Abstract
Sarcopenia and frailty are associated with several important health-related adverse events, including disability, loss of independence, institutionalization and mortality. Sarcopenia can be considered a biological substrate of frailty, and the prevalence of both these conditions progressively increases with age. Telomeres are nucleoprotein structures located at the end of linear chromosomes and implicated in cellular ageing, shorten with age, and are associated with various age-related diseases. In addition, telomere length (TL) is widely considered a molecular/cellular hallmark of the ageing process. This narrative review summarizes the knowledge about telomeres and analyzes for the first time a possible association of TL with sarcopenia and frailty. The overview provided by the present review suggests that leukocyte TL as single measurement, calculated by quantitative real-time polymerase chain reaction (qRT-PCR), cannot be considered a meaningful biological marker for complex, multidimensional age-related conditions, such as sarcopenia and frailty. Panels of biomarkers, including TL, may provide more accurate assessment and prediction of outcomes in these geriatric syndromes in elderly people.
Similar content being viewed by others
References
Abdallah P, Luciano P, Runge KW, Lisby M, Géli V, Gilson E, Teixeira MT (2009) A two-step model for senescence triggered by a single critically short telomere. Nat Cell Biol 11:988–993. https://doi.org/10.1038/ncb1911
Allshire RC, Dempster M, Hastie ND (1989) Human telomeres contain at least three types of G-rich repeat distributed non-randomly. Nucleic Acids Res 17:4611–4627
Aubert G, Hills M, Lansdorp PM (2012) Telomere length measurement-caveats and a critical assessment of the available technologies and tools. Mutat Res 730:59–67. https://doi.org/10.1016/j.mrfmmm.2011.04.003
Aviv A (2002) Telomeres, sex, reactive oxygen species, and human cardiovascular aging. J Mol Med (Berl) 80:689–695
Aviv A, Shay J, Christensen K, Wright W (2005) The longevity gender gap: are telomeres the explanation? Sci Aging Knowl Environ 2005:pe16 (review)
Baerlocher GM, Vulto I, de Jong G, Lansdorp PM (2006) Flow cytometry and FISH to measure the average length of telomeres (flow FISH). Nat Protoc 1:2365–2376
Baird DM, Rowson J, Wynford-Thomas D, Kipling D (2003) Extensive allelic variation and ultrashort telomeres in senescent human cells. Nat Genet 33:203–207
Barberi L, Scicchitano BM, De Rossi M, Bigot A, Duguez S, Wielgosik A, Stewart C, McPhee J, Conte M, Narici M, Franceschi C, Mouly V, Butler-Browne G, Musarò A (2013) Age-dependent alteration in muscle regeneration: the critical role of tissue niche. Biogerontology 14:273–292. https://doi.org/10.1007/s10522-013-9429-4
Batsis JA, Mackenzie TA, Emeny RT, Rippberger P, Lopez-Jimenez F, Bartels S (2017) Sarcopenia, telomere length and mortality: NHANES 1999-2002. Innov Aging 1(1):204
Bayne S, Liu JP (2005) Hormones and growth factors regulate telomerase activity in ageing and cancer. Mol Cell Endocrinol 240:11–22
Bechet D, Tassa A, Taillandier D, Combaret L, Attaix D (2005) Lysosomal proteolysis in skeletal muscle. Int J Biochem Cell Biol 37:2098–2114
Bendix L, Horn PB, Jensen UB, Rubelj I, Kolvraa S (2010) The load of short telomeres, estimated by a new method, Universal STELA, correlates with number of senescent cells. Aging Cell 9:383–397
