✕
Journal of Obesity & Metabolic Syndrome

Search

Article

J Obes Metab Syndr 2019; 28(2): 92-104

Published online June 30, 2019 https://doi.org/10.7570/jomes.2019.28.2.92

Copyright © Korean Society for the Study of Obesity.

How Does Obesity and Physical Activity Affect Aging?: Focused on Telomere as a Biomarker of Aging

Yun-A Shin

Author Affiliations

Department of Prescription and Rehabilitation of Exercise, College of Sport Science, Dankook University, Cheonan, Korea

Correspondence to:
Yun-A Shin,
https://orcid.org/0000-0002-8480-3454,
Department of Prescription and Rehabilitation of Exercise, College of Sport Science, Dankook University, 119 Dandae-ro, Dongnam-gu, Cheonan 31116, Korea,
Tel: +82-41-550-3831,
Fax: +82-41-550-3831,
E-mail: shinagel@dankook.ac.kr

Received: May 6, 2019; Reviewed : May 23, 2019; Accepted: June 7, 2019

This is an Open Access article distributed under the terms of the Creative Commons Attribution Non-Commercial License (http://creativecommons.org/licenses/by-nc/4.0/) which permits unrestricted non-commercial use, distribution, and reproduction in any medium, provided the original work is properly cited.

Abstract

Go to

Obesity is known to continuously increase systemic inflammation and oxidative stress, leading to shorter telomere length. However, research regarding the correlation between physical activity, exercise, obesity, and telomere length is not consistent. Therefore, this review aims to summarize the effects of obesity, physical activity, and exercise on telomere length. Our search for effects of obesity, physical activity, and exercise, on telomeres was conducted using three computerized databases: Medline, PubMed, and EBSCO. Keywords in the search were “physical activity, exercise and obesity,” “physical activity, exercise and telomere,” and “obesity and telomere.” Improving chronic inflammation and oxidative stress levels can prevent telomere attrition due to obesity. In addition, differences in the anti-aging effects of physical activity and exercise are shown in the post-middle-age period, when telomere length changes, rather than in past exercise habits. Maintaining high cardiorespiratory fitness levels through regular exercise and physical activity in the post-middle-age period minimizes obesity-related diseases and helps maintain telomere length, which is an index of cell senescence.

Keywords: Telomere, Obesity, Physical activity, Exercise, Cardiorespiratory fitness

INTRODUCTION

Go to

Obesity is a major risk factor that increases mortality and the prevalence of associated age-related diseases.1 Obesity is known to continuously increase systemic inflammation and oxidative stress2, leading to shorter telomere length (TL).3

Telomeres are DNA protein complexes on the end of the chromosomes of human eukaryotic cells4 and have been reported to generally shorten with age.5 While inflammation and oxidative stress are major causes of aging, they also play an important role in telomere attrition6, and studies on the association of TL with chronic inflammation and oxidative stress have been reported.7

Recent systemic reviews have reported various results regarding the correlation between body weight status and TL, with some claiming an inverse correlation between obesity and TL8–10 and others indicating that there is no correlation.11,12 However, a meta-analysis based on cross-sectional studies reported that body mass index (BMI) and TL have an inverse association.7

Telomeres are not only affected by oxidative stress and inflammation, but also by lifestyle habits such as smoking and sedentary behavior.13–15 Recent reports have documented that physical activity is associated with TL in adults16–18, since physical activity reduces obesity, type 2 diabetes, the risk of hypertension and cancer and improves visceral fat, bone fitness, and insulin resistance.19,20

It is widely known that exercise improves cardiorespiratory function and weight loss and decreases the risk of early chronic diseases. Furthermore, the increase in oxygen consumption during exercise leads to the generation of active oxygen, which causes oxidative stress.21 Studies have shown that high intensity exercise increases oxidative stress and cause cell damage.22 Studies have also reported that excessive physical activity and exercise can promote a decrease in TL.23 Thus, the correlation between physical activity, exercise, and TL is still unclear. Moreover, research findings are not consistent in this area. Some studies report that physical activity reduces the prevalence of obesity-related diseases and that it is effective in weight loss, whereas other studies report that it is ineffective.24,25 Therefore, the purpose of this review is to investigate the correlation between obesity and TL and to determine the effects of physical activity and exercise on obesity and TL through related studies.

TELOMERE AND AGING

Go to

Telomeres are composed of hexanucleotide sequences (TTAGGG) at the ends of eukaryotic chromosomes. The TL of adult mitotic cells decrease due to certain parts not being replicated during every cell division.26,27 When telomeres, which shorten after every cell division, reach a critical point, they cause arrest and malfunction of the cell cycle. This causes replicative senescence and potential genomic instability, leading to cell death.28 Therefore, telomeres reflect divisional activity (loss and stability) of each cell and are used as indicators of biological aging.29

Telomeres are affected by tissue oxidative stress and inflammation30, and chronic inflammation promotes telomere attrition by increasing white blood cell replacement.31 In addition, oxidative stress conditions promote TL attrition in cell replication by decreasing the activity of telomerase, which is the polymerase responsible for maintaining TL.3

People with cardiovascular disease (CVD) are reported to have shorter TL compared to healthy individuals.32 TL is reported to have a negative correlation with factors that cause CVD such as age, BMI, waist-to-hip ratio (WHR), hypertension, triglycerides, fasting blood glucose levels, and body fat mass.33 Hypertension causes continuous stress on blood vessels and endothelial cells and promotes remodeling, thereby increasing oxidative stress and decreasing TL.34 It has been reported that diabetes also promotes cellular aging of tissues associated with glucose transport and metabolism, thereby affecting telomere attrition.35 The accumulation of atherosclerotic plaques in blood vessels affects the aging of vascular endothelial and smooth muscle cells resulting TL reduction. Coronary artery disease is also reported to have a negative correlation with TL.36

Many studies have also reported that shortened telomeres in leukocytes increase the prevalence and risk of disease due to aging.37,38 Short telomeres are involved in disease pathogenesis because senescent cells increase the secretion of proinflammatory cytokines and extra-cellular matrix-degrading enzymes, which promotes disease progression.39,40 Thus, telomere attrition may occur with risk factors and conditions that cause disease, and shortened telomeres may be responsible for promoting diseases caused by aging.

OBESITY AND TELOMERE

Go to

The association between obesity and TL

It is reported that obesity and TL reduction may be correlated because obesity increases oxidative stress and chronic systemic inflammation (Table 1). There is an inverse correlation between TL and BMI, WHR, total fat, and waist circumference (WC), and abdominal adipose tissue is directly related to TL attrition and promotes the aging process.8,9,15,16,41–49 Njajou et al.9 and García-Calzón et al.10 also reported that higher WCs were associated with shorter telomeres, even after age adjustment. However, because many studies have used indirect anthropometric measurements, study results on the correlation between obesity, abdominal fat, and TL have not been consistent. Some studies have shown that telomeres correlate with obesity indices45–47, whilst some report no correlation in middle-aged people11,12 or the elderly.50–52

TLs of adipose tissue are reported to have a negative relationship with WC and adipose tissue size regardless of age.44 It has been reported that subcutaneous adipose tissue and visceral adipose tissue telomeres have a negative correlation with BMI, blood pressure, hyperlipidemia, and the size of adipose tissue. Thus, metabolic diseases associated with obesity seem to be correlated with the amount of fat tissue and TL attrition.42–44

