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Erschienen in: Zeitschrift für Rheumatologie 2/2018

19.09.2016 | Originalie

Association between shortened telomere length and rheumatoid arthritis

A meta-analysis

verfasst von: Y. H. Lee, MD, PhD, S.-C. Bae

Erschienen in: Zeitschrift für Rheumatologie | Ausgabe 2/2018

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Abstract

Objective

This study aimed to evaluate the relationship between telomere length and rheumatoid arthritis (RA).

Methods

We performed a meta-analysis of studies comparing the telomere length in RA patients and healthy controls, and conducted subgroup analysis based on ethnicity, age-matched status, study quality, sample type, assay method, subject number, and shared epitope (SE) status.

Results

Nine studies from seven articles, with 388 RA patients and 362 controls, were included. Meta-analysis showed that the telomere length was significantly shorter in all individuals of the RA group than in those of the control group (SMD = −0.833, 95 % CI = −1.332 to −0.334, p = 0.001). Stratification by ethnicity showed significantly shortened telomere lengths in both mixed and age-matched Caucasian populations with RA (SMD = −1.415, 95 % CI = −1.709 to −1.120, p < 1.0 × 10−8; SMD = −0.658, 95 % CI = −1.187 to −0.0.128, p = 0.015). The telomere length was significantly shorter in the RA group than in the age-matched control group; however, this was not the case in the RA group that was not age-matched (SMD = −1.070, 95 % CI = −1.489 to −0.650, p = 5.7 × 10−7; SMD = 0.155, 95 % CI = −0.119 to 0.429, p = 0.267). Stratification by SE status revealed a significantly shortened telomere length in the SE-positive group, but not in the SE-negative group (SMD = −1.033, 95 % CI = −1.398 to −0.768, p < 1.0 × 10−8; SMD = −0.967, 95 % CI = −2.382 to 0.449, p = 0.181). In addition, the telomere length was significantly shorter in the SE-positive RA group than in the SE-negative RA group (SMD = −0.415, 95 % CI = −0.699 to −0.131, p = 0.004).

