Effect of Physical Activity/Smoking/Sleep on Telomere Length: Comparison
View Latest Version
Please note this is a comparison between Version 2 by Yvaine Wei and Version 1 by Dolores Corella.

Aging is a risk factor for several pathologies, restricting one’s health span, and promoting chronic diseases (e.g., cardiovascular and neurodegenerative diseases), as well as cancer. Telomeres are regions of repetitive DNA located at chromosomal ends. Telomere length has been inversely associated with chronological age and has been considered, for a long time, a good biomarker of aging. Several lifestyle factors have been linked with telomere shortening or maintenance. 

  • aging
  • telomere length
  • physical activity
  • tobacco
  • smoking
  • sleep

1. Introduction

Aging is defined as a diminishing of biological functions over time, in which there is a progressive loss of the function and structure of tissues and systems [6,18][1][2]. The underlying mechanisms of the this process have been studied in depth and it seems they are related with genetic and epigenetic alterations, proteostasis loss, telomere shortening, autophagy deterioration, and mitochondrial dysfunction, among others [1,4,18,19][3][4][2][5]. However, the specific role of each mechanism remains unknown. Furthermore, these mechanisms may be modulated by other risk factors, such as diet, tobacco smoking, physical activity (PA), stress, or sleep, which, in turn, have been associated with certain diseases related to aging [18][2]. 
Currently, several biomarkers of biological aging have been developed. Telomeres are regions of repetitive sequences (TTAGGG)n and associated protective proteins located at the ends of the cap-shaped linear chromosomes that preserve the integrity and stability of chromosomes during DNA replication. They are essential to chromosome stability and protect genomic DNA through various mechanisms [20,21,22,23,24][6][7][8][9][10]. Usually, a relative quantification protocol by calculating the telomere/single copy gene ratio is undertaken.
The telomere is stabilized by a six-protein complex called “shelterin”, including the TRF (telomeric repeat binding factor)1, TRF2, POT1 (protection of telomeres 1), TINF2 (TERF1-interacting nuclear factor 2), RAP1 (repressor activator protein 1 and TPP1 (tripeptidyl peptidase 1) [21,22][7][8]. Telomeres are subject to shortening during each cell division as the DNA replication mechanism cannot copy the DNA in its entirely. The enzyme telomerase, however, can solve this problem by adding the repetitive sequences and maintaining telomere length (TL). Telomere shortening is one of the most frequently studied mechanisms in the aging process. Telomere attrition reflects the cumulative load of oxidative, inflammatory, and mechanical stress [18,25][2][11]. Hence, TL has been proposed as a biomarker of biological age and a risk factor for chronic diseases [4,18,25,26,27,28,29,30][4][2][11][12][13][14][15][16] and total mortality [22,25,28,29,31,32][8][11][14][15][17][18]. Nevertheless, the association between these outcomes and the TL marker are still under discussion due to inconsistent results [19,25,33,34,35,36,37,38,39,40][5][11][19][20][21][22][23][24][25][26]. One of the factors potentially contributing to the heterogeneous results is the measurement approach used to determine TL. This is an important issue given the fact that TL differs in leukocyte subtypes isolated from the same individual. Although blood leukocytes are the most commonly used samples to determine TL, it is known that TL may substantially vary across various tissue types. The terminal restriction fragment (TRF) approach is the oldest method for analyzing TL and remains the “gold standard” even in current studies. It uses the southern blot or in-gel hybridization with a specific proof for telomere DNA [17,18][27][2]. Other methods include the fluorescent in situ hybridization (FISH) by using digital microscopy (quantitative FISH as Q-FISH) and flow cytometry (Flow-FISH). Another method, telomere shortest length assay (TeSLA), measures the distribution of shortest telomeres in heterogeneous situations. It provides a better measurement of the shortest length of telomeres. However, the quantitative polymerase chain reaction (PCR) is most widely used for its high throughput. Despite the fast, highly sensitive nature of PCR approach, which requires low amounts of DNA, the distribution of long and short telomeres cannot be obtained, and it is not possible to evaluate TL of individual cells or chromosomes [17,18][27][2]. This method is often chosen for large cohort studies, using DNA from leukocytes. Additionally, telomerase activity, gene expression, or epigenetic regulation of telomere-related genes are analyzed to delve deeper on the mechanisms [20,21,24][6][7][10]. TL is determined by the interaction between endogenous and external factors that explain greater or lesser susceptibility to accelerated aging [22][8]. Therefore, the exposome could well play a fundamental role through various biological mechanisms in the maintenance of the telomeres during aging [41,42][28][29]. Several studies have analyzed the association between lifestyle and TL, both as a protective factor [16,43[30][31][32],44], and as inducer of their shortening [36,45,46][22][33][34]. Diet has been one of the most commonly studied lifestyle factors with regard to TL. Several studies have shown the benefit of consuming foods rich in antioxidants or the benefits of various diets, such as Mediterranean type diets, on telomere attrition, as witnessed in a number of the already published reviews [47,48,49,50,51,52][35][36][37][38][39][40]. 

