Effect of Physical Activity, Smoking, and Sleep on Telomere Length: A Systematic Review of Observational and Intervention Studies
Abstract
1. Introduction
2. Materials and Methods
2.1. Search Strategy
2.2. Inclusion and Exclusion Criteria
2.3. Quality Control Analysis
3. Results
3.1. Association between PA and TL
Author, Reference | Year | Participants | TL Measurements | Tissue for TL Analysis | Exposure Assessment Methods | Results |
---|---|---|---|---|---|---|
Cassidy et al. [60] | 2010 | 2284 women from NHS | PCR | Blood | PA assessed by questionnaires | No association was observed between PA and TL |
Dankel et al. [61] | 2017 | 4881 subjects from NHANES | PCR | Blood | PA assessed by questionnaires | PA was associated with increased TL, except among those who were overweight or obese |
Ding et al. [62] | 2018 | 588 Chinese participants (18–64 y) | PCR | Blood | PA assessed by questionnaires | No associations were found between PA and TL |
Du et al. [63] | 2012 | 7813 women (43–70 y) from NHS | PCR | Blood | PA assessed by questionnaires | Women with moderate or vigorous activity had a longer TL than less active |
Fretts et al. [64] | 2018 | 2312 American Indian participants from SHFS | PCR | Blood | PA reported by pedometer | Participants in the upper PA quartiles had longer TL |
Hastings et al. [65] | 2019 | 6731 participants from NHANES | PCR | Blood | PA determined with different tests (muscle strength, cardiorespiratory capacity (VO2) and walking speed | Participants with shorter telomeres performed worse on physical function tests |
Kim et al. [66] | 2012 | 44 healthy postmenopausal women | PCR | Blood | PA reported by interview | Regular PA was associated with longer TL |
Latifovic et al. [67] | 2016 | 477 subjects (20–50 y) | PCR | Blood | PA assessed by questionnaires | Vigorous PA related to longer TL |
Loprinzi [68] | 2015 | 6405 participants from NHANES | PCR | Blood | Sedentary PA on screens (TV, computer …) reported by interview | Sedentary behavior based on screen free time was inversely associated with TL |
Loprinzi et al. [69] | 2015 | 6503 participants from NHANES | PCR | Blood | PA reported by interview | Lower TL among those who performed less PA |
Loprinzi et al. [70] | 2016 | 6474 participants from NHANES | PCR | Blood | PA reported by interview | The specific PA of running was the only activity associated with TL |
Ogawa et al. [45] | 2017 | 6933 participants from NHANES | PCR | Blood | PA reported by interview and VO2max in subsample | Those who undertake vigorous PA present longer TL than those who practice moderate PA or do not perform PA |
Sassenroth et al. [71] | 2015 | 815 participants from BASII | PCR | Blood | PA assessed by questionnaires | PA was associated with longer TL only when PA was regular and ≥10 y preceding the assessment |
Savela et al. [72] | 2013 | 204 participants from HBS | SB | Blood | PA assessed by questionnaires | An U-shaped association was found. Moderate PA associated with longer TL |
Shadyab et al. [73] | 2017 | 1476 elderly women from WHI | SB | Blood | PA assessed by questionnaires | Longer TL in the group of more active women compared to those who undertook less PA |
Shadyab et al. [74] | 2017 | 1481 elderly women from WHI | SB | Blood | PA assessed by questionnaires and accelerometer | Longer sedentary time was associated with shorter TL in physically inactive older women |
Shadyab et al. [75] | 2017 | 1405 elderly women from WHI | SB | Blood | PA assessed by questionnaires and accelerometer | Women at the highest level of total PA compared to the lowest level had longer TL, but significance was lost after adjustment for confounded terms |
Silva et al. [76] | 2017 | Elderly subjects (65–85 y) with intense and moderate training, and never trained | Flow-FISH | Blood | PA assessed by questionnaires and VO2max | TL was longer in the intense training group compared to the untrained group |