The effect of change of body weight or fat mass on telomere

Weight gain and obesity are reported to promote telomere attrition regardless of age (Table 2). Rapid weight gain since the age of 18 has been reported to promote telomere attrition.11 A study of 2,912 Chinese women aged 40–70 years showed that TL was shorter when weight gain after age of 50 was more than 15%.46 Furthermore, in a study of 2,721 elderly people aged 70 to 79 years, TL was reported to be shorter with increased body weight and adipose tissue.9

On the other hand, it was also reported that weight loss was correlated with TL elongation. TL elongation was positively correlated with weight loss, and the lengthening rate increased with increase in weight loss.53 In a study of 521 adults aged 55 to 80 years and elderly subjects who underwent the Mediterranean diet intervention for 5 years, TL was inversely correlated with changes in fat tissue including body weight, BMI, WC, and WHR, and it was reported that TL underwent elongation.54 These results suggest that weight loss prevented the decrease of TL and DNA damage.55 Oxidative stress and chronic inflammation due to obesity accelerate telomere attrition56, and telomere DNA is very sensitive to oxidative stress damage. Oxidative stress plays an important role in the decrease of TL, because explicative senescence is considered a stress response blocking the growth of cells that have a high risk of mutation.22 Therefore, it can be suggested that telomere lengthening is correlated with weight loss, decrease of inflammation and oxidative stress. Weight loss intervention not only prevents telomere shortening, but also plays an important role in telomere elongation.53 Another study showed that TLs of severely obese subjects were significantly shortened at 3, 6, 9, and 12 months after bariatric surgery and additional attrition occurred immediately after surgery, likely because of their catabolic state.57 However, there was a report that weight loss through dietary and exercise treatments for 12 months were not correlated with changes in TL.58 Thus long-term studies are needed to observe changes in TL.

Taken together, obesity is correlated with TL decreases due to chronic inflammation and oxidative stress. Obesity-related indicators (WC, WHR, or fat mass) also seem to be correlated to TL. In addition, weight loss has the effect of elongating telomeres, but weight loss through bariatric surgery is considered a catabolic state that promotes TL reduction, indicating that further studies are needed.

The mechanism on association between obesity and TL

Obesity is generally caused by the accumulation of excessive fat tissue due to excessive dietary intake and lack of physical activity.59 The accumulation of ectopic fat surrounding organs is directly correlated to insulin resistance, which is a major cause of metabolic syndrome and CVD.60 Obesity also results in the formation of reactive oxygen species and cytokines which are increased in the inflammation processes. These processes are key factors that may explain the association between obesity and telomere shortening, because inflammation induces further inflammatory reactions causing DNA damage.30 DNA migration was increased in the lymphocytes of overweight and obsese.61 These DNA damage responses are defined by the consequences of genomic instability. This is the reaction of cells to damaged DNA to prevent negative health conditions such as the initiation of mitotic senescence, arrest, repair, and cell death.62–64

Adipose tissue plays a key role in this reaction. Accumulation of visceral fat (abdominal fat) also increases fat cells and is associated with dysfunctional fat tissue.65 Fat, or adipose tissue, plays an important role in the physiological processes of tissues. It plays a role in the production of inflammatory cytokines and chemokines as well as in host defense, immunity, and injury response.66 The mechanism of a proinflammatory state accompanied by obesity may be associated with hyperplasia and hypertrophy of adipocytes, which can induce adipose tissue hypoxia. Dysfunction of adipose tissue causes secretion of prostaglandins, C-reactive proteins (CRPs), and cytokines such as interleukin-6, tumor necrosis factor alpha, and leptin, and proinflammatory biomarkers.67,68 It also lowers the level of adiponectin such as anti-atherosclerotic adipokines. This abnormal secretion of adipose tissue causes type 2 diabetes, hyperlipemia, and CVD.69,70 Obesity, metabolic syndrome, and CVD prevent malignant transformation through the activation of processes that lead to senescence and programmed cell death. These response mechanisms play a key role in the increased of inflammation via DNA damage and the activation of transcription factors as well as telomere dysfunctions.62,64

A high fat ratio in muscle also causes metabolic dysfunction by increasing the circulation of free fatty acids. Increased circulating free fatty acids increase insulin secretion to control glucose metabolism, and hyperinsulinemia reduces insulin sensitivity and causes type 2 diabetes.71 Chronic systemic inflammation also increases oxidative stress and reduces metabolic flexibility, leading to metabolic syndromes and a vicious cycle of disease72 as well as shorter TL.

PHYSICAL ACTIVITY AND TELOMERE

Go to

Effect of physical activity on metabolic health independent from obesity

Several studies have reported a strong correlation between obesity and physical inactivity73–75, and metabolic syndromes have also been associated with sedentary lifestyles and low cardiorespiratory fitness.76 Ostman et al.77 used a systematic review and meta-analysis to conclude that exercise was inversely correlated to body composition, blood cholesterol, fasting plasma glucose, fasting insulin, blood pressure, and clinical outcomes. Hayashino et al.78 also reported that exercise interventions affected insulin resistance, inflammatory markers/cytokines, and adipokines that cause metabolic syndrome and CVD and that there were measurable effects in the decrease of systemic inflammation as exercise duration and frequency increased.

Unlike the positive effects of exercise on disease, results of the effects of exercise on weight loss were somewhat inconsistent. According to a meta-analysis on weight loss effects by Votruba et al.79, six out of 11 studies reported weight loss in which exercise was performed without dietary control, whereas the other five studies reported no change in body weight. In another meta-analysis study, exercise alone resulted in 3 kg weight loss in men after 30 weeks and 1.4 kg weight loss in women after 12 weeks, suggesting that exercise-induced weight loss is limited.80 In a meta-analysis of 16 studies, 11 studies showed a significant decrease in body weight after exercise, but the decrease in body weight was within the range of 0.1 to 5.2 kg and the difference in weight loss between the exercise group compared to a control group who did not exercise was 0.6 to 3.0 kg. The effect of weight loss for exercise alone without dietary control was very limited.81

The effect of exercise on weight loss varies according to the exercise volume. In a study that conducted high intensity (≥65% maximum oxygen consumption [VO2max]) exercise 6 to 7 days per week for at least 30 minutes to 2 hours, a 10 to 20 kg weight loss was reported.82–84 However, other studies have shown that weight loss was in the range of 0.2 to 1.5 kg despite high intensity training.85,86 Such differences in study results exist because exercise volume and weight loss do not necessarily have a measurable correlation, and the threshold of weight loss with exercise is different according to sex, individual differences, and the forms of exercise.87 Furthermore, compensatory actions such as a decrease in basal metabolism is induced because as the intake is reduced by 7,700 kcal, the amount of body weight is reduced by 70% and the amount of fat is reduced by 30%.88,89

Although the weight loss effect of exercise was limited, the risk factors associated with being overweight and obese were reduced even with no change in body weight or a small weight loss of less than 5 kg.90,91 Exercise, regardless of weight loss, has the effect of reducing abdominal obesity, and decreasing abdominal obesity has the effect of reducing systemic inflammation and risk factors for metabolic syndrome and CVD.92,93 Exercise has anti-inflammatory effects regardless of weight loss because it reduces hypoxia in adipose tissue by increasing capillary blood flow.94 In addition, exercise training reduces CRP levels and BMI; this has been observed even without a reduction in body weight.95 The anti-inflammatory effect of exercise reduces oxidative stress, which improves glucose tolerance, insulin resistance, and fat metabolism, and has the effect of reducing blood pressure in people with metabolic diseases as well as in healthy people.96

Therefore, exercise induces a positive improvement in the prevalence of obesity and obesity-related diseases by reducing abdominal obesity, systemic inflammation, and oxidative stress, thereby reducing the risk factors of obesity-related diseases.