2. Association between PA and TL

The impact of PA as a relevant factor in preventing diseases associated with aging was reported in several studies [53,54,55,56,57,58,59][41][42][43][44][45][46][47]. However, the underlying mechanism remains to be clarified. One of the possible mechanisms could be lower telomere attrition. To date, the optimum amount of PA and the type of exercise for maintaining TL remains under debate. 

An important consideration for intervention trials is the length of the intervention. Brandao et al. [95][48] observed that an 8-w intervention combining aerobic and strength training in sedentary women with obesity increased TL. However, it has been reported that different training modalities may exert different effects. Thus, Werner et al. [44][32] in a complex intervention showed that endurance and interval training increased TL, but not endurance training. In this study, telomerase activity was also measured and was positively correlated with TL. Similarly, Zietzer et al. [104][49] in an intervention study carried out in youth and elderly participants showed that in the youngest population, telomerase activity increased significantly in a single session of aerobic exercise [104][49]. When endurance athletes were compared with individuals with an average level of activity, a greater TL was observed compared with the control group.

3. Association between Telomere Length and Tobacco Smoking

Only 2 of the 21 cross-sectional studies report no association between tobacco smoking and TL [60,105][50][51]; in one additional study, the initial association between tobacco smoking and TL was non-significant after adjusting for BMI [120][52]. In another report [108][53], although smoking status was not associated with TL, there was an inverse association between the number of cigarettes smoked and TL. The initial investigation by the NHS, analyzing the association between smoking and TL in 2284 women, found no relationship between both variables [60][50]. Two years later, in 5862 women, that same study observed a slight association between TL and smoking, specifically 8% greater TL in subjects who had never smoked as opposed to smokers [117][54] The authors stated that the combined effect of various risk factors (diet, PA, weight, alcohol, and tobacco) was much greater than the individual additive effect [117][54]. Various authors have also found greater telomere shortening in smokers as opposed to non-smokers [119,121,122,123][55][56][57][58]. Tobacco possibly accounts for 0.64–1.23% of TL variation [116][59]. More specifically, there could exist 50 bp of variation between smokers and non-smokers [119][55], 73 bp [125][60], or 190 bp according to others [112][61].

4. Association between Telomere Length and Sleep

The influence of sleep quality and sleep disorders on aging and on physical and mental health has been recognized more recently [138,139][62][63]. In general, aging is associated with poor sleep. Sleep quantity and efficiency vary across the lifespan, sleep duration being shorter, and sleep efficiency being lower at older ages; these difficulties worsen after 60 years, and with some differences between men and women [139,140,141][63][64][65]. Sex-specific differences are complex and vary by outcome [140][64]. A recent review including 1.1 million people from the Netherlands, United Kingdom and United States, noted that women aged 41 years and older, despite self-reporting shorter sleep duration and lower sleep efficiency than men, had longer and more efficient sleep objectively measured by actigraphy [142][66], suggesting that the studies analyzing the association between sleep and TL should consider this heterogeneity. 