Song et al. [77] | 2010 | 170 subjects (18–80 y) | PCR ELISA | Blood | PA assessed by questionnaires | PA was inversely correlated with biomarkers of DNA damage, and these biomarkers were negatively associated with TL |
Tucker LA [46] | 2017 | 5.823 adults from NHANES | PCR | Blood | PA assessed by questionnaires | PA was inversely associated with TL. High levels of PA were associated with longer telomeres, with a biological aging of 9 y difference compared with the sedentary ones |
von Känel et al. [78] | 2017 | African (n = 96) and Caucasian (n = 107) schoolteachers from SAABPAS | PCR | Blood | PA measured by accelerometry | Regular PA of different intensity was not directly associated with TL |
Williams et al. [79] | 2017 | 5674 adults from NFBC | PCR | Blood | PA determined by physical tests | TL was associated with greater aerobic fitness and muscular endurance only in young adults |
Xue et al. [80] | 2017 | 518 adults from China | SB | Blood | PA assessed by questionnaires | Watching TV was associated with shorter TL However, doing moderate or vigorous PA was not associated with TL |
Author, Reference | Year | Type | Participants | TL Measurements | Tissue for TL Analysis | Exposure Assessment Methods | Results |
---|---|---|---|---|---|---|---|
Colon et al. [81] | 2019 | CC | 7 male triathlon athletes and 7 active controls | PCR | Blood | PA assessed by questionnaires and VO2max | The triathlete subjects had longer telomeres than the active controls. Positive association between TL and VO2max |
Denham et al. [27] | 2016 | CC | Polish endurance athletes (n = 61) and paired active controls (n = 61) | PCR GE | Blood | PA reported by questionnaires | Endurance athletes have longer TL, as well as a higher expression of TERT mRNA |
Denham et al. [82] | 2013 | CC | 67 male ultramarathon runners and 63 controls | PCR | Blood | PA assessed by questionnaires | Ultramarathon runners had telomeres 11% longer than controls |
LaRocca et al. [83] | 2010 | CC | 57 participants: differing by age and PA | SB | Blood | PA assessed by questionnaires and VO2max | TL of the older endurance-trained adults was greater than their sedentary peers. TL was positively related to VO2max |
Magi et al. [84] | 2018 | CC | 26 men (20–50 y) | SB | Muscle | PA reported by interview | Regular physical training was positively with the maintenance of TL |
Mathur et al. [85] | 2013 | CC | 17 marathon runners and 15 controls | FISH | Blood | Different tests were performed | No differences were observed in the TL of the different PA groups or tests |
Muniesa et al. [86] | 2017 | CC | 125 young elite athletes | PCR | Blood | PA reported through a database | Elite athletes had a TL 12.4% longer than controls |
Osthus et al. [87] | 2012 | CC | 10 young and 10 elderlies (50% endurance athletes, 50% medium level) | PCR | Muscle | PA assessed by questionnaires and VO2max | Older endurance athletes had longer TLs compared to their counterparts. These differences were not seen in the young participants |
Puterman et al. [88] | 2010 | CC | 63 postmenopausal women | PCR | Blood | PA assessed by questionnaires | No association between PA and TL was observed. However, vigorous PA was linked to TL |
Rae et al. [89] | 2010 | CC | 18 endurance runners vs. 19 controls | SB | Muscle | PA assessed by questionnaires | No significant differences were found between the mean and minimum TL between the endurance runners and controls |
Simoes et al. [90] | 2017 | CC | Elite sprinters (n = 11) and untrained controls | PCR | Blood | PA reported by medical history | Elite sprinters have longer TL than their paired controls |
Soares-Miranda et al. [91] | 2015 | L | 582 elderly subjects from CHS | SB | Blood | PA assessed by questionnaires and different tests | At baseline, higher PA was associated with longer TL. Prospective analyses show that changes in PA were associated with differences in changes in TL |