Effect of physical activity on telomere in adults

It is well known that regular physical activity improves cardiorespiratory function, induces some weight loss, and lowers the risk of early chronic disease. However, it has been reported that the increase of oxygen consumption during exercise increases the oxidative stress by inducing active oxygen.21 In particular, high intensity exercise greatly increases oxidative stress, resulting in cell damage. Thus, various results on the correlation between physical activity and TL have been reported.22

Many previous studies have reported that people with higher levels of physical activity have longer TLs than those who have a sedentary lifestyle (Table 3). Cherkas et al.16 reported that people with the highest physical activity had longer TLs by 200 nucleotides (7.1 vs. 6.9 bp) than those with the lowest physical activity, suggesting that regular physical activity can prevent aging. It has also been reported that the higher the level of physical activity and the amount of physical activity per week, the longer the TL is.58,97,98

However, while physical activity of moderate intensity (991–3,540 kcal/wk) results in longer TLs, too much physical activity (9,351 kcal/wk) can result in shorter TLs.17 In another study, the TL reduction rate of a moderate intensity exercise group was lower than that of the high intensity and control groups.99 Some studies reported that physical activity was negatively correlated with levels of DNA damage, but not with TL100, whilst others reported that there was no correlation between TL and physical activity.11 As such, study results are inconsistent. Regarding the different study results, the differences in TL and physical activity were found to be different according to age, periods of physical activity, lifestyles, and medical histories.101,102 In teenagers, the correlation between physical activity and TL was only observed in female students.103 Moreover, there was no difference in TL and physical activity in people aged 20 to 30 years, but there was a difference in people who were over 42 years old. In particular, it has been reported that there was a difference according to the presence of obesity, illness, and smoking when the period of physical activity was over 10 years.101

The different effects of physical activity on telomere according to age

In studies where TL changes during long-term regular exercise were observed, many reported that TL was longer in the regular exercise group than in the non-exercise group (Table 3).23,104–106 However, TL according to long-term exercise varied according to age. In the 15-year-old group, there was no difference in TL between marathon runners and ordinary individuals107, and no difference in the young group (18–32 years). However, in the middle aged group (55–72 years) that exercised regularly, TL was reported to be 900 bp longer than that of the sedentary group. Thus, the study reported that exercise habits in the post-middle-age period were effective in preventing aging.18 However, after premenopausal women exercised three times a week for 6 months, and menopausal women aged 50 to 60 years exercised five times a week for 12 months (supervised exercise, three times a week), no difference between the exercise group and the non-exercise group was reported. Thus, the correlation between exercise and TL differs among women depending on exercise training periods and menopause.108,109

In a study of the relationship between cardiorespiratory fitness and TL, it was reported that the maximum oxygen uptake and TL were significantly correlated (Table 4).110,111 However, the positive correlation between cardiorespiratory fitness and TL also showed age-related differences such as a correlation with long-term regular exercise. There was no correlation between cardiorespiratory fitness and TL in the 15-year-old adolescent group106 or in the young (18–32 years) group.18,97 Differences were observed only in the middle-aged group (55–72 years).18 In a study of 582 elderly people aged 60 years and older, TL was reported to be longer in persons showing good performance in sitting and standing, and the TL decrease was reported to be less than 0.9 bp each year for every 1 second decrease in performance.112 In addition, a study correlating leg muscle strength and TL in adults over 50 years of age reported that telomere attrition was reduced by as much as 9% with every 50 N increase in leg strength113, with a possible explanation being that leg muscle strength and exercise performance ability are fitness factors that can be maintained or improved through regular physical activity and exercise, which affect cardiorespiratory fitness.

CONCLUSION

Go to

Telomerase maintains TL according to age. The activity of telomerase gradually decreases between 4 and 39 years of age and, after the age of 40, telomerase activity is not observed in 35% of the population.114 Furthermore, there is a more positive effect of regular physical activity in late middle age, when changes in TL are observed. In particular, considering that it was reported that past athletic experience does not affect TL after 10–20 years102, regular exercise at the time of telomere attrition could be an important precaution to prevent cell senescence.

Tables

Go to

The studies of the association between the TL and obesity

Author (year) Participant LTL measurement method Obesity marker Association
Lee et al. (2011)8 8–80 yr, Adults (n=309, 52% women) qPCR BMI, WC, HipC, %fat, VAT Negative
Njajou et al. (2012)9 70–79 yr, Adults (n=2,721, 51.6% women) qPCR %Body fat, SAT Negative
Bekaert et al. (2007)11 35–55 yr, Adults (n=2,509, 51.5% women) Southern blot for WBC TRF Body weight, BMI, WC No
Diaz et al. (2010)12 40–64 yr, Adults (n=317, 54.9% women) qPCR BMI, VAT No
Valdes et al. (2005)15 18–76 yr, Women (n=1,122) Southern blot for WBC TRF BMI Negative
Cherkas et al. (2008)16 18–81 yr, Twins (n=2,401, 89.6% women) Southern blot for WBC TRF BMI Negative
Nordfjäll et al. (2008)41 26–75 yr, Adults (n=989, 48.0% women) qPCR BMI, body weight, WC, HipC in women Negative
Moreno-Navarrete et al. (2010)42 31–61 yr, Obese women (n=21, waist 110–147cm) qPCR in adipocyte WC, adipocyte size with TL of adipocytes Negative
Monickaraj et al. (2012)43 34–56 yr, Obese, diabetic, and obese-diabetic subjects (n=59, 57.6% women) qPCR in SAT BMI Negative
Jones et al. (2014)44 >35 yr, Obese, diabetic, and obese-diabetic subjects (n=61) qPCR in SAT & VAT Adipose hypertrophy Negative
Kim et al. (2013)45 >60 yr, Women (n=129) qPCR BMI, WC Negative
Cui et al. (2013)46 40–70 yr, Women (n=2,912) qPCR Body weight, WC, HipC, BMI, WHtR WHR, height Negative or no
Al-Attas et al. (2010)47 5–12 yr, Children (n=148, 53.4% girls) qPCR WC in girls Negative
Fitzpatrick et al. (2007)48 74.2±5.2 yr (Mean±SD), adults (n=419) Southern blot for WBC TRF Body size, age ≤73 yr Negative or no
Gardner et al. (2005)49 21–43.5 yr, Adults (n=70, 57.1% women) Southern blot for WBC TRF BMI Negative
Farzaneh-Far et al. (2010)50 55–78 yr, CAD (n=608, 17.9% women) qPCR BMI No
Bischoff et al. (2006)51 79–101 yr, Elderly twins (n=812, 67.9% women) qPCR Obesity No
Oliveira et al. (2018)52 65–74 yr, Women (n=83) qPCR Body weight, BMI, WC No

TL, telomere length; LTL, leukocyte telomere length; qPCR, quantitative polymerase chain reaction; BMI, body mass index; WC, waist circumference; HipC, hip circumference; VAT, visceral adipose tissue; SAT, subcutaneous adipose tissue; WBC, white blood cell; TRF, terminal restriction fragment; WHtR, waist to height ratio; WHR, waist to hip ratio; SD, standard deviation; CAD, coronary artery disease.

