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Table 3 The effect of physical activity on telomere biology: observational studies

From: Physical Activity on Telomere Length as a Biomarker for Aging: A Systematic Review

References

Subjects

Telomere analysis: cell type

Measurement method

Physical activity

Main findings

Du et al. [76]

7,813 women (43–70 years) from Nurses’ Health Study (1988 to 1992)

TL: Leukocytes

qPCR

PA: Moderate- or vigorous-intensity, ≥ 3 MET hrs/week

Controls: sedentary lifestyle

TL: blood collected in 1989 to 1990

↑ Significant increased TL in greater moderate and vigorous intensity activity group (calisthenics or aerobics) versus sedentary group

Savela et al. [77]

204 men (now 76 years) from Helsinki Businessmen Study (1974)

TL: Leukocytes

Southern blot

LTPA: mainly sedentary, low-, moderate-, and high-LTPA, assessed at baseline and at 29 yr follow-up

TL: blood samples from a random sub-cohort of survivors at follow-up in 2003

↑ Significantly longer rTL in moderate LTPA group versus low- or high- PA groups

Significantly lower proportion of short telomeres in the moderate PA group versus low or high PA group

Denham et al. [63]

123 men, healthy

n = 67 ultra-marathon runners (44 ± 9 years)

n = 56 inactive (43 ± 9 years.)

TL: Leukocytes

qPCR

PA: Completion of 2-ultra marathons and average training distance of 40–100 km/week for a minimum of two years

Controls: inactive, healthy

↑ Significantly longer TL in ultra-marathon runners versus age-adjusted controls, biological age difference of 16.2 years

Weischer et al. [50]

4,576 men and woman

(20–100 years) from Copenhagen City Heart Study (1991 to 94)

TL: Leukocytes

qPCR

PA: ≥ 4 h/week of exercise, inactivity < 4 h/week, and other lifestyle factors, at baseline in 2001–2004 (control) and at 10-yr follow-up

TL: blood sampling in 1991 to 94 and at follow-up in 2001 to 03, TL grouped into quartiles

Significant association of shorter TL with physical inactivity (and with several other lifestyle factors) at baseline and at 10-yr follow-up

No significant association with TL change at baseline versus 10-yr follow-up

Laine et al. [120]

599 men (72 ± 6 years)

n = 392 former elite athletes (64 endurance, 221 mixed sport, and 107 power sport athletes)

n = 207 controls

TL: Leucocytes

qPCR

LTPA assessed for each former elite athlete group over past 3 months, MET-h/week calculated

Controls: PA not described

No significant difference in TL between each former elite athlete group and controls

No significant differences in TL amongst the different former elite athlete groups

Loprinzi et al. [80]

6,503 men and woman

(20–84 years) from NHANES (1999 to 2002)

TL: Leukocytes

qPCR

4 types of PA: moderate, vigorous intensity, transportation PA, and muscle-strengthening, for 30 days

MBB index: total number of participated PA types (0 to 4)

TL: from blood collected in 2001 to 2003, TL grouped into tertiles

↑ Significant association of longer TL in higher tertile TL group with higher MBB index

Dose–response relation between MBB and TL

No dose–response relation between TL and muscle-strengthening

Saßenroth et al. [70]

814 men and women (61–82 years) from Berlin Aging Study II

(n = 452 current PA, n = 223 currently inactive)

TL: Leukocytes

qPCR

Current PA: intensive PA, RT, Endurance, or other type of sport, with < 10 years physical inactivity

Controls: currently inactive, with ≥ 10 years physical inactivity

↑ Significantly longer rTL with current PA versus currently inactive group

↑ Significantly longer rTL with endurance PA and intensive PA group

↑ Significantly longer rTL with group of PA ≥ 10 years. versus inactive group

Latifovic et al. [71]

477 men and women

(20–50 years)

TL: Leukocytes

qPCR

Total amount of PA assessed by IPAQ, grouped into quartiles

TL: blood collected from in 2006 to 2008

↑ Significantly longer TL in highest quartile group versus lowest quartile group with vigorous activity

Loprinzi et al. [82]

6,474 men and women

(44 ± 0.31 years) from NHANES (1999 to 2002)

TL: Leukocytes

qPCR

9 types of MVPA: ≥ 2000 MVPA MET-min-month, for 30 days (basketball, bicycling, dance, running, stair climbing, swimming, walking, weight lifting)

TL: from blood collected in 2001 to 2003

↑ Significant association of longer TL only with running

Sillanpää et al. [81]

386 women, twins, elderly

(63–76 years) from the Finnish Twin Study on Aging (FITSA)

n = 186 monozygotic twins

n = 200 dizygotic twins

TL: Leukocytes

qPCR

PA level: modified Grimbsy scale (from inactivity to competitive sports weekly) at baseline, 3- and 11-yr follow-up

Fitness: maximum distance walked in 6 min, at baseline and at 3-yr follow-up (data missing at 11-yr follow-up)