References

  1. Strait, J.B.; Lakatta, E.G. Aging-associated cardiovascular changes and their relationship to heart failure. Heart Fail. Clin. 2012, 8, 143–164.
  2. Zhang, W.; Song, M.; Qu, J.; Liu, G.H. Epigenetic Modifications in Cardiovascular Aging and Diseases. Circ. Res. 2018, 123, 773–786.
  3. Abdellatif, M.; Sedej, S.; Carmona-Gutierrez, D.; Madeo, F.; Kroemer, G. Autophagy in Cardiovascular Aging. Circ. Res. 2018, 123, 803–824.
  4. Paneni, F.; Diaz Canestro, C.; Libby, P.; Luscher, T.F.; Camici, G.G. The Aging Cardiovascular System: Understanding It at the Cellular and Clinical Levels. J. Am. Coll. Cardiol. 2017, 69, 1952–1967.
  5. Marian, A.J.; Bhatnagar, A.; Bolli, R.; Izpisua Belmonte, J.C. Introduction to Cardiovascular Aging Compendium. Circ. Res. 2018, 123, 737–739.
  6. Falus, A.; Marton, I.; Borbenyi, E.; Tahy, A.; Karadi, P.; Aradi, J.; Stauder, A.; Kopp, M. A challenging epigenetic message: Telomerase activity is associated with complex changes in lifestyle. Cell Biol. Int. 2011, 35, 1079–1083.
  7. Fouquerel, E.; Opresko, P.L. Convergence of The Nobel Fields of Telomere Biology and DNA Repair. Photochem. Photobiol. 2017, 93, 229–237.
  8. Martinez, P.; Blasco, M.A. Heart-Breaking Telomeres. Circ. Res. 2018, 123, 787–802.
  9. Munoz-Lorente, M.A.; Cano-Martin, A.C.; Blasco, M.A. Mice with hyper-long telomeres show less metabolic aging and longer lifespans. Nat. Commun. 2019, 10, 4723.
  10. Zhao, Z.; Pan, X.; Liu, L.; Liu, N. Telomere length maintenance, shortening, and lengthening. J. Cell Physiol. 2014, 229, 1323–1329.
  11. Bekaert, S.; De Meyer, T.; Rietzschel, E.R.; De Buyzere, M.L.; De Bacquer, D.; Langlois, M.; Segers, P.; Cooman, L.; Van Damme, P.; Cassiman, P.; et al. Telomere length and cardiovascular risk factors in a middle-aged population free of overt cardiovascular disease. Aging Cell 2007, 6, 639–647.
  12. Aviv, A. Genetics of leukocyte telomere length and its role in atherosclerosis. Mutat. Res. 2012, 730, 68–74.
  13. Denham, J.; O’Brien, B.J.; Prestes, P.R.; Brown, N.J.; Charchar, F.J. Increased expression of telomere-regulating genes in endurance athletes with long leukocyte telomeres. J. Appl. Physiol. 2016, 120, 148–158.
  14. Herrmann, M.; Pusceddu, I.; Marz, W.; Herrmann, W. Telomere biology and age-related diseases. Clin. Chem. Lab. Med. 2018, 56, 1210–1222.
  15. Mons, U.; Muezzinler, A.; Schottker, B.; Dieffenbach, A.K.; Butterbach, K.; Schick, M.; Peasey, A.; De Vivo, I.; Trichopoulou, A.; Boffetta, P.; et al. Leukocyte Telomere Length and All-Cause, Cardiovascular Disease, and Cancer Mortality: Results From Individual-Participant-Data Meta-Analysis of 2 Large Prospective Cohort Studies. Am. J. Epidemiol. 2017, 185, 1317–1326.
  16. Rizvi, S.; Raza, S.T.; Mahdi, F. Telomere length variations in aging and age-related diseases. Curr. Aging Sci. 2014, 7, 161–167.
