Telomere shortening is associated with poor physical performance in knee osteoarthritis

Manoy,Pacharee; Yuktanandana,Pongsak; Tanavalee,Aree; Tanpowpong,Thanathep; Ittipanichpong,Than; Honsawek,Sittisak

doi:10.3892/br.2020.1334

Telomere shortening is associated with poor physical performance in knee osteoarthritis

Authors:
- Pacharee Manoy
- Pongsak Yuktanandana
- Aree Tanavalee
- Thanathep Tanpowpong
- Than Ittipanichpong
- Sittisak Honsawek
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Affiliations: Unit of Excellence for Physical Fitness and Exercise, Department of Physical Therapy, School of Allied Health Sciences, University of Phayao, Phayao 56000, Thailand, Vinai Parkpian Orthopaedic Research Center, Department of Orthopaedics, Faculty of Medicine, Chulalongkorn University, King Chulalongkorn Memorial Hospital, Thai Red Cross Society, Bangkok 10330, Thailand
Published online on: July 22, 2020 https://doi.org/10.3892/br.2020.1334
Article Number: 27

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Abstract

Telomere length is a hallmark characteristic of ageing and age‑related diseases. Osteoarthritis (OA) is the most common cause of joint pain and physical disability in the elderly. Previous studies have revealed the role of telomere shortening in OA; however, the relationship between telomere length, muscle strength and physical performance in knee OA patients remains unknown. The aim of the present study was to investigate the association of telomere length and physical performance in patients with knee OA. A total of 202 patients with knee OA and 60 healthy controls were enrolled in the study. The quality of life was assessed using Western Ontario and McMaster Universities Osteoarthritis (WOMAC) index and Short Form Health Survey. The skeletal muscle mass was examined using bioelectrical impedance analysis, while the muscle strength was analyzed using hand grip force and isometric knee extension force. The physical performance of patients with knee OA was also investigated using gait speed, Timed up and go test (TUGT), Sit to stand test and 6‑min walk test (6MWT). Blood leukocyte relative telomere length (RTL) was assessed using real time quantitative PCR. The mean blood leukocyte RTL in knee OA subjects was significantly lower compared with healthy controls (P<0.001). Knee OA patients with RTL values in the lowest quartile had a slow gait speed (P=0.006) and prolonged TUGT time (P=0.03). Multivariate regression analyses and multiple logistic regression analyses adjusted for age, sex, waist circumference, body mass index, fat mass, skeletal muscle index and the total WOMAC demonstrated that gait speed, TUGT and 6MWT were associated with longer RTL (P‑trend<0.05). These findings suggested that poorer physical performance was associated with shorter RTL. Therefore, leukocyte telomere length and physical performance tests, especially gait speed, TUGT and 6MWT, could predict the health status and quality of life in patients with knee OA.