Blackburn EH (2001) Switching and signaling at the telomere. Cell 106:661–673
Blasco MA (2005) Telomeres and human disease: ageing, cancer and beyond. Nat Rev Genet 6:611–622
Blasco MA (2007) TL, stem cells and aging. Nat Chem Biol 3:640–649
Bodine SC, Latres E, Baumhueter S, Lai VK, Nunez L, Clarke BA, Poueymirou WT, Panaro FJ, Na E, Dharmarajan K, Pan ZQ, Valenzuela DM, DeChiara TM, Stitt TN, Yancopoulos GD, Glass DJ (2001) Identification of ubiquitin ligases required for skeletal muscle atrophy. Science 294:1704–1708
Bodnar AG, Ouellette M, Frolkis M, Holt SE, Chiu CP, Morin GB, Harley CB, Shay JW, Lichtsteiner S, Wright WE (1998) Extension of life-span by introduction of telomerase into normal human cells. Science 279:349–352
Borras M, Panizo S, Sarró F, Valdivielso JM, Fernandez E (2012) Assessment of the potential role of active vitamin D treatment in TL: a case-control study in hemodialysis patients. Clin Ther 34:849–856
Breitling LP, Saum KU, Perna L, Schöttker B, Holleczek B, Brenner H (2016) Frailty is associated with the epigenetic clock but not with TL in a German cohort. Clin Epigenetics 8:21. https://doi.org/10.1186/s13148-016-0186-5
Broer L, Codd V, Nyholt DR, Deelen J, Mangino M, Willemsen G, Albrecht E, Amin N, Beekman M, de Geus EJ, Henders A, Nelson CP, Steves CJ, Wright MJ, de Craen AJ, Isaacs A, Matthews M, Moayyeri A, Montgomery GW, Oostra BA, Vink JM, Spector TD, Slagboom PE, Martin NG, Samani NJ, van Duijn CM, Boomsma DI (2013) Meta-analysis of TL in 19,713 subjects reveals high heritability, stronger maternal inheritance and a paternal age effect. Eur J Hum Genet 21:1163–1168
Bürkle A, Moreno-Villanueva M, Bernhard J, Blasco M, Zondag G, Hoeijmakers JH, Toussaint O, Grubeck-Loebenstein B, Mocchegiani E, Collino S, Gonos ES, Sikora E, Gradinaru D, Dollé M, Salmon M, Kristensen P, Griffiths HR, Libert C, Grune T, Breusing N, Simm A, Franceschi C, Capri M, Talbot D, Caiafa P, Friguet B, Slagboom PE, Hervonen A, Hurme M, Aspinall R (2015) MARK-AGE biomarkers of ageing. Mech Ageing Dev 151:2–12. https://doi.org/10.1016/j.mad.2015.03.006
Calvani R, Marini F, Cesari M, Tosato M, Anker SD, von Haehling S, Miller RR, Bernabei R, Landi F, Marzetti E, the SPRINTT consortium (2015) Biomarkers for physical frailty and sarcopenia: state of the science and future developments. J Cachexia Sarcopenia Muscle 6:278–286
Calvani R, Marini F, Cesari M, Tosato M, Picca A, Anker SD, von Haehling S, Miller RR, Bernabei R, Landi F, Marzetti E, the SPRINTT consortium (2017) Biomarkers for physical frailty and sarcopenia. Aging Clin Exp Res 29(1):29–34. https://doi.org/10.1007/s40520-016-0708-1
Campisi J (2013) Aging, cellular senescence, and cancer. Annu Rev Physiol 75:685–705
Cassidy A, De Vivo I, Liu Y, Han J, Prescott J, Hunter DJ, Rimm EB (2010) Associations between diet, lifestyle factors, and TL in women. Am J Clin Nutr 91:1273–1280
Cawthon RM (2002) Telomere measurement by quantitative PCR. Nucleic Acids Res 30:e47
Cawthon RM (2009) Telomere length measurement by a novel monochrome multiplex quantitative PCR method. Nucleic Acids Res 37:e21
Cawthon RM, Smith KR, O’Brien E, Sivatchenko A, Kerber RA (2003) Association between TL in blood and mortality in people aged 60 years or older. Lancet 361:393–395
