest quartile of LPA (>6.48 vs <4.48 h·d−1) and MVPA (>18.21 min·d−1 vs 2.96 min·d−1) had 0.1 mg·dL−1 lower CRP levels. Likewise, individuals in the lowest quartile of sedentary time (<7.74 h·d−1) had 0.1 mg·dL−1 lower CRP levels than individuals in the highest quartile (>9.84 h·d−1).
Several additional analyses have been conducted examining the associations between objectively measured physical activity and sedentary behavior with CRP, also using data from NHANES. Healy et al. (18) evaluated the association between objectively measured sedentary time and breaks in sedentary time with cardio-biomarkers in 4757 male and female participants from the 2003–2006 cycles. Those who spent <7.24 h·d−1 in sedentary behavior had lower CRP levels than those who spent >9.57 h·d−1 in sedentary behavior (0.20 vs 0.16 mg·dL−1, P < 0.001). Hawkins et al. (16) examined the association between accelerometer determined intensity of physical activity and CRP in 3771 participants with and without diabetes from the 2003–2006 cycles. Among women without diabetes, a 1-min increase in LPA and MVPA was associated with a 0.0572 and 0.7128 decrease in log CRP, respectively. Loprinzi et al. (23) examined the association between accelerometer determined intensity of physical activity and the odds of having elevated levels of CRP (>0.3 mg·dL−1) among 746 men and women from the 2003–2006 NHANES cycles. A 1-min increase in LPA was associated with a lower odds of elevated CRP (OR = 0.99, 95% confidence interval = 0.98–1.00) in women 65 yr or older. Our results extend these findings to pregnant women, which may have important implications for maternal health.
We found that objectively measured physical activity or sedentary behavior was not statistically significantly related to CRP among women in the first trimester of pregnancy, although it followed a similar direction and effect as that observed among women in the second trimester. Similarly, MVPA was not associated with CRP, contrary to reports by others. The lack of statistically significant relationships between physical activity and CRP in women in the first trimester may have been due to the small sample of women (n = 51) in that trimester. Twenty-two women in their first trimester were excluded from the analysis because of noncompliance with accelerometers (<4 d of data). When we relaxed our criteria to include individuals with at least 1 d of accelerometer day, we observed statistically significant inverse associations between total counts per minute and LPA and CRP as well as a significant positive association between time spent in sedentary behavior and CRP among women in their first trimester of pregnancy. Likewise, using this more relaxed compliance criteria, MVPA was inversely associated with CRP among women in their second trimester. The compliance criteria chosen for this study was consistent with previous studies of physical activity and sedentary behavior in pregnant women (10). However, studies determining the number of days needed to estimate current physical activity levels with an accelerometer have been limited to nonpregnant populations (13,15,26,38). Patterns of physical activity differ between pregnant and nonpregnant women; therefore, we presented results using both a stricter and more relaxed compliance criteria.
In the third trimester of pregnancy, self-reported, but not objectively, measured physical activity was associated with CRP. The lack of association between objectively measured physical activity in the third trimester may be due to misclassification of activity with the accelerometer. The women in their third trimester of pregnancy may have performed activities involving upper limb movement that the movement monitor could not capture. Using self-reported physical activity data, we found that relatively higher levels of LTPA were associated with lower levels of CRP in the third trimester. Another limitation to this study is that the NHANES study sample did not have data on prepregnancy BMI or prepregnancy physical activity. However, early pregnancy BMI and physical activity have been found to be highly correlated with their prepregnancy levels (14) to the degree that these variables are independently associated with CRP, lack of control for these variables may have confounded our observed relationships.
In our primary analysis based on objective PA measures, we found that every 30-min increase in LPA was associated with a 0.0701 decrease in log-transformed CRP in women in the second trimester of pregnancy. This translates to a 0.4-mg·L−1 decrease in CRP with every 30-min increase in LPA, which may potentially represent a clinically significant effect. However, we did not have information on adverse pregnancy outcomes for the current pregnancy (e.g., preeclampsia, GDM, and preterm birth), which limits our ability to comment upon the clinical significance of our findings. In general, few studies have examined the linear association between CRP and pregnancy outcomes. One study, however, by Qiu et al. (34) examined the relationship between CRP in early pregnancy (~13 wk gestation) and incidence of GDM in 855 women participating in the OMEGA study. The authors found that every 1 mg·L−1 increase in CRP was associated with a 20% increased risk of developing GDM. In our study, we found that each 30-min increase in LPA was associated with a 0.4-mg·L−1 decrease in CRP among women in the second trimester of pregnancy. This means that after adjusting for age, BMI, smoking status, and history of adverse pregnancy outcomes, a women that accumulated 250 min of LPA (lowest quartile in this population) would have a 1.27-mg·L−1 higher CRP than a woman who accumulates 350 min of LPA (the highest quartile in this population). Potentially, this observed effect could potentially represent a significant reduction in the risk for GDM. We must, however, interpret these results with caution.
The mechanisms by which physical activity may impact CRP levels are poorly understood. Some reports suggest that the relationship between physical activity and CRP is mediated through adiposity and that weight loss is required to reduce CRP levels (21). However, as reported in our study, others have found this relationship to be independent of adiposity (1,16). Physical activity resulting in weight loss may reduce levels of adipokines, such as interleukin 6, resulting in lower levels of CRP (5,28). In pregnant populations, inflammation may be related to maternal adiposity and excessive gestational weight gain. A study by Frils et al. (12) examined the association between BMI and inflammation in 240 pregnant women of Scandinavian heritage. The authors found that maternal adiposity was associated with higher levels of several markers of inflammation including CRP. Physical activity may prevent excess gestational weight gain and maternal adiposity resulting in lower levels of CRP (6). In this current analysis, measures of prepregnancy BMI or gestational weight gain were not available and we were therefore not able to explore these as mediating factors.
In conclusion, in this population-based sample of pregnant women, we found that LPA during the second trimester of pregnancy was associated with lower CRP levels. These findings highlight the need for intervention studies designed to promote active lifestyles among pregnant women.
The authors declare no financial disclosures or conflicts of interest.
The results of this study do not constitute endorsement by the American College of Sports Medicine.
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