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EPIDEMIOLOGY

Physical Activity Domains/Recommendations and Leukocyte Telomere Length in U.S. Adults

OGAWA, ELISA F.1; LEVEILLE, SUZANNE G.2,3,4; WRIGHT, JULIE A.1; SHI, LING2; CAMHI, SARAH M.1; YOU, TONGJIAN1

Author Information
Medicine & Science in Sports & Exercise: July 2017 - Volume 49 - Issue 7 - p 1375-1382
doi: 10.1249/MSS.0000000000001253
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Abstract

Telomeres are located at the ends of chromosomes, where they protect DNA and its integrity during cell division (2). Telomere shortening is a characteristic of human aging and may serve as a biomarker for early mortality (17). However, there is great variability in telomere length among individuals, most likely due to genetic, environmental, and lifestyle factors that interact throughout the life span (21). Although cellular telomere length can be measured in different tissues/cells, leukocyte is frequently used biomarker for telomere studies (12,15).

Although some studies have found that physical activity (PA) may have a protective effect against telomere shortening (12,15,22,24,32), other studies have reported that PA has no effect on telomere length (17,26,27,31). Furthermore, one study has shown that intensively trained athletes have longer telomeres than their inactive peers (29), whereas several studies support an inverted U-shape relationship between telomere length and PA intensity (13,19,36) as vigorous PA or high-intensity exercise may lead to increased oxidative stress (14).

These mixed findings on PA and telomere length could be due to various sample sizes or other covariates unaccounted for (e.g., cigarette smoking and alcohol consumption) that might affect telomere length, considering only a few studies to date have examined the association between PA and telomere length using large population samples using the National Health and Nutrition Examination Survey (NHANES) data set (24,25,31). PA measures and their associations observed with telomere length in previous studies are summarized in Table 1. To our knowledge, current literature has mainly examined the association between telomere length and leisure time PA (LTPA) (12,15,17), total PA (31,35,37), or muscle and cardiovascular exercise/fitness (20,23,24,38) and has not examined the relative influence of different PA domains such as household/yard work PA, transportation PA, moderate LTPA, or vigorous LTPA. Many studies compared telomere length and cardiovascular fitness/exercise measures among older and young athletes and nonathletes, once again focusing on specific type of PA (19,22,27,32,36). PA is defined as any bodily movement that requires energy while exercise is part of PA that is planned and structured (30). Different PA domains such as physical exercise could have different associations with telomere length contributing to the seemingly conflicting findings to data. Moreover, many studies that examined the relationship between PA and telomere length used binary PA outcomes (engaged in moderate or vigorous LTPA or not engaged in moderate or vigorous LTPA) or grouping participants into PA categories (inactive, light activity, moderate activity, and heavy activity) rather than overall duration of PA, which could also affect the findings. In addition, to our knowledge, only one study has examined the association between meeting the PA recommendation (PA ≥150 min·wk−1) and telomere length (25).

TABLE 1
TABLE 1:
Studies examining relationship between PA outcomes and telomere length.

A better understanding of these ongoing questions on the relationship between telomere length and PA will not only provide better information for the public and the scientific community but will also help clarify the overall association of PA on telomere length. Therefore, in this study, we examine the association between PA and telomere length in a nationally representative sample, with specific attention to PA domains and PA recommendations.

METHODS

Study population

The National Center for Health Statistics of the Centers for Disease Control and Prevention (CDC) has been conducting the NHANES since 1960, providing a nationally representative sample of the health and nutritional status of noninstitutionalized U.S. civilians. For these analyses, cross-sectional survey data from the 1999–2000 and the 2001–2002 cycles of NHANES were used. The data from the NHANES 1999–2002 are available for public use from the CDC's website (6). Participants in the NHANES were 21,004 individuals 2 months and older. NHANES 1999–2002 used a four-stage sampling design: 1) primary sampling units (PSU) consisting primarily of single counties, 2) area segments within PSU, 3) households within segment areas, and 4) persons within households (10).