Cesari M, Landi F, Vellas B, Bernabei R, Marzetti E (2014) Sarcopenia and physical frailty: two sides of the same coin. Front Aging Neurosci 6:192. https://doi.org/10.3389/fnagi.2014.00192
Chakkalakal J, Brack A (2012) Extrinsic regulation of satellite cell function and muscle regeneration capacity during aging. J Stem Cell Res Ther Suppl 11:001
Chen LK, Liu LK, Woo J, Assantachai P, Auyeung TW, Bahyah KS, Chou MY, Chen LY, Hsu PS, Krairit O, Lee JS, Lee WJ, Lee Y, Liang CK, LimpawattanaP LC, Peng LN, Satake S, Suzuki T, Won CW, Wu CH, Wu SN, Zhang T, Zeng P, Akishita M, Arai H (2014) Sarcopenia in Asia: consensus report of the Asian Working Group for Sarcopenia. J Am Med Dir Assoc 15:95–101
Cherif H, Tarry JL, Ozanne SE, Hales CN (2003) Ageing and telomeres: a study into organ- and gender-specific telomere shortening. Nucleic Acids Res 31:1576–1583
Cherkas LF, Hunkin JL, Kato BS, Richards JB, Gardner JP, Surdulescu GL, Kimura M, Lu X, Spector TD, Aviv A (2008) The association between physical activity in leisure time and leukocyte telomere length. Arch Intern Med 168:154–158. https://doi.org/10.1001/archinternmed.2007.39
Collerton J, Barrass K, Bond J, Eccles M, Jagger C, James O, Martin-Ruiz C, Robinson L, von Zglinicki T, Kirkwood T (2007) The Newcastle 85 + study: biological, clinical and psychosocial factors associated with healthy ageing: study protocol. BMC Geriatr 7:14
Collerton J, Martin-Ruiz C, Davies K, Hilkens CM, Isaacs J, Kolenda C, Parker C, Dunn M, Catt M, Jagger C, von Zglinicki T, Kirkwood TB (2012) Frailty and the role of inflammation, immunosenescence and cellular ageing in the very old: cross-sectional findings from the Newcastle 85 + Study. Mech Ageing Dev 133:456–466
Collins K, Kobayashi R, Greider CW (1995) Purification of Tetrahymena telomerase and cloning of genes encoding the two protein components of the enzyme. Cell 81:677–686
Cruz-Jentoft AJ, Baeyens JP, Bauer JM, Boirie Y, Cederholm T, Landi F, Martin FC, Michel JP, Rolland Y, Schneider SM, Topinková E, Vandewoude M, Zamboni M; European Working Group on Sarcopenia in Older People (2010) Sarcopenia: European consensus on definition and diagnosis: Report of the European Working Group on Sarcopenia in Older People. Age Ageing 39:412–423
de Lange T (2005) Shelterin: the protein complex that shapes and safeguards human telomeres. Genes Dev 19:2100–2110
de Lange T (2010) How shelterin solves the telomere end-protection problem. Cold Spring Harb Symp Quant Biol 75:167–177
de Magalhães JP (2004) From cells to ageing: a review of models and mechanisms of cellular senescence and their impact on human ageing. Exp Cell Res 300:1–10
Decary S, Mouly V, Hamida CB, Sautet A, Barbet JP, Butler-Browne GS (1997) Replicative potential and telomere length in human skeletal muscle: implications for satellite cell-mediated gene therapy. Hum Gene Ther 8:1429–1438
Delmonico MJ, Harris TB, Visser M, Park SW, Conroy MB, Velasquez-Mieyer P, Boudreau R, Manini TM, Nevitt M, Newman AB, Goodpaster BH, Health, Aging, and Body (2009) Longitudinal study of muscle strength, quality, and adipose tissue infiltration. Am J ClinNutr 90:1579–1585
Demissie S, Levy D, Benjamin EJ, Cupples LA, Gardner JP, Herbert A, Kimura M, Larson MG, Meigs JB, Keaney JF, Aviv A (2006) Insulin resistance, oxidative stress, hypertension, and leukocyte TL in men from the Framingham Heart Study. Aging Cell 5:325–330