Summary of the association between the TL and weight change

Author (year) Participant Intervention LTL measurement method Change of body weight Association
Njajou et al. (2012)9 70–79 yr, Adults (n=2,721, 51.6% women) 7-yr Follow-up qPCR BMI, %body fat loss Positive
Bekaert et al. (2007)11 35–55 yr, Adults (n=2,509, 51.5% women) Cohort study Southern blot for WBC TRF Fast weight gain since age of 18 yr Negative
Cui et al. (2013)46 40–70 yr, Women (n=2,912) Self-report (weight at enrollment, age 50) qPCR Loss (≥5%) Positive
Stable (≤5%) No
Gain (5%–15%) No
Gain (>15%) Negative
Carulli et al. (2016)53 31–52 yr, Obese subjects (n=37, 62.2% women) Bioenteric intragastric balloon qPCR Loss (−18.66 kg) Positive
O’Callaghan et al. (2009)54 55–80 yr, Adults (n=521, 55% women) Mediterranean diet (5 yr) qPCR Loss (−1.09 kg) Positive
BMI (−0.47 kg) Positive
WC (−1.15 cm) Positive
WHR (−0.008) Positive
Adiposity Positive
Latifovic et al. (2016)58 50–75 yr, Women (n=439) Diet/AE/diet+AE/CON (12 mon) qPCR Diet (−8.5%) No
AE (−2.4%)
Diet+AE (−10.8%)
CON (−0.8%)

TL, telomere length; LTL, leukocyte telomere length; qPCR, quantitative polymerase chain reaction; BMI, body mass index; WBC, white blood cell; TRF, terminal restriction fragment; WC, waist circumference; WHR, waist to hip ratio; Diet, diet group; AE, aerobic exercise group; CON, control.

Summary of the association between the TL and physical activity

Author (year) Subject LTL measurement method Intervention or factor Association
Physical activity & TL
 García-Calzón et al. (2014)10 47 yr, Men (n=782) Southern blot for WBC TRF Low/moderate/high PA
Moderate: walking, cycling, skiing, gardening, bowing, fishing, or other light Ex weekly		 Proportion of shorter TRF was lowest in the moderate PA
 Bekaert et al. (2007)11 35–55 yr, Adults (n=2,509, 51.5% women) Southern blot for WBC TRF PA (MET×time per wk) No association
 Cherkas et al. (2008)16 18–81 yr, Twin adults (n=2,401) Southern blot for WBC TRF Self-reported PA during the past 12 mon Positive
 Ludlow et al. (2008)17 50–70 yr, Adults (n=69, 50.7% women) qPCR in mononuclear cells Self-reported PA during the past month Longer LTL of PBMC in 991–3,540 kcal/wk shorter LTL of PBMC in 9,351 kcal/wk
 Latifovic et al. (2016)58 20–50 yr, Healthy adults (n=477, 57.2% women) qPCR Self-reported PA during the past 7 day Positive
 Edwards and Loprinzi (2016)97 >20 yr, Adults (n=1,868, 49.2% women) qPCR Self-reported PA during the past 30 day Positive
 Du et al. (2012)98 43–70 yr, Women (n=7,813) qPCR Self-reported PA during the past year Positive
 Song et al. (2010)100 18–80 yr, Healthy adults (n=80) qPCR in T-lymphocytes Self-reported PA No association LTL & PA
PA was negative associated with DNA damage.
 Saßenroth et al. (2015)101 >61 yr, Adults (n=814, 51.3% women) qPCR Self-reported PA during the last month
Longer period PA at least 10 yr		 Positive association in unadjusted
No association after adjustments such as CHD, medicine, BMI, and smoking etc.
PA was associated with longer LTL at over 42 yr
No association at 20–30 yr
 Laine et al. (2015)102 599 Men (392 former athletes & 207 CON) qPCR Cohort study (1985, 1995 or 2001) No difference in LTL in late life
 Zhu et al. (2011)103 667 Adolescents (14–18 yr, 51% girls) qPCR Vigorous PA Positive only in girls
TL in exercise experience & sedentary
 LaRocca et al. (2010)18 18–32 yr vs. 55–72 yr (n=57, 59.6% women) Southern blot for WBC TRF Endurance Ex-trained vs. SED VO2max Longer LTL in Ex vs. SED in older
No difference in young and adults
 Borghini et al. (2015)23 45.4 ±9.2 yr (Mean±SD), adults (n=62, 21% women) qPCR in saliva Athletes (n=20, 59.4 km/wk, 13.15 yr) LTL in athletics was longer than CON
 Silva et al. (2016)104 65–85 yr, Adults (n=61) Southern blot for PBMCs TRF Regular aerobic training for at least 5 yr Longer T-cell TL in the trained group vs. CON
 Østhus et al. (2012)105 66–77 yr, Men (n=20, 10 young, 22–27 yr; 10 older) qPCR in skeletal muscle Endurance athletes (EA, n=10, long distance & track running competitions) vs. moderate PA (MPA, n=10) Longer LRL in older EA vs. MPA
No difference of LRL in young EA vs. MPA
 Denham et al. (2013)106 >30 yr, Men (n=123) qPCR Ultra-marathon runner (n=67, 40–100 km/wk, ≥2 yr) Longer LTL in runners vs. CON
 Mathur et al. (2013)107 15 yr, Boys (n=32) qPCR in lymphocyte and granulocyte Marathon runner (n=17) vs. CON (n=15) No difference
 Shin et al. (2008)108 47 yr, Obese women (n=16) Southern blot for WBC TRF AE (3 day/wk, 60 min, 6 mon) No difference
 Friedenreich et al. (2018)109 50–60 yr, Postmenopausal women (n=212; 99 Ex vs. 113 CON) qPCR AE (5 day/wk, 12 mon) No difference

TL, telomere length; LTL, leukocyte telomere length; WBC, white blood cell; TRF, terminal restriction fragment; PA, physical activity; Ex, exercise group; MET, metabolic equivalent of task; qPCR, quantitative polymerase chain reaction; PBMC, peripheral blood mononuclear cell; CHD, chronic heart disease; BMI, body mass index; CON, control group; SED, sedentary; VO2max, maximum oxygen consumption; SD, standard deviation; EA, endurance athletes; LRL, long distance & track running competitions; MPA, moderate physical activity; AE, aerobic exercise.

Summary of the association between the TL and cardiorespiratory fitness

Author (year) Subject LTL measurement method Intervention or factor Association
LaRocca et al. (2010)18 18–32 yr vs. 55–72 yr (n=57, 59.6% women) Southern blot for WBC TRF Maximal Ex test (VO2max) LTL was positively associated with VO2max in older adults
Edwards and Loprinzi (2016)97 >20 yr, Adults (n=1,868, 49.2% women) qPCR Submaximal treadmill test (CRF) No association
Mathur et al. (2013)107 15 yr, Boys (n=32) Lymphocyte TL Maximal Ex test (VO2max) No association
Mason et al. (2013)110 50–75 yr, Postmenopausal women (n=439) qPCR Maximal Ex test (VO2max) LTL was positively associated with VO2max
Krauss et al. (2011)111 944 Adults with CVD (20% women) qPCR Maximal Ex test (CRF) High CRF (>7 METs) had two-fold longer LTL vs. low CRF
Soares-Miranda et al. (2015)112 73.5 yr, Adults (n=582, 62% women) Southern blot for WBC TRF 15-ft walk (sec), grip strength (kg), chair stands (sec) A better chair test performance in longer LTL
Changes chair time was associated with changes in LTL

TL, telomere length; LTL, leukocyte telomere length; WBC, white blood cell; TRF, terminal restriction fragment; Ex, exercise; VO2max, maximum oxygen consumption; qPCR, quantitative polymerase chain reaction; CRF, cardiorespiratory fitness; CVD, cardiovascular disease; METs, metabolic equivalent of task.