For the NHANES 1999–2002 surveys, subjects 20 yr and older were asked to provide DNA samples, of whom 7827 (76%) subjects provided samples. We excluded 335 subjects who had missing PA information because the aim of this study was to examine the association between PA domains and leukocyte telomere length (LTL). An additional 559 subjects were excluded from the analytic sample because of missing data on key covariates, including education (n = 10), cigarette smoking (n = 9), body mass index (BMI) (n = 183), and alcohol consumption (n = 357). For the two NHANES surveys, a total of 6933 adult (20–85 yr) subjects (67%) provided complete data for the study variables. The Institutional Review Board at the University of Massachusetts Boston approved this data analysis study.

LTL

The detailed methodology of LTL assay has been reported previously (5,31). Briefly, leukocyte DNA was extracted from whole blood, and the LTL assay was performed using quantitative polymerase chain reaction method to measure telomere length (T) relative to standard (S) reference DNA (T/S ratio). Each sample was assayed three times on three different days. Runs with more than four control DNA values falling outside 2.5 standard deviations from the mean for all assay runs were excluded from further analysis (<6%). In addition, any potential outliers were excluded from the calculations (<2%). CDC conducted a quality control review before linking the LTL data to the NHANES public-use data files (9).

PA

PA variables used in these analyses were either moderate or vigorous intensity: household/yard work PA, transportation PA, moderate LTPA, vigorous LTPA, total moderate PA, and PA recommendation groups. Subjects' general PA during the past 30 d was collected during the household interview portion of the data collection through retrospective recall questions. For household/yard work PA, participants were asked “Did you do any tasks in or around your home or yard for at least 10 min that required moderate or greater physical effort? By moderate physical effort I mean, tasks that cause light sweating or a slight to moderate increase in your heart rate or breathing, such as ranking leaves, mowing the lawn or heavy cleaning.” For transportation PA, participants were asked “Have you walked or bicycled as part of getting to and from work, or school, or to do errands?” For moderate LTPA, participants were asked “Did you do moderate activates for at least 10 min that cause only light sweating or slight to moderate increase in breathing or heart rate? Some examples are brisk walking, bicycling for pleasure, golf, and dancing.” For vigorous LTPA, participants were asked “Did you do any vigorous activities for at least 10 min that cause heavy sweating, or large increase in breathing or heart rate? Some examples are running, lap swimming, aerobic classes, or fast bicycling.” Participants who answered “yes” to any of the PA domain in bouts of at least 10 min during the past 30 d were further questioned on the level of exertion, frequency, and duration of each PA domain. Activities for which the reported duration was less than 10 min were counted as 0 in the PA variables (8). The concurrent validity of these questions has been assessed using accelerometer data (r = 0.27) (39).

Total moderate PA score was computed using the four PA domains (household/yard work PA, transportation PA, moderate LTPA, and vigorous LTPA). Both the U.S. Department of Health and Human Services (40) and NHANES (7) have recommended that 1 min of vigorous activity counts as 2 min of moderate activity. Therefore, 1 min of vigorous-LTPA was multiplied by two to account for its intensity. Furthermore, we categorized three PA recommendation groups using the cut points from the U.S. Department of Health and Human Services' Physical Activity Guidelines for Americans recommendation (40). The recommendation states that for substantial health benefits, adults should do at least 150 min·wk−1 of moderate-intensity or 75 min·wk−1 of vigorous-intensity aerobic PA or an equivalent combination of moderate- and vigorous-intensity aerobic activity (34). In addition, the recommendation states that for additional extensive health benefits, adults should increase their aerobic PA to 300 min·wk−1 of moderate intensity or 150 min·wk−1 of vigorous-intensity aerobic PA or an equivalent combination of moderate- and vigorous-intensity activity (34). From these guidelines, we created three PA recommendation groups: not meeting the recommendation (total moderate PA < 150 min·wk−1 of PA), meeting the recommendation (total moderate PA ≥ 150 min·wk−1 and <300 min·wk−1), and exceeding the recommendation (total moderate PA ≥300 min·wk−1). Hence, we converted vigorous-intensity activity to moderate intensity by multiplying participation time by two.