Dlouha D, Maluskova J, Kralova Lesna I, Lanska V, Hubacek JA (2014) Comparison of the relative telomere length measured in leukocytes and eleven different human tissues. Physiol Res 63(Suppl 3):S343–S350
Du J, Wang X, Miereles C, Bailey JL, Debigare R, Zheng B, Price SR, Mitch WE (2004) Activation of caspase-3 is an initial step triggering accelerated muscle proteolysis in catabolic conditions. J Clin Invest 113:115–123
Dupont-Versteegden EE (2006) Apoptosis in skeletal muscle and its relevance to atrophy. World J Gastroenterol 12:7463–7466
Farzaneh-Far R, Lin J, Epel ES, Harris WS, Blackburn EH, Whooley MA (2010) Association of marine omega-3 fatty acid levels with telomeric aging in patients with coronary heart disease. JAMA 303:250–257
Fielding RA, Vellas B, Evans WJ, Bhasin S, Morley JE, Newman AB, Abellan van Kan G, Andrieu S, Bauer J, Breuille D, Cederholm T, Chandler J, De Meynard C, Donini L, Harris T, Kannt A, Keime Guibert F, Onder G, Papanicolaou D, Rolland Y, Rooks D, Sieber C, Souhami E, Verlaan S, Zamboni M (2011) Sarcopenia: an undiagnosed condition in older adults. Current consensus definition: prevalence, etiology, and consequences. International working group on sarcopenia. J Am Med Dir Assoc 12:249–256
Finkel D, Whitfield K, McGue M (1995) Genetic and environmental influences on functional age: a twin study. J Gerontol B 50:P104–P113
Fossel M (2012) Use of TL as a biomarker for aging and age-related disease. Curr Transl Geriatr Exp Gerontol Rep 1:121–127
Fougère B, Vellas B, van Kan GA, Cesari M (2015) Identification of biological markers for better characterization of older subjects with physical frailty and sarcopenia. Transl Neurosci 6:103–110
Fried LP, Tangen CM, Walston J, Newman AB, Hirsch C, Gottdiener J, Seeman T, Tracy R, Kop WJ, Burke G, McBurnie MA; Cardiovascular Health Study Collaborative Research Group (2001) Frailty in older adults: evidence for a phenotype. J Gerontol A 56:M146–M156
Fried LP, Xue QL, Cappola AR, Ferrucci L, Chaves P, Varadhan R, Guralnik JM, Leng SX, Semba RD, Walston JD, Blaum CS, Bandeen-Roche K (2009) Nonlinear multisystem physiological dysregulation associated with frailty in older women: implications for etiology and treatment. J Gerontol A 64:1049–1057. https://doi.org/10.1093/gerona/glp076
Friedrich U, Griese E, Schwab M, Fritz P, Thon K, Klotz U (2000) Telomere length in different tissues of elderly patients. Mech Ageing Dev 119(3):89–99
Fyhrquist F, Saijonmaa O (2012) TL and cardiovascular aging. Ann Med 44:S138–S142
García-Prat L, Sousa-Victor P, Muñoz-Cánoves P (2013) Functional dysregulation of stem cells during ageing: a focus on skeletal muscle stem cells. FEBS J 280(17):4051–4062. https://doi.org/10.1111/febs.12221
Gardner JP, Kimura M, Chai W, Durrani JF, Tchakmakjian L, Cao X, Lu X, Li G, Peppas AP, Skurnick J, Wright WE, Shay JW, Aviv A (2007) Telomere dynamics in macaques and humans. J Gerontol A 62(4):367–374
Goggins WB, Woo J, Sham A, Ho SC (2005) Frailty index as a measure of biological age in a Chinese population. J Gerontol A 60:1046–1051
Griffith JD, Comeau L, Rosenfield S, Stansel RM, Bianchi A, Moss H, de Lange T (1999) Mammalian telomeres end in a large duplex loop. Cell 97:503–514
Hayflick L, Moorhead PS (1961) The serial cultivation of human diploid cell strains. Exp Cell Res 25:585–621