Conclusions

Our meta-analysis demonstrated that the telomere length was significantly shorter in patients with RA, and was significantly more so in the SE-positive group than in the SE-negative group.
Literatur
1.
Zurück zum Zitat Harris ED Jr. (1990) Rheumatoid arthritis. Pathophysiology and implications for therapy. N Engl J Med 322(18):1277–1289CrossRefPubMed Harris ED Jr. (1990) Rheumatoid arthritis. Pathophysiology and implications for therapy. N Engl J Med 322(18):1277–1289CrossRefPubMed
2.
Zurück zum Zitat Choi SJ, Rho YH, Ji JD, Song GG, Lee YH (2006) Genome scan meta-analysis of rheumatoid arthritis. Rheumatology (Oxford) 45(2):166–170CrossRef Choi SJ, Rho YH, Ji JD, Song GG, Lee YH (2006) Genome scan meta-analysis of rheumatoid arthritis. Rheumatology (Oxford) 45(2):166–170CrossRef
4.
5.
Zurück zum Zitat Collado M, Blasco MA, Serrano M (2007) Cellular senescence in cancer and aging. Cell 130(2):223–233CrossRefPubMed Collado M, Blasco MA, Serrano M (2007) Cellular senescence in cancer and aging. Cell 130(2):223–233CrossRefPubMed
6.
Zurück zum Zitat Correia-Melo C, Hewitt G, Passos JF (2014) Telomeres, oxidative stress and inflammatory factors: partners in cellular senescence? Longev Healthspan 3(1):1CrossRefPubMedPubMedCentral Correia-Melo C, Hewitt G, Passos JF (2014) Telomeres, oxidative stress and inflammatory factors: partners in cellular senescence? Longev Healthspan 3(1):1CrossRefPubMedPubMedCentral
7.
Zurück zum Zitat Schonland SO, Lopez C, Widmann T, Zimmer J, Bryl E, Goronzy JJ et al (2003) Premature telomeric loss in rheumatoid arthritis is genetically determined and involves both myeloid and lymphoid cell lineages. Proc Natl Acad Sci U S A 100(23):13471–13476CrossRefPubMedPubMedCentral Schonland SO, Lopez C, Widmann T, Zimmer J, Bryl E, Goronzy JJ et al (2003) Premature telomeric loss in rheumatoid arthritis is genetically determined and involves both myeloid and lymphoid cell lineages. Proc Natl Acad Sci U S A 100(23):13471–13476CrossRefPubMedPubMedCentral
8.
Zurück zum Zitat Blinova EA, Zinnatova EV, Barkovskaya M, Borisov VI, Sizikov AE, Kozhevnikov VS et al (2016) Telomere length of individual chromosomes in patients with rheumatoid arthritis. Bull Exp Biol Med 160(6):779–782CrossRefPubMed Blinova EA, Zinnatova EV, Barkovskaya M, Borisov VI, Sizikov AE, Kozhevnikov VS et al (2016) Telomere length of individual chromosomes in patients with rheumatoid arthritis. Bull Exp Biol Med 160(6):779–782CrossRefPubMed
9.
Zurück zum Zitat Antoniou KM, Margaritopoulos GA, Proklou A, Karagiannis K, Lasithiotaki I, Soufla G et al (2012) Investigation of telomerase/telomeres system in bone marrow mesenchymal stem cells derived from IPF and RA-UIP. J Inflamm (Lond) 9(1):27CrossRef Antoniou KM, Margaritopoulos GA, Proklou A, Karagiannis K, Lasithiotaki I, Soufla G et al (2012) Investigation of telomerase/telomeres system in bone marrow mesenchymal stem cells derived from IPF and RA-UIP. J Inflamm (Lond) 9(1):27CrossRef
10.
Zurück zum Zitat Tamayo M, Mosquera A, Rego JI, Fernandez-Sueiro JL, Blanco FJ, Fernandez JL (2010) Differing patterns of peripheral blood leukocyte telomere length in rheumatologic diseases. Mutat Res 683(1–2):68–73CrossRefPubMed Tamayo M, Mosquera A, Rego JI, Fernandez-Sueiro JL, Blanco FJ, Fernandez JL (2010) Differing patterns of peripheral blood leukocyte telomere length in rheumatologic diseases. Mutat Res 683(1–2):68–73CrossRefPubMed
11.
Zurück zum Zitat Colmegna I, Diaz-Borjon A, Fujii H, Schaefer L, Goronzy JJ, Weyand CM (2008) Defective proliferative capacity and accelerated telomeric loss of hematopoietic progenitor cells in rheumatoid arthritis. Arthritis Rheum 58(4):990–1000CrossRefPubMedPubMedCentral Colmegna I, Diaz-Borjon A, Fujii H, Schaefer L, Goronzy JJ, Weyand CM (2008) Defective proliferative capacity and accelerated telomeric loss of hematopoietic progenitor cells in rheumatoid arthritis. Arthritis Rheum 58(4):990–1000CrossRefPubMedPubMedCentral