  17. Goglin, S.E.; Farzaneh-Far, R.; Epel, E.S.; Lin, J.; Blackburn, E.H.; Whooley, M.A. Change in Leukocyte Telomere Length Predicts Mortality in Patients with Stable Coronary Heart Disease from the Heart and Soul Study. PLoS ONE 2016, 11, e0160748.
  18. Turner, K.J.; Vasu, V.; Griffin, D.K. Telomere Biology and Human Phenotype. Cells 2019, 8, 73.
  19. Brouilette, S.; Singh, R.K.; Thompson, J.R.; Goodall, A.H.; Samani, N.J. White cell telomere length and risk of premature myocardial infarction. Arterioscler. Thromb. Vasc. Biol. 2003, 23, 842–846.
  20. Brouilette, S.W.; Moore, J.S.; McMahon, A.D.; Thompson, J.R.; Ford, I.; Shepherd, J.; Packard, C.J.; Samani, N.J.; West of Scotland Coronary Prevention Study, G. Telomere length, risk of coronary heart disease, and statin treatment in the West of Scotland Primary Prevention Study: A nested case-control study. Lancet 2007, 369, 107–114.
  21. Carty, C.L.; Kooperberg, C.; Liu, J.; Herndon, M.; Assimes, T.; Hou, L.; Kroenke, C.H.; LaCroix, A.Z.; Kimura, M.; Aviv, A.; et al. Leukocyte Telomere Length and Risks of Incident Coronary Heart Disease and Mortality in a Racially Diverse Population of Postmenopausal Women. Arterioscler. Thromb. Vasc. Biol. 2015, 35, 2225–2231.
  22. De Meyer, T.; Nawrot, T.; Bekaert, S.; De Buyzere, M.L.; Rietzschel, E.R.; Andres, V. Telomere Length as Cardiovascular Aging Biomarker: JACC Review Topic of the Week. J. Am. Coll. Cardiol. 2018, 72, 805–813.
  23. Haycock, P.C.; Heydon, E.E.; Kaptoge, S.; Butterworth, A.S.; Thompson, A.; Willeit, P. Leucocyte telomere length and risk of cardiovascular disease: Systematic review and meta-analysis. BMJ 2014, 349, g4227.
  24. Okuda, K.; Khan, M.Y.; Skurnick, J.; Kimura, M.; Aviv, H.; Aviv, A. Telomere attrition of the human abdominal aorta: Relationships with age and atherosclerosis. Atherosclerosis 2000, 152, 391–398.
  25. Sharifi-Sanjani, M.; Oyster, N.M.; Tichy, E.D.; Bedi, K.C., Jr.; Harel, O.; Margulies, K.B.; Mourkioti, F. Cardiomyocyte-Specific Telomere Shortening is a Distinct Signature of Heart Failure in Humans. J. Am. Heart Assoc. 2017, 6, 25211.
  26. Willeit, P.; Willeit, J.; Brandstatter, A.; Ehrlenbach, S.; Mayr, A.; Gasperi, A.; Weger, S.; Oberhollenzer, F.; Reindl, M.; Kronenberg, F.; et al. Cellular aging reflected by leukocyte telomere length predicts advanced atherosclerosis and cardiovascular disease risk. Arterioscler. Thromb. Vasc. Biol. 2010, 30, 1649–1656.
  27. Pataky, M.W.; Young, W.F.; Nair, K.S. Hormonal and Metabolic Changes of Aging and the Influence of Lifestyle Modifications. Mayo Clin. Proc. 2021, 96, 788–814.
  28. Blackburn, E.H.; Epel, E.S.; Lin, J. Human telomere biology: A contributory and interactive factor in aging, disease risks, and protection. Science 2015, 350, 1193–1198.
  29. Opresko, P.L.; Shay, J.W. Telomere-associated aging disorders. Ageing Res. Rev. 2017, 33, 52–66.