Hemann MT, Strong MA, Hao LY, Greider CW (2001) The shortest telomere, not average telomere length, is critical for cell viability and chromosome stability. Cell 107(1):67–77
Horvath S (2013) DNA methylation age of human tissues and cell types. Genome Biol 14(10):R115
Houben JM, Moonen HJ, van Schooten FJ, Hageman GJ (2008) TL assessment: biomarker of chronic oxidative stress? Free Radic Biol Med 44:235–246
Hubbard RE, O’Mahony MS, Calver BL, Woodhouse KW (2008) Nutrition, inflammation, and leptin levels in aging and frailty. J Am Geriatr Soc 56:279–284
Hubbard RE, O’Mahony MS, Savva GM, Calver BL, Woodhouse KW (2009) Inflammation and frailty measures in older people. J Cell Mol Med 13:3103–3109
Hunt SC, Chen W, Gardner JP, Kimura M, Srinivasan SR, Eckfeldt JH, Berenson GS, Aviv A (2008) Leukocyte telomeres are longer in African Americans than in whites: the National Heart, Lung, and Blood Institute Family Heart Study and the Bogalusa Heart Study. Aging Cell 7:451–458
Inglés M, Gambini J, Carnicero JA, García-García FJ, Rodríguez-Mañas L, Olaso-González G, Dromant M, Borrás C, Viña J (2014) Oxidative stress is related to frailty, not to age or sex, in a geriatric population: lipid and protein oxidation as biomarkers of frailty. J Am Geriatr Soc 62(7):1324–1328. https://doi.org/10.1111/jgs.12876
Jang YC, Sinha M, Cerletti M, Dall’Osso C, Wagers AJ (2011) Skeletal muscle stem cells: effects of ageing and metabolism on muscle regenerative function. Cold Spring Harb Symp Q Biol 76:101–111. https://doi.org/10.1101/sqb.2011.76.010652
Jaskelioff M, Muller FL, Paik JH, Thomas E, Jiang S, Adams AC, Sahin E, Kost-Alimova M, Protopopov A, Cadiñanos J, Horner JW, Maratos-Flier E, Depinho RA (2011) Telomerase reactivation reverses tissue degeneration in aged telomerase-deficient mice. Nature 469:102–106
Kadi F, Ponsot E (2010) The biology of satellite cells and telomeres in human skeletal muscle: effects of ageing and physical activity. Scand J Med Sci Sports 20(1):39–48. https://doi.org/10.1111/j.1600-0838.2009.00966.x
Kim NW, Piatyszek MA, Prowse KR, Harley CB, West MD, Ho PL, Coviello GM, Wright WE, Weinrich SL, Shay JW (1994) Specific association of human telomerase activity with immortal cells and cancer. Science 266:2011–2015
Kong CM, Lee XW, Wang X (2013) Telomere shortening in human diseases. FEBS J 280:3180–3193
Landi F, Calvani R, Cesari M, Tosato M, Martone AM, Bernabei R, Onder G, Marzetti E (2015) Sarcopenia as the Biological Substrate of Physical Frailty. Clin Geriatr Med 31:367–374
Liu JJ, Prescott J, Giovannucci E, Hankinson SE, Rosner B, Han J, De Vivo I (2013) Plasma vitamin D biomarkers and leukocyte TL. Am J Epidemiol 177:1411–1417
Ludlow AT, Zimmerman JB, Witkowski S, Hearn JW, Hatfield BD, Roth SM (2008) Relationship between physical activity level, telomere length, and telomerase activity. Med Sci Sports Exerc 40(10):1764–1771. https://doi.org/10.1249/MSS.0b013e31817c92aa
Ludlow AT, Witkowski S, Marshall MR, Wang J, Lima LC, Guth LM, Spangenburg EE, Roth SM (2012) Chronic exercise modifies age-related telomere dynamics in a tissue-specific fashion. J Gerontol A 67(9):911–926. https://doi.org/10.1093/gerona/gls002
Ludlow AT, Spangenburg EE, Chin ER, Cheng WH, Roth SM (2014) Telomeres shorten in response to oxidative stress in mouse skeletal muscle fibers. J Gerontol A 69(7):821–830. https://doi.org/10.1093/gerona/glt211