12.
Zurück zum Zitat Koetz K, Bryl E, Spickschen K, O’Fallon WM, Goronzy JJ, Weyand CM (2000) T cell homeostasis in patients with rheumatoid arthritis. Proc Natl Acad Sci U S A 97(16):9203–9208CrossRefPubMedPubMedCentral Koetz K, Bryl E, Spickschen K, O’Fallon WM, Goronzy JJ, Weyand CM (2000) T cell homeostasis in patients with rheumatoid arthritis. Proc Natl Acad Sci U S A 97(16):9203–9208CrossRefPubMedPubMedCentral
13.
Zurück zum Zitat Steer SE, Williams FM, Kato B, Gardner JP, Norman PJ, Hall MA et al (2007) Reduced telomere length in rheumatoid arthritis is independent of disease activity and duration. Ann Rheum Dis 66(4):476–480CrossRefPubMed Steer SE, Williams FM, Kato B, Gardner JP, Norman PJ, Hall MA et al (2007) Reduced telomere length in rheumatoid arthritis is independent of disease activity and duration. Ann Rheum Dis 66(4):476–480CrossRefPubMed
14.
Zurück zum Zitat Costenbader KH, Prescott J, Zee RY, De Vivo I (2011) Immunosenescence and rheumatoid arthritis: does telomere shortening predict impending disease? Autoimmun Rev 10(9):569–573CrossRefPubMedPubMedCentral Costenbader KH, Prescott J, Zee RY, De Vivo I (2011) Immunosenescence and rheumatoid arthritis: does telomere shortening predict impending disease? Autoimmun Rev 10(9):569–573CrossRefPubMedPubMedCentral
15.
Zurück zum Zitat Prelog M (2006) Aging of the immune system: a risk factor for autoimmunity? Autoimmun Rev 5(2):136–139CrossRefPubMed Prelog M (2006) Aging of the immune system: a risk factor for autoimmunity? Autoimmun Rev 5(2):136–139CrossRefPubMed
16.
Zurück zum Zitat Hoffecker BM, Raffield LM, Kamen DL, Nowling TK (2013) Systemic lupus erythematosus and vitamin D deficiency are associated with shorter telomere length among African Americans: a case-control study. PLOS ONE 8(5):e63725CrossRefPubMedPubMedCentral Hoffecker BM, Raffield LM, Kamen DL, Nowling TK (2013) Systemic lupus erythematosus and vitamin D deficiency are associated with shorter telomere length among African Americans: a case-control study. PLOS ONE 8(5):e63725CrossRefPubMedPubMedCentral
17.
Zurück zum Zitat Haque S, Rakieh C, Marriage F, Ho P, Gorodkin R, Teh LS et al (2013) Shortened telomere length in patients with systemic lupus erythematosus. Arthritis Rheum 65(5):1319–1323CrossRefPubMed Haque S, Rakieh C, Marriage F, Ho P, Gorodkin R, Teh LS et al (2013) Shortened telomere length in patients with systemic lupus erythematosus. Arthritis Rheum 65(5):1319–1323CrossRefPubMed
18.
Zurück zum Zitat Skamra C, Romero-Diaz J, Sandhu A, Huang Q, Lee J, Pearce W et al (2013) Telomere length in patients with systemic lupus erythematosus and its associations with carotid plaque. Rheumatology (Oxford) 52(6):1101–1108CrossRef Skamra C, Romero-Diaz J, Sandhu A, Huang Q, Lee J, Pearce W et al (2013) Telomere length in patients with systemic lupus erythematosus and its associations with carotid plaque. Rheumatology (Oxford) 52(6):1101–1108CrossRef
19.
Zurück zum Zitat Beier F, Balabanov S, Amberger CC, Hartmann U, Manger K, Dietz K et al (2007) Telomere length analysis in monocytes and lymphocytes from patients with systemic lupus erythematosus using multi-color flow-FISH. Lupus 16(12):955–962CrossRefPubMed Beier F, Balabanov S, Amberger CC, Hartmann U, Manger K, Dietz K et al (2007) Telomere length analysis in monocytes and lymphocytes from patients with systemic lupus erythematosus using multi-color flow-FISH. Lupus 16(12):955–962CrossRefPubMed
20.
Zurück zum Zitat Wu CH, Hsieh SC, Li KJ, Lu MC, Yu CL (2007) Premature telomere shortening in polymorphonuclear neutrophils from patients with systemic lupus erythematosus is related to the lupus disease activity. Lupus 16(4):265–272CrossRefPubMed Wu CH, Hsieh SC, Li KJ, Lu MC, Yu CL (2007) Premature telomere shortening in polymorphonuclear neutrophils from patients with systemic lupus erythematosus is related to the lupus disease activity. Lupus 16(4):265–272CrossRefPubMed