Stenbäck et al. [92] | 2019 | L | 700 elderly subjects (Finland) | PCR | Blood | PA assessed by questionnaires and accelerometry | PA for 2-w was not associated with TL after adjustment. However, moderate PA was associated with longest TL |
Weischer et al. [93] | 2014 | L | 4576 participants from CCHS | PCR | Blood | PA assessed by questionnaires | Increased PA was associated with short TL at baseline, but not with a change in TL during 10 years of follow-up |
Author, Reference | Year | Participants | TL Measurements | Tissue for TL Analysis | Intervention | Results |
Borghini et al. [94] | 2015 | 17 male endurance athletes and 32 controls | PCR | Saliva | Ultra-endurance race in athletes (330 km in a maximum time of 150 h) | Endurance athletes present longer TL than controls. Acute extreme intervention increased TL attrition compared to baseline |
Brandao et al. [95] | 2020 | 20 obese sedentary women (20–40 y) | PCR | Blood | Combined aerobic and strength training (55 min/d, 3 times/w, 8 w) | Combination training for 8 w promoted an increase in TL, fat-free mass, and physical performance |
Chilton et al. [96] | 2014 | 22 healthy young men, nonsmokers | GE | Blood | 30 min of continuous running on a treadmill at 80% O2 | Increased expression of the key telomeric gene TERT mRNA, associated with longer TL |
Diman et al. [97] | 2016 | 10 healthy and moderately active young men | FISH GE | Muscle | Two cycling exercise groups: low intensity (50% VO2) and a high intensity (75% VO2). | Endurance cycling exercise increased the TERRA gene expression, a key player in telomere integrity, associated with longer TL |
Dimauro et al. [98] | 2017 | 24 men, 12 T2D and 12 controls. | FISH | Blood | Two groups: untrained and trained (moderate PA over at least 1 y) | Individuals who participated in the regular exercise program showed longer TL |
Friedenreich et al. [99] | 2018 | 212 Healthy women aged (50–74 y). | PCR | Blood | Two groups: aerobic exercise (45 min, 5 d/w for y, n = 99) vs. inactivity | No association between aerobic exercise and TL |
Laye et al. [100] | 2012 | 8 participants in the “2010 Bornholm Ultramarathon 7” | PCR GE | Muscle and whole blood | Carrying out 7 marathons on 7 consecutive d | A positive regulation of gene expression of the components of the shelterin complex was found without observing changes in TL |
Mason C et [101] | 2013 | 439 women with overweight or obesity (50–75 y) | PCR | Blood | Four groups: weight loss with diet (n = 118), PA (n = 117), diet + exercise (n = 117) and control (n = 87); for 12 m | After 12 m, no changes were seen in the TL of the intervention groups compared to the control group |
Puterman et al. [102] | 2018 | 68 careers of elderly people | PCR | Blood | Two groups: aerobic training and control for 24 w | Significant changes in TL were observed in aerobic exercise intervention group |
Sjögren et al. [103] | 2014 | 49 participants (68 y) with low PA | PCR | Blood | Two groups: PA and minimal PA. Intervention for 6 m | The decrease in seated time in the intervention group was associated with TL |
Werner et al. [44] | 2019 | 125 inactive participants | PCR FlowFISH FACS | Blood | Three groups: aerobic endurance training; high intensity exercises; resistance training | Endurance training and high intensity, but not strength training, was associated with increased telomerase activity and TL |
Zietzer et al. [104] | 2017 | 26 youth and 14 elderly participants | PCR | Blood | Randomization to 2 trials: -ISRT-1: crossover trial (2 separate sessions). -ISRT-2: 1 session of ISRT, and subsequently 5 d/w of 90 min. | Telomerase activity in young individuals increased with exercise. In contrast, short-term ISRT exercises were not associated with telomerase activity. However, after 5 w of daily ISRT, telomerase increased |
3.2. Association between Telomere Length and Tobacco Smoking
Author, Reference | Year | Participants | TL Measurements | Tissue for TL Analysis | Exposure Assessment Methods | Results |
---|---|---|---|---|---|---|