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1	Manoy P, Anomasiri W, Yuktanandana P, Tanavalee A, Mabey T and Honsawek S: Relationship of serum leptin and 25-hydroxyvitamin D in knee osteoarthritis patients. Chula Med J. 62:1037–1047. 2018.
2	Zhan D and Honsawek S: Reduction of leukocyte mitochondrial DNA copy number in knee osteoarthritis. Chula Med J. 63:207–209. 2019.PubMed/NCBI View Article : Google Scholar
3	Litwic A, Edwards MH, Dennison EM and Cooper C: Epidemiology and burden of osteoarthritis. Br Med Bull. 105:185–199. 2013.PubMed/NCBI View Article : Google Scholar
4	Kuszel L, Trzeciak T, Richter M and Czarny-Ratajczak M: Osteoarthritis and telomere shortening. J Appl Genet. 56:169–176. 2015.PubMed/NCBI View Article : Google Scholar
5	Mather KA, Jorm AF, Parslow RA and Christensen H: Is telomere length a biomarker of aging? A review. J Gerontol A Biol Sci Med Sci. 66:202–213. 2011.PubMed/NCBI View Article : Google Scholar
6	Xi H, Li C, Ren F, Zhang H and Zhang L: Telomere, aging and age-related diseases. Aging Clin Exp Res. 25:139–146. 2013.PubMed/NCBI View Article : Google Scholar
7	Li D, Yuan Q and Wang W: The role of telomeres in musculoskeletal diseases. J Int Med Res. 40:1242–1250. 2012.PubMed/NCBI View Article : Google Scholar
8	Fossel M: Use of telomere length as a biomarker for aging and age-related disease. Curr Transl Geriatrics Exp Gerontology Rep. 1:121–127. 2012. View Article : Google Scholar
9	Soares-Miranda L, Imamura F, Siscovick D, Jenny NS, Fitzpatrick AL and Mozaffarian D: Physical activity, physical fitness, and leukocyte telomere length: The cardiovascular health study. Med Sci Sports Exerc. 47:2525–2534. 2015.PubMed/NCBI View Article : Google Scholar
10	Loprinzi PD: Cardiorespiratory capacity and leukocyte telomere length among adults in the United States. Am J Epidemiol. 182:198–201. 2015.PubMed/NCBI View Article : Google Scholar
11	Tamayo M, Mosquera A, Rego I, Blanco FJ, Gosálvez J and Fernández JL: Decreased length of telomeric DNA sequences and increased numerical chromosome aberrations in human osteoarthritic chondrocytes. Mutat Res. 708:50–58. 2011.PubMed/NCBI View Article : Google Scholar
12	McAlindon T, Roberts M, Driban J, Schaefer L, Haugen IK, Smith SE, Duryea J, Cunha D, Blanco F, Fernández-Garcia JL and Eaton C: Incident hand OA is strongly associated with reduced peripheral blood leukocyte telomere length. Osteoarthritis Cartilage. 26:1651–1657. 2018. View Article : Google Scholar
13	Altman R, Asch E, Bloch D, Bole G, Borenstein D, Brandt K, Christy W, Cooke TD, Greenwald R and Hochberg M: Development of criteria for the classification and reporting of osteoarthritis. Classification of osteoarthritis of the knee. Diagnostic and therapeutic criteria committee of the American rheumatism association. Arthritis Rheum. 29:1039–1049. 1986.PubMed/NCBI View Article : Google Scholar
14	Spector TD and Cooper C: Radiographic assessment of osteoarthritis in population studies: Whither kellgren and lawrence? Osteoarthritis Cartilage. 1:203–206. 1993.PubMed/NCBI View Article : Google Scholar
15	Teerawattanapong N, Udomsinprasert W, Ngarmukos S, Tanavalee A and Honsawek S: Blood leukocyte LINE-1 hypomethylation and oxidative stress in knee osteoarthritis. Heliyon. 5(e01774)2019. View Article : Google Scholar
16	Sakthong P, Kasemsup V and Winit-Watjana W: Assessment of health-related quality of life in thai patients after heart surgery. Asian Biomed. 9:203–210. 2015. View Article : Google Scholar
17	Udomsinprasert W, Poovorawan Y, Chongsrisawat V, Vejchapipat P, Zhan D and Honsawek S: Telomere length in peripheral blood leukocytes is associated with severity of biliary atresia. PLoS One. 10(e0134689)2015. View Article : Google Scholar
18	Livak KJ and Schmittgen TD: Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) method. Methods. 25:402–408. 2001.PubMed/NCBI View Article : Google Scholar
19	Poonpet T, Saetan N, Tanavalee A, Wilairatana V, Yuktanandana P and Honsawek S: Association between leukocyte telomere length and angiogenic cytokines in knee osteoarthritis. Int J Rheum Dis. 21:118–125. 2018.PubMed/NCBI View Article : Google Scholar
20	Colbert CJ, Song J, Dunlop D, Chmiel JS, Hayes KW, Cahue S, Moisio KC, Chang AH and Sharma L: Knee confidence as it relates to physical function outcome in persons with or at high risk of knee osteoarthritis in the osteoarthritis initiative. Arthritis Rheum. 64:1437–1446. 2012.PubMed/NCBI View Article : Google Scholar