21.
Zurück zum Zitat Kurosaka D, Yasuda J, Yoshida K, Yoneda A, Yasuda C, Kingetsu I et al (2006) Abnormal telomerase activity and telomere length in T and B cells from patients with systemic lupus erythematosus. J Rheumatol 33(6):1102–1107PubMed Kurosaka D, Yasuda J, Yoshida K, Yoneda A, Yasuda C, Kingetsu I et al (2006) Abnormal telomerase activity and telomere length in T and B cells from patients with systemic lupus erythematosus. J Rheumatol 33(6):1102–1107PubMed
22.
Zurück zum Zitat Lin J, Xie J, Qian WB (2005) Telomerase activity and telomere length in CD4+, CD8+ and CD19+ lymphocytes from patients with systemic lupus erythematosus. Zhejiang Da Xue Xue Bao Yi Xue Ban 34(6):534–537PubMed Lin J, Xie J, Qian WB (2005) Telomerase activity and telomere length in CD4+, CD8+ and CD19+ lymphocytes from patients with systemic lupus erythematosus. Zhejiang Da Xue Xue Bao Yi Xue Ban 34(6):534–537PubMed
23.
Zurück zum Zitat Honda M, Mengesha E, Albano S, Nichols WS, Wallace DJ, Metzger A et al (2001) Telomere shortening and decreased replicative potential, contrasted by continued proliferation of telomerase-positive CD8+CD28(lo) T cells in patients with systemic lupus erythematosus. Clin Immunol 99(2):211–221CrossRefPubMed Honda M, Mengesha E, Albano S, Nichols WS, Wallace DJ, Metzger A et al (2001) Telomere shortening and decreased replicative potential, contrasted by continued proliferation of telomerase-positive CD8+CD28(lo) T cells in patients with systemic lupus erythematosus. Clin Immunol 99(2):211–221CrossRefPubMed
24.
Zurück zum Zitat Lee YH, Rho YH, Choi SJ, Ji JD, Song GG (2007) PADI4 polymorphisms and rheumatoid arthritis susceptibility: a meta-analysis. Rheumatol Int 27(9):827–833CrossRefPubMed Lee YH, Rho YH, Choi SJ, Ji JD, Song GG (2007) PADI4 polymorphisms and rheumatoid arthritis susceptibility: a meta-analysis. Rheumatol Int 27(9):827–833CrossRefPubMed
25.
Zurück zum Zitat Lee YH, Bae SC, Choi SJ, Ji JD, Song GG (2011) Associations between vitamin D receptor polymorphisms and susceptibility to rheumatoid arthritis and systemic lupus erythematosus: a meta-analysis. Mol Biol Rep 38(6):3643–3651CrossRefPubMed Lee YH, Bae SC, Choi SJ, Ji JD, Song GG (2011) Associations between vitamin D receptor polymorphisms and susceptibility to rheumatoid arthritis and systemic lupus erythematosus: a meta-analysis. Mol Biol Rep 38(6):3643–3651CrossRefPubMed
26.
Zurück zum Zitat Lee YH, Woo JH, Choi SJ, Ji JD, Song GG (2010) Associations between osteoprotegerin polymorphisms and bone mineral density: a meta-analysis. Mol Biol Rep 37(1):227–234CrossRefPubMed Lee YH, Woo JH, Choi SJ, Ji JD, Song GG (2010) Associations between osteoprotegerin polymorphisms and bone mineral density: a meta-analysis. Mol Biol Rep 37(1):227–234CrossRefPubMed
27.
Zurück zum Zitat Hozo SP, Djulbegovic B, Hozo I (2005) Estimating the mean and variance from the median, range, and the size of a sample. BMC Med Res Methodol 5:13CrossRefPubMedPubMedCentral Hozo SP, Djulbegovic B, Hozo I (2005) Estimating the mean and variance from the median, range, and the size of a sample. BMC Med Res Methodol 5:13CrossRefPubMedPubMedCentral
28.
Zurück zum Zitat Ridout KK, Ridout SJ, Price LH, Sen S, Tyrka AR (2016) Depression and telomere length: A meta-analysis. J Affect Disord 191:237–247CrossRefPubMed Ridout KK, Ridout SJ, Price LH, Sen S, Tyrka AR (2016) Depression and telomere length: A meta-analysis. J Affect Disord 191:237–247CrossRefPubMed
29.
Zurück zum Zitat Wells G, Shea B, O’connell D, Peterson J, Welch V, Losos M et al (2000) The Newcastle-Ottawa Scale (NOS) for assessing the quality of nonrandomised studies in meta-analyses Wells G, Shea B, O’connell D, Peterson J, Welch V, Losos M et al (2000) The Newcastle-Ottawa Scale (NOS) for assessing the quality of nonrandomised studies in meta-analyses