Cassidy et al. [60] | 2010 | 2284 women from NHS | PCR | Blood | Tobacco smoking reported by questionnaire | Tobacco use was not associated with TL |
Flannagan et al. [105] | 2017 | 20 smokers and 20 non-smokers | PCR | Blood | Tobacco smoking reported by questionnaire | No association was detected between smoking and TL |
Gao et al. [106] | 2016 | 548 participants from ESTHER | PCR and methylation | Blood | Tobacco smoking reported by questionnaire | Lower methylation was observed in current smokers associated with TL |
Huzen et al. [107] | 2014 | 8592 subjects from PREVEND | PCR | Blood | Tobacco smoking reported by questionnaire | Dose-dependent association between number of cigarettes smoked and baseline TL |
Khan et al. [108] | 2019 | 5864 participants from NHANES | PCR | Blood | Tobacco smoking reported by questionnaire | No association was detected between TL and smoker status, but there was an inverse association between the number of cigarettes smoked and shorter TL |
Latifovic et al. [67] | 2016 | 477 subjects (20–50 y) | PCR | Blood | Tobacco smoking reported by questionnaire | Smokers had shorter TL than those who had never smoked |
Lei et al. [109] | 2020 | 500 African Americans from FACHS | Methylation arrays | Blood | Tobacco smoking reported by questionnaire | Associations between smoking and aging by differences in methylation |
Lu et al. [110] | 2019 | 2256 participants from WHI and JHS; 1078 participants from FHS | SB and methylation arrays | Blood | Tobacco smoking reported by questionnaire | Being a smoker was associated with lower values of mtlDNA (level of DNA methylation as an estimator of TL). In addition, smoking was associated with a shorter TL |
Lu et al. [111] | 2017 | 1303 non-smoking adult participants from GS:GFHS | PCR | Blood | Tobacco smoking reported by questionnaire | TL decreased more rapidly with increasing age among passive smokers compared to those who were not exposed |
Nawrot et al. [112] | 2010 | 216 non-smokers and 89 smokers from FLEMENGHO | SB | Blood | Tobacco smoking reported by questionnaire | The TL of smokers was shorter than in non-smokers |
Needham et al. [113] | 2013 | 5360 subjects from NHANES | PCR | Blood | Tobacco smoking reported by questionnaire (number of cigarettes/d and years of smoking) | Smokers of 60 packs of cigarettes/y or more showed significantly shorter TL than those who had never smoked |
Patel et al. [114] | 2017 | 461 subjects NHANES | PCR and GE | Blood | Tobacco smoking reported by questionnaire | The number of cigarettes smoked/d was associated with a shorter TL, but no differences were detected in the expression levels of candidate genes |
Rode et al. [115] | 2014 | 55,568 participants from CGPS | PCR | Blood | Tobacco smoking reported by questionnaire | An association was observed between high cumulative tobacco use and short TL |
Song et al. [77] | 2010 | 170 adults (18–80 y) | PCR | Blood | Tobacco smoking reported by questionnaire | Inverse association between smoking and TL |
Sulastri et al. [116] | 2017 | 130 Minangkabau men (40–50 y) | PCR | Blood | Tobacco smoking reported by questionnaire | Smoking was a risk factor for telomere shortening |
Sun et al. [117] | 2012 | 5862 women from NHS | PCR | Blood | Tobacco smoking reported by questionnaire | Compared to current smokers, women who had never smoked had longer TLs |
Verde et al. [118] | 2015 | 147 healthy smokers from Spain | PCR | Blood | Smoking habit was determined by survey and Fagerström test | Association between cumulative tobacco use and years of smoking and reduction in TL. No significant differences between the values of metabolized nicotine and TL |
Weischer et al. [93] | 2014 | 4576 participants from CCHS | PCR | Blood | Tobacco smoking reported by questionnaire | Short TL was associated with increased tobacco use |
Wulaningsih et al. [119] | 2016 | 6456 participants from NHANES | PCR | Blood | Questionnaires for smoking and serum cotinine levels were evaluated | Being a smoker was associated with a 50 bp decrease in TL compared to those who had never smoked |