Sociodemographic and health measures

Covariates included in the models were chosen based on previous literature (31). Covariates included age, gender, race/ethnicity (Hispanic, non-Hispanic White, non-Hispanic Black, or other), education (less than high school, high school grad or General Education Development, or attended college or college grad), income (<$10,000, $10,000–$19,999, $20,000–$34,999, $35,000–$54,999, $55,000–$74,999, >$75,000, or missing), self-reported smoking status (never, former, or current), self-reported alcohol consumption (abstainers, light/moderate drinkers, or heavy drinkers), BMI, calculated from measured height and weight, and cardiovascular fitness (estimated maximal oxygen uptake [V˙O2max]). The submaximal (75% HRmax) treadmill exercise test was done to estimate participants' V˙O2max (11). We determined alcohol consumption categories by the reported number of drinks per week: abstainers (no alcohol consumption in the past 12 months), light/moderate drinkers (women who reported having drunk more than zero drinks but less than two drinks per day on average in the past 12 months and men who reported more than zero drinks but less than three drinks per day on average in the past 12 months), and heavy drinkers (women who reported having two or more alcoholic beverages per day in the past 12 months and men having three or more alcoholic beverages per day in the past 12 months) (31).

Statistical analyses

All descriptive statistics and regression models accommodate the complex sampling design of NHANES by incorporating strata and PSU, which is the sampling unit that is selected in the first of the multistage samples, as indicators, as well as sample weight (6). The LTL data were not normally distributed and were transformed by natural logarithm before regression modeling. We report the exponentiated regression coefficients, which is the ratio of the geometric mean for one unit increase in the independent variable; therefore, we report the percentage change in the average value of telomere length (T/S ratio) for one unit increase in the independent variable while holding all other predictors constant.

PA variables for which the reported durations were more than three standard deviations away from the mean were recoded to the same value as three standard deviations away from the mean to reduce the outlier effect. To examine the percent change in LTL with an increase in 1 h·wk−1 of PA variables, we divided minutes of participation in PA by 60 (household/yard work PA, transportation PA, moderate LTPA, vigorous LTPA, and total moderate PA).

We used linear regression models to explore the association of LTL on PA and adjusted for covariates that have been shown to affect LTL (age, gender, race or ethnicity, education, cigarette smoking, alcohol consumption, and body composition). Using multivariable linear regression modeling, we adjusted for demographic variables such as age, gender, race, education, and income (model 1) then further adjusted for additional health behaviors that have been shown to have influence LTL, including BMI, cigarette smoking, and alcohol consumption (model 2). Four PA domains (household/yard work PA, transportation PA, moderate LTPA, and vigorous LTPA), total moderate PA, and PA recommendation groups were included separately in our models to avoid multicollinearity.

Additional analyses to further clarify the relationship between PA and LTL were performed. Tertiles of vigorous LTPA and LTL were examined to investigate the inverse U-shape relationship between LTL and PA, which has been reported in the literature (13,19,36). In addition, we further adjusted for total moderate PA in our linear regression model which included four PA domains to examine the relative effect of four PA domains in a single model. We performed an additional step to further adjust for V˙O2max in a set of models using the subsample of participants 20–49 yr old (n = 1829) who completed the submaximal treadmill test. All data analyses were conducted using STATA SE 14.1 (StataCorp, College Station, TX). Statistical significance was determined by the alpha set at P value <0.05.

RESULTS

The average age of the population was 45.6 ± 0.38 yr old; half were female, and 40% of the population did not meet the PA recommendation for Americans. Education, non-White race, lower BMI, and never smoking were associated with longer LTL (Table 2). Table 3 displays the weighted statistics for PA measures in total population and according to LTL tertiles. The proportions of the population exceeding the PA recommendations across the tertiles, respectively, were 40%, 44%, and 46% (Table 3).

TABLE 2
TABLE 2:
Sociodemographic and health characteristics of the U.S. population according to LTL, NHANES 1999–2002 (n = 6933).
TABLE 3
TABLE 3:
Weighted characteristics of the study population, NHANES 1999–2002 (n = 6933).