Markle-Reid M, Browne G (2003) Conceptualizations of frailty in relation to older adults. J Adv Nur 44:58–68
Martin-Ruiz CM, Gussekloo J, van Heemst D, von Zglinicki T, Westendorp RG (2005) TL in white blood cells is not associated with morbidity or mortality in the oldest old: a population-based study. Aging Cell 4:287–290
Marzetti E, Lees HA, Wohlgemuth SE, Leeuwenburgh C (2009) Sarcopenia of aging: underlying cellular mechanisms and protection by calorie restriction. BioFactors 35:28–35
Marzetti E, Calvani R, Bernabei R, Leeuwenburgh C (2012) Apoptosis in skeletal myocytes: a potential target for interventions against sarcopenia and physical frailty—a mini-review. Gerontology 58:99–106
Marzetti E, Calvani R, Cesari M, Buford TW, Lorenzi M, Behnke BJ, Leeuwenburgh C (2013) Mitochondrial dysfunction and sarcopenia of ageing: from signaling pathways to clinical trials. Int J Biochem Cell Biol 45(10):2288–2301. https://doi.org/10.1016/j.biocel.2013.06.024
Marzetti E, Lorenzi M, Antocicco M, Bonassi S, Celi M, Mastropaolo S, Settanni S, Valdiglesias V, Landi F, Bernabei R, Onder G (2014) Shorter telomeres in peripheral blood mononuclear cells from older persons with sarcopenia: results from an exploratory study. Front Aging Neurosci 6:233
McGrath M, Wong JY, Michaud D, Hunter DJ, De Vivo I (2007) TL, cigarette smoking, and bladder cancer risk in men and women. Cancer Epidemiol Biomark Prev 16:815–819
Meng S-J, Yu L-J (2010) Oxidative stress, molecular inflammation and sarcopenia. Int J Mol Sci 11(4):1509–1526. https://doi.org/10.3390/ijms11041509
Mitnitski AB, Mogilner AJ, Rockwood K (2001) Accumulation of deficits as a proxy measure of ageing. Sci World J 1:323–336
Mitnitski A, Collerton J, Martin-Ruiz C, Jagger C, von Zglinicki T, Rockwood K, Kirkwood TB (2015) Age-related frailty and its association with biological markers of ageing. BMC Med 13:161. https://doi.org/10.1186/s12916-015-0400-x
Morgan JE, Partridge TA (2003) Muscle satellite cells. Int J Biochem Cell Biol 35(8):1151–1156
Moyzis RK, Buckingham JM, Cram LS, Dani M, Deaven LL, Jones MD, Meyne J, Ratliff RL, Wu JR (1988) A highly conserved repetitive DNA sequence, (TTAGGG)n, present at the telomeres of human chromosomes. Proc Natl Acad Sci USA 85(18):6622–6626
Nandakumar J, Cech TR (2013) Finding the end: recruitment of telomerase to telomeres. Nat Rev Mol Cell Biol 14:69–82
Nikitina T, Woodcock CL (2004) Closed chromatin loops at the ends of chromosomes. J Cell Biol 166:161–165
O’Donovan A, Pantell MS, Puterman E, Dhabhar FS, Blackburn EH, Yaffe K, Cawthon RM, Opresko PL, Hsueh WC, Satterfield S, Newman AB, Ayonayon HN, Rubin SM, Harris TB, Epel ES (2011) Health Aging and Body Composition Study. Cumulative inflammatory load is associated with short leukocyte TL in the Health, Aging and Body Composition Study. PLoS ONE 6:e19687
Palm W, de Lange T (2008) How shelterin protects mammalian telomeres. Annu Rev Genet 42:301–334
Ponsot E, Lexell J, Kadi F (2008) Skeletal muscle telomere length is not impaired in healthy physically active old women and men. Muscle Nerve 37(4):467–472. https://doi.org/10.1002/mus.20964
Poon SS, Lansdorp PM (2001) Measurements of telomere length on individual chromosomes by image cytometry. Methods Cell Biol 64:69–96
Proctor CJ, Kirkwood TB (2002) Modelling telomere shortening and the role of oxidative stress. Mech Ageing Dev 123:351–363