Yun et al. [120] | 2019 | 1037 adults (729 white and 308 African American) | SB | Blood | Tobacco smoking reported by questionnaire | An association was observed between smoking and TL. Body weight had a suppressing effect on this association |
Author, Reference | Year | Type of Study | Participants | TL Measurements | Tissue for TL Analysis | Exposure Assessment Methods | Results |
---|---|---|---|---|---|---|---|
Zhang et al. [121] | 2016 | Longitudinal | 5624 participants from HRS, 16 y follow up | PCR | Saliva | Tobacco smoking reported by questionnaire | Shorter TL observed in smokers. The number of cigarettes was also inversely associated with TL in women, but not in men. Sex-specific prospective changes on smokers and TL were detected |
Bendix et al. [122] | 2014 | Longitudinal | 1356 individuals (30–70 y). 10-y follow-up | PCR | Blood | Tobacco smoking reported by questionnaire | Tobacco influences the change in TL after follow-up, with smokers having a greater risk of telomere shortening |
Chen et al. [123] | 2011 | Longitudinal | Follow-up of 271 participants at 3 times | SB | Blood | Tobacco smoking reported by survey | Smoking at baseline was associated with shorter TL and accelerated shortening |
Marcon et al. [124] | 2017 | Twin study (case-control) | 22 homozygous twins (one smoker and the other non-smoker) | SB and methylation arrays | Blood | Tobacco smoking reported by questionnaire, and urine cotinine | Statistically significant higher values of TL in smokers compared to non-smoking twins |
Müezzinler et al. [125] | 2015 | Longitudinal | 3600 elderly adults. Follow-up on 1000 participants | PCR | Blood | Tobacco smoking reported by questionnaire | Smoking was inversely associated with TL at baseline. On average, current smokers had 73 bp shorter telomeres, but this relationship could not be shown longitudinally |
Strandberg et al. [126] | 2011 | Longitudinal | 622 participants from Finland (30–45 y). Follow-up at 30–40 years | SB | Blood | Tobacco smoking reported by questionnaire | Age-adjusted TL was significantly longer among lifelong non-smokers compared to past or present smokers |
Walters et al. [127] | 2014 | Case-Control | Healthy smokers (n = 29) vs. non-smokers (n = 29) | SB | Epithelial cells or whole blood | Tobacco smoking reported by questionnaire, and urine cotinine | No differences were observed between TL and being a smoker or not |
3.3. Association between Telomere Length and Sleep
Author, Reference | Year | Type of Study | Participants | TL Measurements | Tissue for TL Analysis | Exposure Assessment Methods | Results |
---|---|---|---|---|---|---|---|
Cribbet et al. [128] | 2014 | Cross-sectional | 154 subjects (45–77 y) | PCR | Blood | Sleep quality and duration by questionnaire (PSQI) | Better quality of sleep was significantly associated with longer TL. Sleep durations of >7 h/night or ≤5 h/night associated with shorter TL in older adults. Sleep duration in middle-aged adults was not associated with TL |
Grieshober et al. [129] | 2019 | Cross-sectional | 3145 post-menopausal women (EA, AA) from the WHIS | SB | Blood | Sleep duration and sleep disturbance by questionnaires (WHIIRS) | Longer TL was associated with longer sleep duration in the whole sample (associations being strongest among AA). No associations were observed with sleep disturbances |
Jackowska et al. [130] | 2012 | Cross-sectional | 494 men and women (mean age 63.3 y) from the WIIS | PCR | Blood | Sleep duration assessed by interview | Sleep duration was associated with TL in men, but not in women. TL was 6% shorter in men who sleep ≤5 h/night compared to >7 h/night |