The relationship between total moderate PA and LTL is shown in Figure 1. We found that an increase of 1 h·wk−1 of total moderate PA was associated with 0.08% longer LTL (P = 0.02), adjusted for age, gender, race, education, income, BMI, cigarette smoking, and alcohol drinking. Also, adjusted for sociodemographic and health characteristics, we found that an increase of 1 h·wk−1 in vigorous LTPA was associated with 0.31% (P < 0.001) longer LTL. Conversely, 1 h·wk−1 of household/yard work PA was associated with 0.21% (P = 0.03) reduction in LTL (Table 4). Other measures of PA such as transportation PA or moderate LTPA were not associated with LTL after adjusting for covariates. The proportion of the population who exceeded the recommended PA had 1.47% (P = 0.04) longer LTL compared with participants who did not meet the recommended PA, and there was no statistical difference between participants who did not meet the recommendation and participants who met but did not exceed the PA recommendation (P = 0.61) (P for trend <0.001) (Fig. 2).

FIGURE 1
FIGURE 1:
Scatter plot showing the log transformed LTL (T/S ratio) and total moderate PA (min·wk−1).
TABLE 4
TABLE 4:
Relationship between PA and LTL adjusted for demographic and health characteristics (n = 6933).*
FIGURE 2
FIGURE 2:
Weighted mean of LTL (T/S ratio) across PA recommendation groups. *P = 0.04 exceed recommendation compared with not meet recommendation.

In a further analysis, additionally adjusting for total moderate PA, to examine the relative effect of the four PA domains with LTL, results were similar to the previously mentioned data. Vigorous LTPA was associated with longer LTL (P = 0.01), household/yard work PA was inversely associated with LTL (P = 0.01), and transportation PA and moderate LTPA were not significantly associated with LTL. Compared with participants in the lowest vigorous LTL tertile (LTL = 1.0289 T/S ratio), on average, participants in the middle tertile had 1.1038 T/S ratio (P = 0.17) and participants in the highest tertile had 1.1041 T/S ratio (P < 0.01) (P for trend <0.001).

In a subgroup analysis (data not shown) adjusting for estimated V˙O2max and four PA domains and covariates (n = 1829), we again found similar relationships between PA and LTL: vigorous LTPA was positively associated with LTL (P = 0.002), and household/yard work PA, transportation PA, or moderate LTPA were not significantly associated with LTL.

DISCUSSION

We found that several measures of PA were associated with longer LTL, including vigorous LTPA, total time in moderate PA, and overall PA time exceeding the PA recommendation. Our findings suggest that being engaged in more PA, especially more vigorous LTPA, is associated with longer LTL. Our findings are consistent with those reported previously, supporting a positive relationship between PA and LTL (12,15,22,24,32). However, our findings do not support a previously reported inverted U-shape relationship between PA and LTL (13,19,36); instead, the relationship we found between PA and LTL was linear. To our knowledge, this is the first study reporting that vigorous LTPA is more closely associated with telomere length than other PA domains, and that only those exceeding the recommended PA level were found to have longer LTL compared with those who were not meeting the recommended PA level. Results from our study are in line with current evidence that vigorous PA has more health benefits than moderate PA (16).

The unexpected finding that longer time spent in household/yard work PA was associated with shorter LTL needs to be carefully interpreted and needs further investigation. No studies have examined these specific PA domains and their effects on telomere length. It is possible that household/yard work PA has a different effect on LTL compared with LTPA. Although the intent of the household/yard work PA questions was to capture activity that is beyond moderate intensity, many household yard work activities are considered low intensity (4). In a review of accelerometer outputs for adults, researchers concluded that many moderate lifestyle-oriented activities such as household chores are below traditional moderate-intensity cut points (28), further supporting the idea that participants may be including light household/yard work PA as moderate-intensity PA. In addition, there are mixed results on whether light household/yard PA has health benefits (1,18). It is possible that participants who reported household/yard work PA were engaged in lighter intensity rather than moderate to vigorous household/yard work PA. Nevertheless, it is important to note that there is a low correlation between questionnaire and accelerometer PA data (39), and that the negative association found could be due to uncontrolled confounding variables. Although the relationship between sedentary behavior and telomere length is not clear (15), it is known that sedentary behavior could lead to increased premature mortality risk (33). It is possible that participants who were engaged in household/yard work PA were also engaged in more sedentary behavior.