21	Schober P, Boer C and Schwarte LA: Correlation coefficients: Appropriate use and interpretation. Anesth Analg. 126:1763–1768. 2018.PubMed/NCBI View Article : Google Scholar
22	Shammas MA: Telomeres, lifestyle, cancer, and aging. Curr Opin Clin Nutr Metab Care. 14:28–34. 2011.PubMed/NCBI View Article : Google Scholar
23	Ding C, Jones G, Wluka AE and Cicuttini F: What can we learn about osteoarthritis by studying a healthy person against a person with early onset of disease? Curr Opin Rheumatol. 22:520–527. 2010.PubMed/NCBI View Article : Google Scholar
24	Fragkiadaki P, Nikitovic D, Kalliantasi K, Sarandi E, Thanasoula M, Stivaktakis PD, Nepka C, Spandidos DA, Tosounidis T and Tsatsakis A: Telomere length and telomerase activity in osteoporosis and osteoarthritis. Exp Ther Med. 19:1626–1632. 2020.PubMed/NCBI View Article : Google Scholar
25	Tamayo M, Mosquera A, Rego JI, Fernández-Sueiro JL, Blanco FJ and Fernandez JL: Differing patterns of peripheral blood leukocyte telomere length in rheumatologic diseases. Mutat Res. 683:68–73. 2010.PubMed/NCBI View Article : Google Scholar
26	Lee JY, Bang HW, Ko JH, Kim JH and Lee DC: Leukocyte telomere length is independently associated with gait speed in elderly women. Maturitas. 75:165–169. 2013.PubMed/NCBI View Article : Google Scholar
27	Sassenroth D, Meyer A, Salewsky B, Kroh M, Norman K, Steinhagen-Thiessen E and Demuth I: Sports and exercise at different ages and leukocyte telomere length in later life-data from the Berlin aging study II (BASE-II). PLoS One. 10(e0142131)2015.PubMed/NCBI View Article : Google Scholar
28	Cherkas LF, Hunkin JL, Kato BS, Richards JB, Gardner JP, Surdulescu GL, Kimura M, Lu X, Spector TD and Aviv A: The association between physical activity in leisure time and leukocyte telomere length. Arch Intern Med. 168:154–158. 2008.PubMed/NCBI View Article : Google Scholar
29	Bekaert S, Van Pottelbergh I, De Meyer T, Zmierczak H, Kaufman JM, Van Oostveldt P and Goemaere S: Telomere length versus hormonal and bone mineral status in healthy elderly men. Mech Ageing Dev. 126:1115–1122. 2005. View Article : Google Scholar
30	Harris SE, Deary IJ, MacIntyre A, Lamb KJ, Radhakrishnan K, Starr JM, Whalley LJ and Shiels PG: The association between telomere length, physical health, cognitive ageing, and mortality in non-demented older people. Neurosci Lett. 406:260–264. 2006. View Article : Google Scholar
31	Mather KA, Jorm AF, Milburn PJ, Tan X, Easteal S and Christensen H: No associations between telomere length and age-sensitive indicators of physical function in mid and later life. J Gerontol A Biol Sci Med Sci. 65:792–799. 2010.PubMed/NCBI View Article : Google Scholar
32	Woo J, Yu R, Tang N and Leung J: Telomere length is associated with decline in grip strength in older persons aged 65 years and over. Age (Dordr). 36(9711)2014.PubMed/NCBI View Article : Google Scholar
33	Marzetti E, Lorenzi M, Antocicco M, Bonassi S, Celi M, Mastropaolo S, Settanni S, Valdiglesias V, Landi F, Bernabei R and Onder G: Shorter telomeres in peripheral blood mononuclear cells from older persons with sarcopenia: Results from an exploratory study. Front Aging Neurosci. 6(233)2014.PubMed/NCBI View Article : Google Scholar
34	Singh A, Kukreti R, Saso L and Kukreti S: Oxidative stress: Role and response of short guanine tracts at genomic locations. Int J Mol Sci. 20(4258)2019. View Article : Google Scholar
35	Fouquerel E, Lormand J, Bose A, Lee HT, Kim GS, Li J, Sobol R, Freudenthal BD, Myong S and Opresko PL: Oxidative guanine base damage regulates human telomerase activity. Nat Struct Mol Biol. 23:1092–1100. 2016.PubMed/NCBI View Article : Google Scholar
36	Brandl A, Hartmann A, Bechmann V, Graf B, Nerlich M and Angele P: Oxidative stress induces senescence in chondrocytes. J Orthop Res. 29:1114–1120. 2011.PubMed/NCBI View Article : Google Scholar
37	Yudoh K, van Nguyen T, Nakamura H, Hongo-Masuko K, Kato T and Nishioka K: Potential involvement of oxidative stress in cartilage senescence and development of osteoarthritis: Oxidative stress induces chondrocyte telomere instability and downregulation of chondrocyte function. Arthritis Res Ther. 7(R380-R391)2005.PubMed/NCBI View Article : Google Scholar
38	Martin JA, Brown TD, Heiner AD and Buckwalter JA: Chondrocyte senescence, joint loading and osteoarthritis. Clin Orthop Relat Res. (427 Suppl)(S96-S103)2004.PubMed/NCBI View Article : Google Scholar
39	Martin JA, Brown T, Heiner A and Buckwalter JA: Post-traumatic osteoarthritis: The role of accelerated chondrocyte senescence. Biorheology. 41:479–491. 2004.PubMed/NCBI