References

Go to
  1. Reilly JJ, Kelly J. Long-term impact of overweight and obesity in childhood and adolescence on morbidity and premature mortality in adulthood: systematic review. Int J Obes (Lond) 2011;35:891-8.
    Pubmed CrossRef
  2. Furukawa S, Fujita T, Shimabukuro M, Iwaki M, Yamada Y, Nakajima Y, et al. Increased oxidative stress in obesity and its impact on metabolic syndrome. J Clin Invest 2004;114:1752-61.
    Pubmed KoreaMed CrossRef
  3. Kurz DJ, Decary S, Hong Y, Trivier E, Akhmedov A, Erusalimsky JD. Chronic oxidative stress compromises telomere integrity and accelerates the onset of senescence in human endothelial cells. J Cell Sci 2004;117 Pt 11:2417-26.
    Pubmed CrossRef
  4. Moyzis RK, Buckingham JM, Cram LS, Dani M, Deaven LL, Jones MD, et al. A highly conserved repetitive DNA sequence, (TTAGGG)n, present at the telomeres of human chromosomes. Proc Natl Acad Sci U S A 1988;85:6622-6.
    Pubmed KoreaMed CrossRef
  5. Njajou OT, Cawthon RM, Damcott CM, Wu SH, Ott S, Garant MJ, et al. Telomere length is paternally inherited and is associated with parental lifespan. Proc Natl Acad Sci U S A 2007;104:12135-9.
    Pubmed KoreaMed CrossRef
  6. Minamino T, Orimo M, Shimizu I, Kunieda T, Yokoyama M, Ito T, et al. A crucial role for adipose tissue p53 in the regulation of insulin resistance. Nat Med 2009;15:1082-7.
    Pubmed CrossRef
  7. Müezzinler A, Zaineddin AK, Brenner H. Body mass index and leukocyte telomere length in adults: a systematic review and meta-analysis. Obes Rev 2014;15:192-201.
    Pubmed CrossRef
  8. Lee M, Martin H, Firpo MA, Demerath EW. Inverse association between adiposity and telomere length: The Fels Longitudinal Study. Am J Hum Biol 2011;23:100-6.
    KoreaMed CrossRef
  9. Njajou OT, Cawthon RM, Blackburn EH, Harris TB, Li R, Sanders JL, et al. Shorter telomeres are associated with obesity and weight gain in the elderly. Int J Obes (Lond) 2012;36:1176-9.
    Pubmed KoreaMed CrossRef
  10. García-Calzón S, Gea A, Razquin C, Corella D, Lamuela-Raventós RM, Martínez JA, et al. Longitudinal association of telomere length and obesity indices in an intervention study with a Mediterranean diet: the PREDIMED-NAVARRA trial. Int J Obes (Lond) 2014;38:177-82.
    Pubmed CrossRef
  11. Bekaert S, De Meyer T, Rietzschel ER, De Buyzere ML, De Bacquer D, Langlois M, et al. Telomere length and cardiovascular risk factors in a middle-aged population free of overt cardiovascular disease. Aging Cell 2007;6:639-47.
    Pubmed CrossRef
  12. Diaz VA, Mainous AG, Player MS, Everett CJ. Telomere length and adiposity in a racially diverse sample. Int J Obes (Lond) 2010;34:261-5.
    Pubmed CrossRef
  13. Epel ES, Blackburn EH, Lin J, Dhabhar FS, Adler NE, Morrow JD, et al. Accelerated telomere shortening in response to life stress. Proc Natl Acad Sci U S A 2004;101:17312-5.
    Pubmed KoreaMed CrossRef
  14. Demissie S, Levy D, Benjamin EJ, Cupples LA, Gardner JP, Herbert A, et al. Insulin resistance, oxidative stress, hypertension, and leukocyte telomere length in men from the Framingham Heart Study. Aging Cell 2006;5:325-30.
    Pubmed CrossRef
  15. Valdes AM, Andrew T, Gardner JP, Kimura M, Oelsner E, Cherkas LF, et al. Obesity, cigarette smoking, and telomere length in women. Lancet 2005;366:662-4.
    Pubmed CrossRef
  16. Cherkas LF, Hunkin JL, Kato BS, Richards JB, Gardner JP, Surdulescu GL, et al. The association between physical activity in leisure time and leukocyte telomere length. Arch Intern Med 2008;168:154-8.
    Pubmed CrossRef
  17. Ludlow AT, Zimmerman JB, Witkowski S, Hearn JW, Hatfield BD, Roth SM. Relationship between physical activity level, telomere length, and telomerase activity. Med Sci Sports Exerc 2008;40:1764-71.
    Pubmed KoreaMed CrossRef
  18. LaRocca TJ, Seals DR, Pierce GL. Leukocyte telomere length is preserved with aging in endurance exercise-trained adults and related to maximal aerobic capacity. Mech Ageing Dev 2010;131:165-7.
    Pubmed KoreaMed CrossRef
  19. Barbeau P, Johnson MH, Howe CA, Allison J, Davis CL, Gutin B, et al. Ten months of exercise improves general and visceral adiposity, bone, and fitness in black girls. Obesity (Silver Spring) 2007;15:2077-85.
    Pubmed CrossRef
  20. Davis C, Boyle CA, Gutin B. Dose-response effect of aerobic exercise training on insulin resistance in overweight children. Obesity 2007;15 Suppl:A19.
  21. Kojda G, Hambrecht R. Molecular mechanisms of vascular adaptations to exercise: physical activity as an effective antioxidant therapy?. Cardiovasc Res 2005;67:187-97.
    Pubmed CrossRef
  22. Tanaka T, Nakamura H, Yodoi J, Bloom ET. Redox regulation of the signaling pathways leading to eNOS phosphorylation. Free Radic Biol Med 2005;38:1231-42.
    Pubmed CrossRef
  23. Borghini A, Giardini G, Tonacci A, Mastorci F, Mercuri A, Mrakic-Sposta S, et al. Chronic and acute effects of endurance training on telomere length. Mutagenesis 2015;30:711-6.
    Pubmed CrossRef
  24. Avenell A, Brown TJ, McGee MA, Campbell MK, Grant AM, Broom J, et al. What interventions should we add to weight reducing diets in adults with obesity? A systematic review of randomized controlled trials of adding drug therapy, exercise, behaviour therapy or combinations of these interventions. J Hum Nutr Diet 2004;17:293-316.
    Pubmed CrossRef
  25. Curioni CC, Lourenço PM. Long-term weight loss after diet and exercise: a systematic review. Int J Obes (Lond) 2005;29:1168-74.
    Pubmed CrossRef
  26. Counter CM, Avilion AA, LeFeuvre CE, Stewart NG, Greider CW, Harley CB, et al. Telomere shortening associated with chromosome instability is arrested in immortal cells which express telomerase activity. EMBO J 1992;11:1921-9.
    Pubmed KoreaMed CrossRef
  27. Harley CB, Futcher AB, Greider CW. Telomeres shorten during ageing of human fibroblasts. Nature 1990;345:458-60.
    Pubmed CrossRef
  28. Hayflick L. The limited in vitro lifetime of human diploid cell strains. Exp Cell Res 1965;37:614-36.
    Pubmed CrossRef
  29. Blackburn EH. Structure and function of telomeres. Nature 1991;350:569-73.
    Pubmed CrossRef