PA is a broad term, and examining total moderate PA may not be sufficient to identify its relationship with LTL. A previous study that examined mode-specific PA and LTL using NHANES data found that PA that involved running was the only type of PA that was positively associated with LTL (25). In another study, researchers created a movement-based behavior index, which summed moderate-intensity PA, vigorous-intensity PA, walking/cycling for transportation, and strengthening activities, and found that greater engagement in movement-based behavior was positively associated with LTL (24). These findings, along with ours, support that different PA domains and activities may vary in their effects on LTL.

In this sample, 17.26% of the variance in LTL was explained by PA domains and the covariates, age, gender, race, education, cigarette smoking, alcohol consumption, and BMI. Specifically, 15.61% of the variance in LTL can be accounted by age itself. Although vigorous LTPA and participation in activity exceeding the PA recommendation were positively associated with LTL, age had the greatest influence on LTL, with older age associated with shorter LTL.

Given that V˙O2max is partly genetic and those with higher V˙O2max can tolerate more vigorous activity (3), it is possible that those endowed with higher V˙O2max have longer LTL. A previous study examined the relationship between cardiorespiratory fitness (estimated V˙O2max) and LTL in the NHANES sample concluded that higher cardiorespiratory fitness was associated with longer LTL (23). The findings from our subsample (n = 1829; age 20–49) analysis suggest that an increase in vigorous LTPA was associated with longer LTL even after adjusting for estimated V˙O2max and other covariates, whereas activity such as household/yard work PA, transportation PA, or moderate LTPA were not associated with LTL. Of note, the relationship between cardiorespiratory fitness and LTL was not significant when the PA domains were included in the model; the association between LTL and V˙O2max could be due to the influence of vigorous LTPA. Engaging in vigorous LTPA may have a greater protective effect rather than higher cardiorespiratory fitness on LTL.

Despite the advantages of using a nationally representative sample, limitations should be noted. Given that these data are cross-sectional, directionality of the association cannot be determined, and we are not able to conclude causal relationships. Prospective studies may provide a better indication of the rate of telomere shortening over time. In addition, our PA measurements were self-reported, which could lead participants to overestimate or underestimate their PA time. In our population, more participants reported exercise levels exceeding the PA recommendation than meeting the guideline, which could be an indication of over estimation. In addition, our PA recommendation groups were created based on U.S. Department of Health and Human Services' Physical Activity Guidelines for Americans published in 2008 (40). Our data were collected during 1999–2000 and 2000–2002 cycles when the population had a different PA recommendation (30 min·d−1, five times per week). Our aim was to examine the association between current PA recommendation and LTL so that they would be relevant to today's guidelines.

In summary, an analysis in a nationally representative sample supports that participating in vigorous LTPA and exceeding the PA recommendation are associated with a longer LTL. This study produced several intriguing findings that highlight the need for additional research. Genetic components, sedentary behavior, dietary intake, inflammatory markers, and oxidative stress in the large U.S. representative sample will be important for fully understanding factors influencing telomere length. Moreover, objective measures of PA will be recommended to further substantiate the analysis as accelerometer-based objective measures of PA were added to the NHANES assessment in 2003, yet LTL has not been measured since then. Using objective measures of PA could eliminate overestimation and underestimation of each PA domain as well as being able to capture sedentary behavior. Future studies should examine the possible role of increased exercise in the maintenance of telomere length and its possible role leading to healthier and longer lives.

The present study was not funded by any additional resources, institution, or entity. The authors thank Dr. Philimon N. Gona for his assistance and support. The authors do not have any professional relationship with companies or manufactures that will benefit from the results of the present study. The results of the study do not constitute endorsement by the American College of Sports Medicine. The authors declare that the results of the study are presented clearly, honestly, and without fabrication, falsification, or inappropriate data manipulation.

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Keywords:

VIGOROUS LEISURE TIME PHYSICAL ACTIVITY; PHYSICAL ACTIVITY RECOMMENDATIONS; TELOMERE SHORTENING; NATIONAL HEALTH AND NUTRITION EXAMINATION SURVEY

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