Radak Z, Taylor AW, Sasvari M, Ohno H, Horkay B, Furesz J, Gaal D, Kanel T (2001) Telomerase activity is not altered by regular strenuous exercise in skeletal muscle or by sarcoma in liver of rats. Redox Rep 6(2):99–103
Reuter S, Gupta SC, Chaturvedi MM, Aggarwal BB (2010) Oxidative stress, inflammation, and cancer: how are they linked? Free Radic Biol Med 49:1603–1616
Richards JB, Valdes AM, Gardner JP, Paximadas D, Kimura M, Nessa A, Lu X, Surdulescu GL, Swaminathan R, Spector TD, Aviv A (2007) Higher serum vitamin D concentrations are associated with longer leukocyte TL in women. Am J Clin Nutr 86:1420–1425
Richter T, von Zglinicki T (2007) A continuous correlation between oxidative stress and telomere shortening in fibroblasts. Exp Gerontol 42:1039–1042
Rockwood K, Song X, MacKnight C, Bergman H, Hogan DB, McDowell I, Mitnitski A (2005) A global clinical measure of fitness and frailty in elderly people. CMAJ 173:489–495
Rodríguez-Mañas L, Féart C, Mann G, Viña J, Chatterji S, Chodzko-Zajko W, Gonzalez-ColaçoHarmand M, Bergman H, Carcaillon L, Nicholson C, Scuteri A, Sinclair A, Pelaez M, Van der Cammen T, Beland F, Bickenbach J, Delamarche P, Ferrucci L, Fried LP, Gutiérrez-Robledo LM, Rockwood K, Rodríguez Artalejo F, Serviddio G, Vega E (2013) Searching for an operational definition of frailty: a Delphi method based consensus statement: the frailty operative definition-consensus conference project. J Gerontol A 68:62–67
Samani NJ, Boultby R, Butler R, Thompson JR, Goodall AH (2001) Telomere shortening in atherosclerosis. Lancet 358:472–473
Sánchez-Flores M, Marcos-Pérez D, Costa S, Teixeira JP, Bonassi S, Pásaro E, Laffon B, Valdiglesias V (2017) Oxidative stress, genomic features and DNA repair in frail elderly: a systematic review. Ageing Res Rev 37:1–15. https://doi.org/10.1016/j.arr.2017.05.001
Saum KU, Dieffenbach AK, Müezzinler A, Müller H, Holleczek B, Stegmaier C, Butterbach K, Schick M, Canzian F, Stammer H, Boukamp P, Hauer K, Brenner H (2014) Frailty and TL: cross-sectional analysis in 3537 older adults from the ESTHER cohort. Exp Gerontol 58:250–255
Searle SD, Mitnitski A, Gahbauer EA, Gill TM, Rockwood K (2008) A standard procedure for creating a frailty index. BMC Geriatr 8:24
Shay JW, Bacchetti S (1997) A survey of telomerase activity in human cancer. Eur J Cancer 33:787–791
Shay JW, Zou Y, Hiyama E, Wright WE (2001) Telomerase and cancer. Hum Mol Genet 10:677–685
Shen J, Gammon MD, Terry MB, Wang Q, Bradshaw P, Teitelbaum SL, Neugut AI, Santella RM (2009) TL, oxidative damage, antioxidants and breast cancer risk. Int J Cancer 124:1637–1643
Smogorzewska A, van Steensel B, Bianchi A, Oelmann S, Schaefer MR, Schnapp G, de Lange T (2000) Control of human TL by TRF1 and TRF2. Mol Cell Biol 20:1659–1668
Sprott RL (2010) Biomarkers of aging and disease: introduction and definitions. Exp Gerontol 45:2–4
Valdes AM, Andrew T, Gardner JP, Kimura M, Oelsner E, Cherkas LF, Aviv A, Spector TD (2005) Obesity, cigarette smoking, and TL in women. Lancet 366:662–664
van der Harst P, van der Steege G, de Boer RA, Voors AA, Hall AS, Mulder MJ, van Gilst WH, van Veldhuisen DJ, MERIT-HF Study Group (2007) TL of circulating leukocytes is decreased in patients with chronic heart failure. J Am Coll Cardiol 49:1459–1464
Varela E, Blasco MA (2010) 2009 nobel prize in physiology or medicine: telomeres and telomerase. Oncogene 29:1561–1565