  30. Freitas-Simoes, T.M.; Cofan, M.; Blasco, M.A.; Soberon, N.; Foronda, M.; Serra-Mir, M.; Roth, I.; Valls-Pedret, C.; Domenech, M.; Ponferrada-Ariza, E.; et al. Walnut Consumption for Two Years and Leukocyte Telomere Attrition in Mediterranean Elders: Results of a Randomized Controlled Trial. Nutrients 2018, 10, 1907.
  31. Liang, G.; Schernhammer, E.; Qi, L.; Gao, X.; De Vivo, I.; Han, J. Associations between rotating night shifts, sleep duration, and telomere length in women. PLoS ONE 2011, 6, e23462.
  32. Werner, C.M.; Hecksteden, A.; Morsch, A.; Zundler, J.; Wegmann, M.; Kratzsch, J.; Thiery, J.; Hohl, M.; Bittenbring, J.T.; Neumann, F.; et al. Differential effects of endurance, interval, and resistance training on telomerase activity and telomere length in a randomized, controlled study. Eur. Heart J. 2019, 40, 34–46.
  33. Ogawa, E.F.; Leveille, S.G.; Wright, J.A.; Shi, L.; Camhi, S.M.; You, T. Physical Activity Domains/Recommendations and Leukocyte Telomere Length in U.S. Adults. Med. Sci. Sports Exerc. 2017, 49, 1375–1382.
  34. Tucker, L.A. Physical activity and telomere length in U.S. men and women: An NHANES investigation. Prev. Med. 2017, 100, 145–151.
  35. Crous-Bou, M.; Molinuevo, J.L.; Sala-Vila, A. Plant-Rich Dietary Patterns, Plant Foods and Nutrients, and Telomere Length. Adv. Nutr. 2019, 10, S296–S303.
  36. Freitas-Simoes, T.M.; Ros, E.; Sala-Vila, A. Nutrients, foods, dietary patterns and telomere length: Update of epidemiological studies and randomized trials. Metabolism 2016, 65, 406–415.
  37. Galie, S.; Canudas, S.; Muralidharan, J.; Garcia-Gavilan, J.; Bullo, M.; Salas-Salvado, J. Impact of Nutrition on Telomere Health: Systematic Review of Observational Cohort Studies and Randomized Clinical Trials. Adv. Nutr. 2020, 11, 576–601.
  38. Marti, A.; Echeverria, R.; Morell-Azanza, L.; Ojeda-Rodriguez, A. Telomeres and diet quality. Nutr. Hosp. 2017, 34, 1226–1245.
  39. Perez, L.M.; Amaral, M.A.; Mundstock, E.; Barbe-Tuana, F.M.; Guma, F.; Jones, M.H.; Machado, D.C.; Sarria, E.E.; Marques, E.M.M.; Preto, L.T.; et al. Effects of Diet on Telomere Length: Systematic Review and Meta-Analysis. Public Health Genom. 2017, 20, 286–292.
  40. Rafie, N.; Golpour Hamedani, S.; Barak, F.; Safavi, S.M.; Miraghajani, M. Dietary patterns, food groups and telomere length: A systematic review of current studies. Eur. J. Clin. Nutr. 2017, 71, 151–158.
  41. Bray, N.W.; Pieruccini-Faria, F.; Bartha, R.; Doherty, T.J.; Nagamatsu, L.S.; Montero-Odasso, M. The effect of physical exercise on functional brain network connectivity in older adults with and without cognitive impairment. A systematic review. Mech. Ageing Dev. 2021, 196, 111493.
  42. Duggal, N.A.; Niemiro, G.; Harridge, S.D.R.; Simpson, R.J.; Lord, J.M. Can physical activity ameliorate immunosenescence and thereby reduce age-related multi-morbidity? Nat. Rev. Immunol. 2019, 19, 563–572.
  43. Harridge, S.D.; Lazarus, N.R. Physical Activity, Aging, and Physiological Function. Physiology 2017, 32, 152–161.