TL: blood collected from 2000 to 2001

↑ Significantly longer TL with higher PA level (and not distance walked) at 3-yr follow-up versus baseline

Denham et al. [59]

122 men and women, healthy

(18–55 years)

n = 61 endurance athletes in cycling, triathlon, or middle-/long-distance

n = 61 controls

TL: Leukocytes

qPCR

Endurance athletes: competition at national/ international level

PA: at least 3 trainings/week, for ≥ 1 yr

Controls: recreationally active

↑ Significantly longer TL in endurance athletes (7.1%) and higher TERT expression (twofold) versus age-adjusted controls

Resting heart rate was an independent predictor for TL

Denham et al. [40]

84 men and women, healthy

n = 44 endurance athletes (32 ± 10 years.) in cycling, triathlon, or middle-/long-distance

n = 40 controls (30 ± 10 years.)

TL: PBMC, Leukocytes

qPCR

Endurance athletes: competition at national/ international level

PA: at least 3 trainings/week, for ≥ 1 yr

Controls: recreationally active

↑ Significantly longer TL in endurance athletes versus age-adjusted controls, biological age difference of 10.4 years

Dankel et al. [72]

4,881 men and woman (36–85 years) from NHANES study (1999 to 2002) and WATCH paradigm, placed into 6 groups (active or inactive; normal weight or overweight/obese; and normal weight or overweight/obese 10 years ago)

TL: Leukocytes

qPCR

PA: Sports-, exercise-, and recreational-related activities, ≥ 2000 MVPA MET-min-month over past 30 days

Control: active, normal weight for ≥ 10 years

TL: blood collected from 1989 to 1990

↑ Significant increased odds of longer TL with physical activity in all groups except if overweight/obese for ≥ 10 years versus multi-variate adjusted controls (age, gender, race/ ethnicity, CRP, and change in physical activity level)

↑ Significantly increased odds of shorter TL with inactivity in all groups

Edwards et al. [73]

1,868 men and women (20–49 years) from NHANES (1999 to 2002)

TL: Leukocytes

qPCR

PA: ≥ 1835 MVPA MET-min-month for 30 days

CRF: VO2 max of ≥ 39 mL/kg/min

Sedentary behaviour: ≥ 2 h/day of sitting for 30 days

TL: blood collected from 2001 to 2003

↑ Significant association of longest TL with greater physical activity, higher cardiorespiratory fitness and less sedentary behavior

Only MVPA was independently associated with longer TL

Ogawa et al. [99]

6,933 men and women

(20–84 years) from NHANES (1999 to 2002)

TL: Leukocytes

qPCR

3 groups of moderate PA: < 150 min/week, 150–300 min/week, and ≥ 300 min/week (or ≥ 150 min/week moderate to vigorous PA) for 30 days (household/yard work, transportation PA, moderate and vigorous LTPA)

TL: from blood collected in 2001 to 2003

↑ Significant association of longer TL with increment of 1 h/week of moderate PA, vigorous LTPA, or household/yard work

↑ Significant association of longer TL with moderate PA ≥ 300 min/week

Shadyab et al. [74]

1,476 African American and white women, postmenopausal

(50–79 years) from Women’s Health Initiative Study (2012–13) with follow-up in the Long Life Study (2012 to 2013)

TL: Leukocytes

Southern blot

PA: total amount, light, MVPA hr/week calculated via hip-worn accelerometer ≥ 10 h/day for 7 days

TL: blood collected from 2012 to 2013

↑ Significantly longer TL with ≥ 2.5 h/week MVPA group versus < 2.5 h/week MVPA group

Shadyab et al. [79]

1,476 African American and white women, postmenopausal

(50–79 years) from the Women’s Health Initiative Study (1974 to 1978) with follow-up in the Long Life Study (2012 to 2013)

TL: Leukocytes

Southern blot

LTPA: light, moderate, vigorous, with MET-h/week calculated based on total PA,

TL: blood collected from 2012 to 2013

↑ Significantly longer TL with higher MET-h/week of LTPA

↑ Significantly longer TL in ≧17 MET-h/week group versus < 1.25 MET-h/week group

Significant linear association of moderate to vigorous PA with TL; no association between light PA and TL

Associations of TL with PA did not vary by race/ethnicity

Fretts et al. [75]

2,312 American Indians (40 ± 16 years) from Strong Heart Family Study (2001 to 2003)

TL: Leukocytes

qPCR

PA: Steps/day via pedometer, with ≥ 3 days of recorded steps, grouped into quartiles

Control: lowest quartile of measured steps/day

TL: blood collected from 2001 to 2003

↑ Significant correlation between longer TL and greater number steps/day in all 3 upper quartile groups versus control group

Colon et al. [60]

14 men, healthy

n = 7 competitive triathletes (35.11 ± 5.86 years)

n = 7 recreationally active controls (34.14 ± 10.29 years.)