  30. Wolkowitz OM, Mellon SH, Epel ES, Lin J, Dhabhar FS, Su Y, et al. Leukocyte telomere length in major depression: correlations with chronicity, inflammation and oxidative stress: preliminary findings. PLoS One 2011;6:e17837.
    Pubmed KoreaMed CrossRef
  31. Samani NJ, Boultby R, Butler R, Thompson JR, Goodall AH. Telomere shortening in atherosclerosis. Lancet 2001;358:472-3.
    Pubmed CrossRef
  32. Lusis AJ. Atherosclerosis. Nature 2000;407:233-41.
    Pubmed KoreaMed CrossRef
  33. Kim S, Parks CG, DeRoo LA, Chen H, Taylor JA, Cawthon RM, et al. Obesity and weight gain in adulthood and telomere length. Cancer Epidemiol Biomarkers Prev 2009;18:816-20.
    Pubmed KoreaMed CrossRef
  34. Hamet P, Thorin-Trescases N, Moreau P, Dumas P, Tea BS, deBlois D, et al. Workshop: excess growth and apoptosis: is hypertension a case of accelerated aging of cardiovascular cells?. Hypertension 2001;37 2 Pt 2:760-6.
    Pubmed CrossRef
  35. Nolan CJ, Damm P, Prentki M. Type 2 diabetes across generations: from pathophysiology to prevention and management. Lancet 2011;378:169-81.
    Pubmed CrossRef
  36. Obana N, Takagi S, Kinouchi Y, Tokita Y, Sekikawa A, Takahashi S, et al. Telomere shortening of peripheral blood mononuclear cells in coronary disease patients with metabolic disorders. Intern Med 2003;42:150-3.
    Pubmed CrossRef
  37. Epel ES. Psychological and metabolic stress: a recipe for accelerated cellular aging?. Hormones (Athens) 2009;8:7-22.
    Pubmed CrossRef
  38. Zee RY, Castonguay AJ, Barton NS, Germer S, Martin M. Mean leukocyte telomere length shortening and type 2 diabetes mellitus: a case-control study. Transl Res 2010;155:166-9.
    Pubmed CrossRef
  39. Blackburn EH. Telomeres and telomerase: their mechanisms of action and the effects of altering their functions. FEBS Lett 2005;579:859-62.
    Pubmed CrossRef
  40. Effros RB, Dagarag M, Spaulding C, Man J. The role of CD8+ T-cell replicative senescence in human aging. Immunol Rev 2005;205:147-57.
    Pubmed CrossRef
  41. Nordfjäll K, Eliasson M, Stegmayr B, Melander O, Nilsson P, Roos G. Telomere length is associated with obesity parameters but with a gender difference. Obesity (Silver Spring) 2008;16:2682-9.
    Pubmed CrossRef
  42. Moreno-Navarrete JM, Ortega F, Sabater M, Ricart W, Fernández-Real JM. Telomere length of subcutaneous adipose tissue cells is shorter in obese and formerly obese subjects. Int J Obes (Lond) 2010;34:1345-8.
    Pubmed CrossRef
  43. Monickaraj F, Gokulakrishnan K, Prabu P, Sathishkumar C, Anjana RM, Rajkumar JS, et al. Convergence of adipocyte hypertrophy, telomere shortening and hypoadiponectinemia in obese subjects and in patients with type 2 diabetes. Clin Biochem 2012;45:1432-8.
    Pubmed CrossRef
  44. Jones DA, Prior SL, Barry JD, Caplin S, Baxter JN, Stephens JW. Changes in markers of oxidative stress and DNA damage in human visceral adipose tissue from subjects with obesity and type 2 diabetes. Diabetes Res Clin Pract 2014;106:627-33.
    Pubmed CrossRef
  45. Kim JH, Kim HK, Ko JH, Bang H, Lee DC. The relationship between leukocyte mitochondrial DNA copy number and telomere length in community-dwelling elderly women. PLoS One 2013;8:e67227.
    Pubmed KoreaMed CrossRef
  46. Cui Y, Gao YT, Cai Q, Qu S, Cai H, Li HL, et al. Associations of leukocyte telomere length with body anthropometric indices and weight change in Chinese women. Obesity (Silver Spring) 2013;21:2582-8.
    Pubmed KoreaMed CrossRef
  47. Al-Attas OS, Al-Daghri N, Bamakhramah A, Shaun Sabico S, McTernan P, Huang TT. Telomere length in relation to insulin resistance, inflammation and obesity among Arab youth. Acta Paediatr 2010;99:896-9.
    Pubmed CrossRef
  48. Fitzpatrick AL, Kronmal RA, Gardner JP, Psaty BM, Jenny NS, Tracy RP, et al. Leukocyte telomere length and cardiovascular disease in the cardiovascular health study. Am J Epidemiol 2007;165:14-21.
    Pubmed CrossRef
  49. Gardner JP, Li S, Srinivasan SR, Chen W, Kimura M, Lu X, et al. Rise in insulin resistance is associated with escalated telomere attrition. Circulation 2005;111:2171-7.
    Pubmed CrossRef
  50. Farzaneh-Far R, Lin J, Epel E, Lapham K, Blackburn E, Whooley MA. Telomere length trajectory and its determinants in persons with coronary artery disease: longitudinal findings from the heart and soul study. PLoS One 2010;5:e8612.
    Pubmed KoreaMed CrossRef
  51. Bischoff C, Petersen HC, Graakjaer J, Andersen-Ranberg K, Vaupel JW, Bohr VA, et al. No association between telomere length and survival among the elderly and oldest old. Epidemiology 2006;17:190-4.
    Pubmed CrossRef
  52. Oliveira BS, Pirkle CM, Zunzunegui MV, Batistuzzo de Medeiros SR, Thomasini RL, Guerra RO. Leukocyte telomere length and chronic conditions in older women of northeast brazil: a cross-sectional study. Cells 2018;7:E193.
    Pubmed KoreaMed CrossRef
  53. Carulli L, Anzivino C, Baldelli E, Zenobii MF, Rocchi MB, Bertolotti M. Telomere length elongation after weight loss intervention in obese adults. Mol Genet Metab 2016;118:138-42.
    Pubmed CrossRef
  54. O’Callaghan NJ, Clifton PM, Noakes M, Fenech M. Weight loss in obese men is associated with increased telomere length and decreased abasic sites in rectal mucosa. Rejuvenation Res 2009;12:169-76.
    Pubmed CrossRef
  55. Zhang J, Rane G, Dai X, Shanmugam MK, Arfuso F, Samy RP, et al. Ageing and the telomere connection: an intimate relationship with inflammation. Ageing Res Rev 2016;25:55-69.
    Pubmed CrossRef
  56. von Zglinicki T. Oxidative stress shortens telomeres. Trends Biochem Sci 2002;27:339-44.
    Pubmed CrossRef
  57. Formichi C, Cantara S, Ciuoli C, Neri O, Chiofalo F, Selmi F, et al. Weight loss associated with bariatric surgery does not restore short telomere length of severe obese patients after 1 year. Obes Surg 2014;24:2089-93.
    Pubmed CrossRef
  58. Latifovic L, Peacock SD, Massey TE, King WD. The influence of alcohol consumption, cigarette smoking, and physical activity on leukocyte telomere length. Cancer Epidemiol Biomarkers Prev 2016;25:374-80.
    Pubmed CrossRef
  59. Lau DC, Douketis JD, Morrison KM, Hramiak IM, Sharma AM, Ur E, et al. 2006 Canadian clinical practice guidelines on the management and prevention of obesity in adults and children [summary]. CMAJ 2007;176:S1-13.