  44. Jakovljevic, D.G. Physical activity and cardiovascular aging: Physiological and molecular insights. Exp. Gerontol. 2018, 109, 67–74.
  45. Orkaby, A.R.; Forman, D.E. Physical activity and CVD in older adults: An expert’s perspective. Expert Rev. Cardiovasc. Ther. 2018, 16, 1–10.
  46. Rosique-Esteban, N.; Diaz-Lopez, A.; Martinez-Gonzalez, M.A.; Corella, D.; Goday, A.; Martinez, J.A.; Romaguera, D.; Vioque, J.; Aros, F.; Garcia-Rios, A.; et al. Leisure-time physical activity, sedentary behaviors, sleep, and cardiometabolic risk factors at baseline in the PREDIMED-PLUS intervention trial: A cross-sectional analysis. PLoS ONE 2017, 12, e0172253.
  47. Talar, K.; Hernandez-Belmonte, A.; Vetrovsky, T.; Steffl, M.; Kalamacka, E.; Courel-Ibanez, J. Benefits of Resistance Training in Early and Late Stages of Frailty and Sarcopenia: A Systematic Review and Meta-Analysis of Randomized Controlled Studies. J. Clin. Med. 2021, 10, 1630.
  48. Brandao, C.F.C.; Nonino, C.B.; de Carvalho, F.G.; Nicoletti, C.F.; Noronha, N.Y.; San Martin, R.; de Freitas, E.C.; Junqueira-Franco, M.V.M.; Marchini, J.S. The effects of short-term combined exercise training on telomere length in obese women: A prospective, interventional study. Sports Med. Open 2020, 6, 5.
  49. Zietzer, A.; Buschmann, E.E.; Janke, D.; Li, L.; Brix, M.; Meyborg, H.; Stawowy, P.; Jungk, C.; Buschmann, I.; Hillmeister, P. Acute physical exercise and long-term individual shear rate therapy increase telomerase activity in human peripheral blood mononuclear cells. Acta Physiol. 2017, 220, 251–262.
  50. Cassidy, A.; De Vivo, I.; Liu, Y.; Han, J.; Prescott, J.; Hunter, D.J.; Rimm, E.B. Associations between diet, lifestyle factors, and telomere length in women. Am. J. Clin. Nutr. 2010, 91, 1273–1280.
  51. Flannagan, K.S.; Jansen, E.C.; Rozek, L.S.; Rentschler, K.M.; Roman, A.V.; Ramirez-Zea, M.; Villamor, E.; Nine Mesoamerican Countries Metabolic Syndrome Study (NiMeCoMeS) Group. Sociodemographic correlates and family aggregation of leukocyte telomere length in adults and children from Mesoamerica. Am. J. Hum. Biol. 2017, 29, e22942.
  52. Yun, M.; Li, S.; Yan, Y.; Zhang, T.; Bazzano, L.; He, J.; Chen, W. Suppression effect of body weight on the association between cigarette smoking and telomere length: The Bogalusa Heart Study. Aging 2019, 11, 9893–9900.
  53. Khan, R.J.; Gebreab, S.Y.; Gaye, A.; Crespo, P.R.; Xu, R.; Davis, S.K. Associations of smoking indicators and cotinine levels with telomere length: National Health and Nutrition Examination Survey. Prev. Med. Rep. 2019, 15, 100895.
  54. Sun, Q.; Shi, L.; Prescott, J.; Chiuve, S.E.; Hu, F.B.; De Vivo, I.; Stampfer, M.J.; Franks, P.W.; Manson, J.E.; Rexrode, K.M. Healthy lifestyle and leukocyte telomere length in U.S. women. PLoS ONE 2012, 7, e38374.
  55. Wulaningsih, W.; Serrano, F.E.; Utarini, A.; Matsuguchi, T.; Watkins, J.; Network, P.R. Smoking, second-hand smoke exposure and smoking cessation in relation to leukocyte telomere length and mortality. Oncotarget 2016, 7, 60419–60431.