Liang et al. [43] | 2011 | Cross-sectional | 4117 women from the NHS | PCR | Blood | Sleep duration and rotating night shifts assessed by questionnaires | Sleep duration was associated with TL (compared to women in the 9 h/night, those in the <6 h/night category, had decreased TL). However, heterogeneity by age was observed (sleep duration and TL were only associated in women <50 y, and not older). No significant associations were found between rotating shift history and TL |
Nguyen et al. [131] | 2020 | Cross-sectional | 1070 parents/careers with a (mean age 44 y), from the LSAC | PCR | Blood | Sleep behavior determined by interview and actigraphy over 8 d | Sleep duration and most other sleep metrics were not associated with TL |
Prather et al. [132] | 2015 | Cross-sectional | 87 obese adults from a trial (San Francisco, CA) at baseline | PCR (DTC) | Blood | Sleep quality and duration by questionnaire (PSQI) | Poorer global sleep quality was associated with shorter TL in lymphocytes, but not in granulocytes. Sleep duration was not related to TL |
Prather et al. [133] | 2011 | Cross-sectional | 245 women (49 to 66 y) | PCR | Blood | Sleep quality and duration by questionnaire (adapted from the PSQI) | Lower sleep quality was associated to shorter TL |
Tempaku et al. [134] | 2018 | Cross-sectional | 925 participants from EPISONO cohort | PCR | Blood | Sleep quality and duration assessed by questionnaires (PSQI, UNIFESP, Epworth, ISI, PSPDN), and polysomnography | Insomnia disorders and long sleepers were associated with shorter TL |
Wynchank et al. [135] | 2019 | Longitudinal | 2936 European subjects from the NSDA analyzed at two waves 6 y apart | PCR | Blood | Sleep duration and insomnia symptoms by questionnaire (ISR). Chronotype determined by the MCTQ | Indicators of delayed circadian rhythm, Late MSFsc, late sleep onset time, and moderately late chronotype, were associated with shorter TL at both waves. No predictors showed accelerated TL attrition over 6 y. Sleep duration and insomnia were not associated with TL |
Zgheib et al. [136] | 2018 | Cross-sectional | 497 Lebanese (men and women >18 y) | PCR | Blood | Sleep habits determined by questionnaire (3 questions) | Difficulties to sleep (but not short sleep duration) were associated with shorter TL |
Zhao H [137] | 2017 | Cross-sectional | 12,178 Mexican Americans (20–85 y, 80% women) from the MM:MACS | PCR | Blood | Sleep duration determined by questionnaire | TL was associated with sleeping time per d (longer in those participants who slept at least 9 h/d, followed by those who slept between 7–8 h/d, and shortest in those who slept ≤6 h/d) |
4. Discussion
5. Conclusions
Author Contributions
Funding
Institutional Review Board Statement
Informed Consent Statement
Conflicts of Interest
References
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Barragán, R.; Ortega-Azorín, C.; Sorlí, J.V.; Asensio, E.M.; Coltell, O.; St-Onge, M.-P.; Portolés, O.; Corella, D. Effect of Physical Activity, Smoking, and Sleep on Telomere Length: A Systematic Review of Observational and Intervention Studies. J. Clin. Med. 2022, 11, 76. https://doi.org/10.3390/jcm11010076
Barragán R, Ortega-Azorín C, Sorlí JV, Asensio EM, Coltell O, St-Onge M-P, Portolés O, Corella D. Effect of Physical Activity, Smoking, and Sleep on Telomere Length: A Systematic Review of Observational and Intervention Studies. Journal of Clinical Medicine. 2022; 11(1):76. https://doi.org/10.3390/jcm11010076
Chicago/Turabian StyleBarragán, Rocío, Carolina Ortega-Azorín, Jose V. Sorlí, Eva M. Asensio, Oscar Coltell, Marie-Pierre St-Onge, Olga Portolés, and Dolores Corella. 2022. "Effect of Physical Activity, Smoking, and Sleep on Telomere Length: A Systematic Review of Observational and Intervention Studies" Journal of Clinical Medicine 11, no. 1: 76. https://doi.org/10.3390/jcm11010076
APA StyleBarragán, R., Ortega-Azorín, C., Sorlí, J. V., Asensio, E. M., Coltell, O., St-Onge, M.-P., Portolés, O., & Corella, D. (2022). Effect of Physical Activity, Smoking, and Sleep on Telomere Length: A Systematic Review of Observational and Intervention Studies. Journal of Clinical Medicine, 11(1), 76. https://doi.org/10.3390/jcm11010076