    Pubmed KoreaMed CrossRef
  60. Sironi AM, Gastaldelli A, Mari A, Ciociaro D, Positano V, Buzzigoli E, et al. Visceral fat in hypertension: influence on insulin resistance and beta-cell function. Hypertension 2004;44:127-33.
    Pubmed CrossRef
  61. Pálmai-Pallag T, Bachrati CZ. Inflammation-induced DNA damage and damage-induced inflammation: a vicious cycle. Microbes Infect 2014;16:822-32.
    Pubmed CrossRef
  62. Erol A. Systemic DNA damage response and metabolic syndrome as a premalignant state. Curr Mol Med 2010;10:321-34.
    Pubmed CrossRef
  63. Caldon CE. Estrogen signaling and the DNA damage response in hormone dependent breast cancers. Front Oncol 2014;4:106.
    Pubmed KoreaMed CrossRef
  64. Shimizu I, Yoshida Y, Suda M, Minamino T. DNA damage response and metabolic disease. Cell Metab 2014;20:967-77.
    Pubmed CrossRef
  65. Huth C, Pigeon É, Riou MÈ, St-Onge J, Arguin H, Couillard E, et al. Fitness, adiposopathy, and adiposity are independent predictors of insulin sensitivity in middle-aged men without diabetes. J Physiol Biochem 2016;72:435-44.
    Pubmed CrossRef
  66. Dusserre E, Moulin P, Vidal H. Differences in mRNA expression of the proteins secreted by the adipocytes in human subcutaneous and visceral adipose tissues. Biochim Biophys Acta 2000;1500:88-96.
    Pubmed CrossRef
  67. Ellulu MS, Khaza’ai H, Rahmat A, Patimah I, Abed Y. Obesity can predict and promote systemic inflammation in healthy adults. Int J Cardiol 2016;215:318-24.
    Pubmed CrossRef
  68. Das UN. Is obesity an inflammatory condition?. Nutrition 2001;17:953-66.
    Pubmed CrossRef
  69. Guarner V, Rubio-Ruiz ME. Low-grade systemic inflammation connects aging, metabolic syndrome and cardiovascular disease. Interdiscip Top Gerontol 2015;40:99-106.
    Pubmed CrossRef
  70. Marsland AL, McCaffery JM, Muldoon MF, Manuck SB. Systemic inflammation and the metabolic syndrome among middle-aged community volunteers. Metabolism 2010;59:1801-8.
    Pubmed KoreaMed CrossRef
  71. Eaton SB, Eaton SB. Physical inactivity, obesity, and type 2 diabetes: an evolutionary perspective. Res Q Exerc Sport 2017;88:1-8.
    Pubmed CrossRef
  72. Nunn AV, Guy GW, Brodie JS, Bell JD. Inflammatory modulation of exercise salience: using hormesis to return to a healthy lifestyle. Nutr Metab (Lond) 2010;7:87.
    Pubmed KoreaMed CrossRef
  73. Telford RD. Low physical activity and obesity: causes of chronic disease or simply predictors?. Med Sci Sports Exerc 2007;39:1233-40.
    Pubmed CrossRef
  74. Bullock VE, Griffiths P, Sherar LB, Clemes SA. Sitting time and obesity in a sample of adults from Europe and the USA. Ann Hum Biol 2017;44:230-6.
    Pubmed CrossRef
  75. Roda C, Charreire H, Feuillet T, Mackenbach JD, Compernolle S, Glonti K, et al. Lifestyle correlates of overweight in adults: a hierarchical approach (the SPOTLIGHT project). Int J Behav Nutr Phys Act 2016;13:114.
    Pubmed KoreaMed CrossRef
  76. Lakka TA, Laaksonen DE, Lakka HM, Männikkö N, Niskanen LK, Rauramaa R, et al. Sedentary lifestyle, poor cardiorespiratory fitness, and the metabolic syndrome. Med Sci Sports Exerc 2003;35:1279-86.
    Pubmed CrossRef
  77. Ostman C, Smart NA, Morcos D, Duller A, Ridley W, Jewiss D. The effect of exercise training on clinical outcomes in patients with the metabolic syndrome: a systematic review and meta-analysis. Cardiovasc Diabetol 2017;16:110.
    Pubmed KoreaMed CrossRef
  78. Hayashino Y, Jackson JL, Hirata T, Fukumori N, Nakamura F, Fukuhara S, et al. Effects of exercise on C-reactive protein, inflammatory cytokine and adipokine in patients with type 2 diabetes: a meta-analysis of randomized controlled trials. Metabolism 2014;63:431-40.
    Pubmed CrossRef
  79. Votruba SB, Horvitz MA, Schoeller DA. The role of exercise in the treatment of obesity. Nutrition 2000;16:179-88.
    Pubmed CrossRef
  80. Garrow JS, Summerbell CD. Meta-analysis: effect of exercise, with or without dieting, on the body composition of overweight subjects. Eur J Clin Nutr 1995;49:1-10.
    Pubmed
  81. Catenacci VA, Wyatt HR. The role of physical activity in producing and maintaining weight loss. Nat Clin Pract Endocrinol Metab 2007;3:518-29.
    Pubmed KoreaMed CrossRef
  82. Lee L, Kumar S, Leong LC. The impact of five-month basic military training on the body weight and body fat of 197 moderately to severely obese Singaporean males aged 17 to 19 years. Int J Obes Relat Metab Disord 1994;18:105-9.
    Pubmed
  83. Van Loan MD, Keim NL, Barbieri TF, Mayclin PL. The effects of endurance exercise with and without a reduction of energy intake on fat-free mass and the composition of fat-free mass in obese women. Eur J Clin Nutr 1994;48:408-15.
    Pubmed
  84. Keim NL, Barbieri TF, Van Loan MD, Anderson BL. Energy expenditure and physical performance in overweight women: response to training with and without caloric restriction. Metabolism 1990;39:651-8.
    Pubmed CrossRef
  85. Church TS, Earnest CP, Thompson AM, Priest EL, Rodarte RQ, Saunders T, et al. Exercise without weight loss does not reduce C-reactive protein: the INFLAME study. Med Sci Sports Exerc 2010;42:708-16.
    Pubmed KoreaMed CrossRef
  86. Kraus WE, Houmard JA, Duscha BD, Knetzger KJ, Wharton MB, McCartney JS, et al. Effects of the amount and intensity of exercise on plasma lipoproteins. N Engl J Med 2002;347:1483-92.
    Pubmed CrossRef
  87. Rosenkilde M, Auerbach P, Reichkendler MH, Ploug T, Stallknecht BM, Sjödin A. Body fat loss and compensatory mechanisms in response to different doses of aerobic exercise: a randomized controlled trial in overweight sedentary males. Am J Physiol Regul Integr Comp Physiol 2012;303:R571-9.
    Pubmed CrossRef
  88. Church TS, Martin CK, Thompson AM, Earnest CP, Mikus CR, Blair SN. Changes in weight, waist circumference and compensatory responses with different doses of exercise among sedentary, overweight postmenopausal women. PLoS One 2009;4:e4515.
    Pubmed KoreaMed CrossRef