  56. Zhang, C.; Lauderdale, D.S.; Pierce, B.L. Sex-Specific and Time-Varying Associations between Cigarette Smoking and Telomere Length among Older Adults. Am. J. Epidemiol. 2016, 184, 922–932.
  57. Bendix, L.; Thinggaard, M.; Fenger, M.; Kolvraa, S.; Avlund, K.; Linneberg, A.; Osler, M. Longitudinal changes in leukocyte telomere length and mortality in humans. J. Gerontol. A Biol. Sci. Med. Sci. 2014, 69, 231–239.
  58. Chen, W.; Kimura, M.; Kim, S.; Cao, X.; Srinivasan, S.R.; Berenson, G.S.; Kark, J.D.; Aviv, A. Longitudinal versus cross-sectional evaluations of leukocyte telomere length dynamics: Age-dependent telomere shortening is the rule. J. Gerontol. A Biol. Sci. Med. Sci. 2011, 66, 312–319.
  59. Sulastri, D.; Lestari, Y.; Afriwardi; Desmawati. Relationship Between Body Composition and Smoking Habit with Telomere Length of Minangkabau Ethnicity Men, in West Sumatera, Indonesia. Pak. J. Biol. Sci. 2017, 20, 516–522.
  60. Muezzinler, A.; Mons, U.; Dieffenbach, A.K.; Butterbach, K.; Saum, K.U.; Schick, M.; Stammer, H.; Boukamp, P.; Holleczek, B.; Stegmaier, C.; et al. Smoking habits and leukocyte telomere length dynamics among older adults: Results from the ESTHER cohort. Exp. Gerontol. 2015, 70, 18–25.
  61. Nawrot, T.S.; Staessen, J.A.; Holvoet, P.; Struijker-Boudier, H.A.; Schiffers, P.; Van Bortel, L.M.; Fagard, R.H.; Gardner, J.P.; Kimura, M.; Aviv, A. Telomere length and its associations with oxidized-LDL, carotid artery distensibility and smoking. Front Biosci 2010, 2, 1164–1168.
  62. Sella, E.; Miola, L.; Toffalini, E.; Borella, E. The Relationship between Sleep Quality and Quality of Life in Aging: A Systematic Review and Meta-Analysis. Health Psychol. Rev. 2021, 1–23.
  63. Taillard, J.; Gronfier, C.; Bioulac, S.; Philip, P.; Sagaspe, P. Sleep in Normal Aging, Homeostatic and Circadian Regulation and Vulnerability to Sleep Deprivation. Brain Sci. 2021, 11, 1003.
  64. Carrier, J.; Semba, K.; Deurveilher, S.; Drogos, L.; Cyr-Cronier, J.; Lord, C.; Sekerovick, Z. Sex Differences in Age-Related Changes in the Sleep-Wake Cycle. Front. Neuroendocrinol. 2017, 47, 66–85.
  65. Evans, M.A.; Buysse, D.J.; Marsland, A.L.; Wright, A.G.C.; Foust, J.; Carroll, L.W.; Kohli, N.; Mehra, R.; Jasper, A.; Srinivasan, S.; et al. Meta-Analysis of Age and Actigraphy-Assessed Sleep Characteristics across the Lifespan. Sleep 2021, 44, zsab088.
  66. Kocevska, D.; Lysen, T.S.; Dotinga, A.; Koopman-Verhoeff, M.E.; Luijk, M.P.C.M.; Antypa, N.; Biermasz, N.R.; Blokstra, A.; Brug, J.; Burk, W.J.; et al. Sleep Characteristics across the Lifespan in 1.1 Million People from the Netherlands, United Kingdom and United States: A Systematic Review and Meta-Analysis. Nat. Hum. Behav. 2021, 5, 113–122.
More
© Text is available under the terms and conditions of the Creative Commons Attribution (CC BY) license (http://creativecommons.org/licenses/by/4.0/)
Video Production Service
Feedback