Visser M, Pahor M, Taaffe DR, Goodpaster BH, Simonsick EM, Newman AB, Nevitt M, Harris TB (2002) Relationship of interleukin-6 and tumor necrosis factor-alpha with muscle mass and muscle strength in elderly men and women: the Health ABC Study. J Gerontol A 57:M326–M332
von Zglinicki T (2000) Role of oxidative stress in TL regulation and replicative senescence. Ann N Y Acad Sci 908:99–110
Walston JD (2012) Sarcopenia in older adults. Curr Opin Rheumatol 24(6):623–627
Werner C, Fürster T, Widmann T, Pöss J, Roggia C, Hanhoun M, Scharhag J, Büchner N, Meyer T, Kindermann W, Haendeler J, Böhm M, Laufs U (2009) Physical exercise prevents cellular senescence in circulating leukocytes and in the vessel wall. Circulation 120:2438–2447
Wernig A, Schäfer R, Knauf U, Mundegar RR, Zweyer M, Högemeier O, Martens UM, Zimmermann S (2005) On the regenerative capacity of human skeletal muscle. Artif Organs 29(3):192–198
Wolkowitz OM, Mellon SH, Epel ES, Lin J, Dhabhar FS, Su Y, Reus VI, Rosser R, Burke HM, Kupferman E, Compagnone M, Nelson JC, Blackburn EH (2011) Leukocyte TL in major depression: correlations with chronicity, inflammation and oxidative stress–preliminary findings. PLoS ONE 6:e17837
Wong LS, Oeseburg H, de Boer RA, van Gilst WH, van Veldhuisen DJ, van der Harst P (2009) Telomere biology in cardiovascular disease: the TERC-/- mouse as a model for heart failure and ageing. Cardiovasc Res 81:244–252
Woo J, Tang NL, Suen E, Leung JC, Leung PC (2008) Telomeres and frailty. Mech Ageing Dev 129:642–648
Woo J, Yu R, Tang N, Leung J (2014) TL is associated with decline in grip strength in older persons aged 65 years and over. Age (Dordr) 36:9711
Wright WE, Piatyszek MA, Rainey WE, Byrd W, Shay JW (1996) Telomerase activity in human germline and embryonic tissues and cells. Dev Genet 18:173–179
Xi H, Li C, Ren F, Zhang H, Zhang L (2013) Telomere, aging and age-related diseases. Aging Clin Exp Res 25:139–146
Yu R, Tang N, Leung J, Woo J (2015) TL is not associated with frailty in older Chinese elderly: cross-sectional and longitudinal analysis. Mech Ageing Dev 152:74–79
Zhang L, Hu XZ, Li X, Li H, Smerin S, Russell D, Ursano RJ (2014) TL—a cellular aging marker for depression and post-traumatic stress disorder. Med Hypotheses 83:182–185
Zhao J, Miao K, Wang H, Ding H, Wang DW (2013) Association between TL and type 2 diabetes mellitus: a meta-analysis. PLoS ONE 8:e79993
Zhu H, Guo D, Li K, Pedersen-White J, Stallmann-Jorgensen IS, Huang Y, Parikh S, Liu K, Dong Y (2012) Increased telomerase activity and vitamin D supplementation in overweight African Americans. Int J Obes (Lond) 36:805–809
Acknowledgements
We thank “Centro Studi Achille e Linda Lorenzon” for supporting ML. We are grateful to Katie Palmer for the English language revision.
Funding
The work of ML has been supported by the “Centro Studi Achille e Linda Lorenzon”.
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Conflict of interest
The authors declare that they have no conflict of interest.
Rights and permissions
About this article
Cite this article
Lorenzi, M., Bonassi, S., Lorenzi, T. et al. A review of telomere length in sarcopenia and frailty. Biogerontology 19, 209–221 (2018). https://doi.org/10.1007/s10522-018-9749-5
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10522-018-9749-5