  89. King NA, Hopkins M, Caudwell P, Stubbs RJ, Blundell JE. Individual variability following 12 weeks of supervised exercise: identification and characterization of compensation for exercise-induced weight loss. Int J Obes (Lond) 2008;32:177-84.
    Pubmed CrossRef
  90. Church TS, Earnest CP, Skinner JS, Blair SN. Effects of different doses of physical activity on cardiorespiratory fitness among sedentary, overweight or obese postmenopausal women with elevated blood pressure: a randomized controlled trial. JAMA 2007;297:2081-91.
    Pubmed CrossRef
  91. Johannsen NM, Swift DL, Lavie CJ, Earnest CP, Blair SN, Church TS. Categorical analysis of the impact of aerobic and resistance exercise training, alone and in combination, on cardiorespiratory fitness levels in patients with type 2 diabetes: results from the HART-D study. Diabetes Care 2013;36:3305-12.
    Pubmed KoreaMed CrossRef
  92. Pedersen BK, Saltin B. Exercise as medicine: evidence for prescribing exercise as therapy in 26 different chronic diseases. Scand J Med Sci Sports 2015;25 Suppl 3:1-72.
    Pubmed CrossRef
  93. Stewart KJ, Bacher AC, Turner K, Lim JG, Hees PS, Shapiro EP, et al. Exercise and risk factors associated with metabolic syndrome in older adults. Am J Prev Med 2005;28:9-18.
    Pubmed CrossRef
  94. You T, Arsenis NC, Disanzo BL, Lamonte MJ. Effects of exercise training on chronic inflammation in obesity: current evidence and potential mechanisms. Sports Med 2013;43:243-56.
    Pubmed CrossRef
  95. Kasapis C, Thompson PD. The effects of physical activity on serum C-reactive protein and inflammatory markers: a systematic review. J Am Coll Cardiol 2005;45:1563-9.
    Pubmed CrossRef
  96. Golbidi S, Frisbee JC, Laher I. Chronic stress impacts the cardiovascular system: animal models and clinical outcomes. Am J Physiol Heart Circ Physiol 2015;308:H1476-98.
    Pubmed CrossRef
  97. Edwards MK, Loprinzi PD. Sedentary behavior, physical activity and cardiorespiratory fitness on leukocyte telomere length. Health Promot Perspect 2016;7:22-7.
    Pubmed KoreaMed CrossRef
  98. Du M, Prescott J, Kraft P, Han J, Giovannucci E, Hankinson SE, et al. Physical activity, sedentary behavior, and leukocyte telomere length in women. Am J Epidemiol 2012;175:414-22.
    Pubmed KoreaMed CrossRef
  99. Savela S, Saijonmaa O, Strandberg TE, Koistinen P, Strandberg AY, Tilvis RS, et al. Physical activity in midlife and telomere length measured in old age. Exp Gerontol 2013;48:81-4.
    Pubmed CrossRef
  100. Song Z, von Figura G, Liu Y, Kraus JM, Torrice C, Dillon P, et al. Lifestyle impacts on the aging-associated expression of biomarkers of DNA damage and telomere dysfunction in human blood. Aging Cell 2010;9:607-15.
    Pubmed KoreaMed CrossRef
  101. Saßenroth D, Meyer A, Salewsky B, Kroh M, Norman K, Steinhagen-Thiessen E, et al. Sports and exercise at different ages and leukocyte telomere length in later life: data from the Berlin aging study II (BASE-II). PLoS One 2015;10:e0142131.
    Pubmed KoreaMed CrossRef
  102. Laine MK, Eriksson JG, Kujala UM, Raj R, Kaprio J, Bäckmand HM, et al. Effect of intensive exercise in early adult life on telomere length in later life in men. J Sports Sci Med 2015;14:239-45.
    Pubmed KoreaMed
  103. Zhu H, Wang X, Gutin B, Davis CL, Keeton D, Thomas J, et al. Leukocyte telomere length in healthy Caucasian and African-American adolescents: relationships with race, sex, adiposity, adipokines, and physical activity. J Pediatr 2011;158:215-20.
    Pubmed KoreaMed CrossRef
  104. Silva LC, de Araújo AL, Fernandes JR, Matias Mde S, Silva PR, Duarte AJ, et al. Moderate and intense exercise lifestyles attenuate the effects of aging on telomere length and the survival and composition of T cell subpopulations. Age (Dordr) 2016;38:24.
    Pubmed KoreaMed CrossRef
  105. Østhus IB, Sgura A, Berardinelli F, Alsnes IV, Brønstad E, Rehn T, et al. Telomere length and long-term endurance exercise: does exercise training affect biological age? A pilot study. PLoS One 2012;7:e52769.
    Pubmed KoreaMed CrossRef
  106. Denham J, Nelson CP, O’Brien BJ, Nankervis SA, Denniff M, Harvey JT, et al. Longer leukocyte telomeres are associated with ultra-endurance exercise independent of cardiovascular risk factors. PLoS One 2013;8:e69377.
    Pubmed KoreaMed CrossRef
  107. Mathur S, Ardestani A, Parker B, Cappizzi J, Polk D, Thompson PD. Telomere length and cardiorespiratory fitness in marathon runners. J Investig Med 2013;61:613-5.
    Pubmed CrossRef
  108. Shin YA, Lee JH, Song W, Jun TW. Exercise training improves the antioxidant enzyme activity with no changes of telomere length. Mech Ageing Dev 2008;129:254-60.
    Pubmed CrossRef
  109. Friedenreich CM, Wang Q, Ting NS, Brenner DR, Conroy SM, McIntyre JB, et al. Effect of a 12-month exercise intervention on leukocyte telomere length: results from the ALPHA Trial. Cancer Epidemiol 2018;56:67-74.
    Pubmed CrossRef
  110. Mason C, Risques RA, Xiao L, Duggan CR, Imayama I, Campbell KL, et al. Independent and combined effects of dietary weight loss and exercise on leukocyte telomere length in postmenopausal women. Obesity (Silver Spring) 2013;21:E549-54.
    Pubmed KoreaMed CrossRef
  111. Krauss J, Farzaneh-Far R, Puterman E, Na B, Lin J, Epel E, et al. Physical fitness and telomere length in patients with coronary heart disease: findings from the Heart and Soul Study. PLoS One 2011;6:e26983.
    Pubmed KoreaMed CrossRef
  112. Soares-Miranda L, Imamura F, Siscovick D, Jenny NS, Fitzpatrick AL, Mozaffarian D. Physical activity, physical fitness, and leukocyte telomere length: the cardiovascular health study. Med Sci Sports Exerc 2015;47:2525-34.
    Pubmed KoreaMed CrossRef
  113. Loprinzi PD, Loenneke JP. Lower extremity muscular strength and leukocyte telomere length: implications of muscular strength in attenuating age-related chronic disease. J Phys Act Health 2016;13:454-7.
    Pubmed CrossRef
  114. Iwama H, Ohyashiki K, Ohyashiki JH, Hayashi S, Yahata N, Ando K, et al. Telomeric length and telomerase activity vary with age in peripheral blood cells obtained from normal individuals. Hum Genet 1998;102:397-402.
    Pubmed CrossRef

Share this article on :

Related articles in Jomes

more