TL: Whole blood

qPCR

Competitive triathletes: competition at the national/ international level

Controls: recreationally active

↑ Significant association of longer TL in competitive triathletes versus controls

Aguiar et al. [61]

32 men, heathy

n = 21 master athletes (51.62 ± 8.19 years)

n = 11 recreationally active controls (45.41 ± 10.34 years)

TL: Leucocytes

qPCR

Master athletes: competition at the national/international level (in 100 m to marathon distance events)

Controls: recreationally active

↑ Significantly longer TL in master athletes versus controls

Stenbäck et al. [65]

700 men and woman

(68.9 ± 0.6 years) from City of Oulu Finland health survey follow-up (2013 to 2015)

TL: Whole blood

qPCR

PA: total steps calculated via wrist-worn accelerometer for 2 weeks, and questionnaire of PA intensity (light, moderate, or vigorous), PA history (at 15, 30, 50, and current age), and sedentary time, grouped into quartiles

TL: blood collected from 2013 to 2015

↑ Significant positive correlation of longer rTL with higher volume of steps in men, not in women

↑ Significantly longer rTL in the highest quartile moderate PA exercise versus lower three quartiles

Significantly longer rTL in women versus men at 69, but no differences at 68 and 70 years of age

No association between current rTL and PA in earlier years (age of 15, 30, 50)

Aström et al. [78]

1,035 men (n = 453) and women (n = 582) elderly, healthy (61 years at baseline) from the Helsinki Birth Cohort Study (2001 to 2004)

TL: Leucocytes

qPCR

PA: SFT (strength, flexibility, and endurance) at baseline in 2001–2004 (control) and at 10-years follow-up

TL: blood collected from 2001 to 2004 and from 2011 to 2013

↑ Significant association of longer TL with better physical performance in women at follow-up

Shorter TL and greater TL attrition associated with poorer physical performance in women at follow-up

Rosa et al. [95]

60 men, healthy

n = 31 athletes (18 endurance 53 ± 8 years, 13 sprinter 50 ± 9 years)

n = 29 controls (12 middle-aged 45.5 ± 10 years., 17 young 22.7 ± 4 years)

TL: Serum ADMA

ELISA

Athletes: ≥ 20 years continuous training, current competition at national and international level in endurance (10,000 m to marathon) and sprint (60 m to 400 m) events

Controls: inactive

TL control: blood sample from one young male

No difference in rTL between endurance athletes and sprinter athletes

↑ Significantly longer rTL in sprinter athletes versus middle-aged controls

Bastos et al. [96]

53 men, elderly, healthy

(66–75 years)

n = 23 low physical fitness

n = 7 moderate physical fitness

n = 23 high physical fitness

TL: T-cells

(CD4+, CD8+ CD28+)

MACS, FACS, Flow-FISH

PA: VO2 max as per ACSM

TL control: 1301 (human T-cell leukemia) cell line

↑ Significant association of longer TL in CD8+CD28+ cells of the moderate physical fitness group versus cell-line control

Hagman et al. [62]

140 healthy men

n = 35 young, elite football players (35 ± 0.5 years)

n = 35 elderly, football players (72 ± 0.5 years)

n = 35 young, untrained (35 ± 0.6 years)

n = 35 elderly, untrained (70 ± 0.7 years)

TL & Telomerase:

MNC

FISH, qPCR,

TRAP assay

PA of young footballers: ≥ 2nd Division in Denmark, ≥ 4 football sessions/week, and ≥ 10 years of regular football training

PA of elderly footballers: > 40 years of regular football training and still ≥ 1 football session/week

Controls: no regular physical exercise for ≥ 1 yr or no history of participation in sports at a high level earlier in life

↑ Significant increase in TL in the elderly football players group versus elderly untrained control group

↑ Significant Increase in telomerase activity and expression of telomere stabilizing proteins in young football players versus young untrained controls

Jantunen et al. [49]

1,014 men and women, elderly (56–69 years) from Helsinki Birth Cohort Study (2001 to 2004)

TL: Leukocytes

qPCR

LTPA assessed over past 12 months, MET-h/week calculated in 2001 to 2004 (baseline LTPA), grouped into quartiles

TL: baseline and 10 yr follow-up

rTL: blood collected from 2001 to 2004 and at follow-up from 2011 to 2013

No significant association of TL (at baseline and at follow-up) with LTPA at baseline

No significant association of rTL with LTPA at baseline for men

Significant inverse relationship in change in rTL with amount of LTPA at baseline in women

Nickels et al. [48]

107 men and women

(20 ± 5 years)

n = 51 swimmers (22 female, 29 male)

n = 56 controls (29 female, 27 male)

TL: Buccal cells

qPCR

Swimmers: competing at the national/international level

Controls: recreationally active, with ≥ 150 min/week moderate PA or ≥ 75 min/week of vigorous PA

↓ Significantly shorter TL in female swimmers versus female controls

No significant difference in TL between male swimmers and male controls

No correlation in TL between swimming performance, weekly training distance or competing level with TL