30.
Zurück zum Zitat Cohen J (1988) Statistical power analysis for the behavioral sciences, 2nd edn. L. Erlbaum, Hillsdale Cohen J (1988) Statistical power analysis for the behavioral sciences, 2nd edn. L. Erlbaum, Hillsdale
32.
Zurück zum Zitat DerSimonian R, Laird N (1986) Meta-analysis in clinical trials. Control Clin Trials 7(3):177–188CrossRefPubMed DerSimonian R, Laird N (1986) Meta-analysis in clinical trials. Control Clin Trials 7(3):177–188CrossRefPubMed
33.
Zurück zum Zitat Higgins JP, Thompson SG (2002) Quantifying heterogeneity in a meta-analysis. Stat Med 21(11):1539–1558CrossRefPubMed Higgins JP, Thompson SG (2002) Quantifying heterogeneity in a meta-analysis. Stat Med 21(11):1539–1558CrossRefPubMed
34.
35.
Zurück zum Zitat Zhu X, Han W, Xue W, Zou Y, Xie C, Du J et al (2016) The association between telomere length and cancer risk in population studies. Sci Rep 6:22243CrossRefPubMedPubMedCentral Zhu X, Han W, Xue W, Zou Y, Xie C, Du J et al (2016) The association between telomere length and cancer risk in population studies. Sci Rep 6:22243CrossRefPubMedPubMedCentral
36.
Zurück zum Zitat Hohensinner PJ, Goronzy JJ, Weyand CM (2011) Telomere dysfunction, autoimmunity and aging. Aging Dis 2(6):524–537PubMedPubMedCentral Hohensinner PJ, Goronzy JJ, Weyand CM (2011) Telomere dysfunction, autoimmunity and aging. Aging Dis 2(6):524–537PubMedPubMedCentral
37.
Zurück zum Zitat Lin PY, Huang YC, Hung CF (2016) Shortened telomere length in patients with depression: A meta-analytic study. J Psychiatr Res 76:84–93CrossRefPubMed Lin PY, Huang YC, Hung CF (2016) Shortened telomere length in patients with depression: A meta-analytic study. J Psychiatr Res 76:84–93CrossRefPubMed
38.
Zurück zum Zitat Willeit P, Raschenberger J, Heydon EE, Tsimikas S, Haun M, Mayr A et al (2014) Leucocyte telomere length and risk of type 2 diabetes mellitus: new prospective cohort study and literature-based meta-analysis. PLOS ONE 9(11):e112483CrossRefPubMedPubMedCentral Willeit P, Raschenberger J, Heydon EE, Tsimikas S, Haun M, Mayr A et al (2014) Leucocyte telomere length and risk of type 2 diabetes mellitus: new prospective cohort study and literature-based meta-analysis. PLOS ONE 9(11):e112483CrossRefPubMedPubMedCentral
39.
Zurück zum Zitat Dehbi AZ, Radstake TR, Broen JC (2013) Accelerated telomere shortening in rheumatic diseases: cause or consequence? Expert Rev Clin Immunol 9(12):1193–1204CrossRefPubMed Dehbi AZ, Radstake TR, Broen JC (2013) Accelerated telomere shortening in rheumatic diseases: cause or consequence? Expert Rev Clin Immunol 9(12):1193–1204CrossRefPubMed
40.
Zurück zum Zitat Starkweather AR, Alhaeeri AA, Montpetit A, Brumelle J, Filler K, Montpetit M et al (2014) An integrative review of factors associated with telomere length and implications for biobehavioral research. Nurs Res 63(1):36–50CrossRefPubMedPubMedCentral Starkweather AR, Alhaeeri AA, Montpetit A, Brumelle J, Filler K, Montpetit M et al (2014) An integrative review of factors associated with telomere length and implications for biobehavioral research. Nurs Res 63(1):36–50CrossRefPubMedPubMedCentral
41.
Zurück zum Zitat Honda M, Mengesha E, Albano S, Nichols WS, Wallace DJ, Metzger A et al (2001) Telomere shortening and decreased replicative potential, contrasted by continued proliferation of telomerase-positive CD8+CD28(lo) T cells in patients with systemic lupus erythematosus. Clin Immunol 99(2):211–221CrossRefPubMed Honda M, Mengesha E, Albano S, Nichols WS, Wallace DJ, Metzger A et al (2001) Telomere shortening and decreased replicative potential, contrasted by continued proliferation of telomerase-positive CD8+CD28(lo) T cells in patients with systemic lupus erythematosus. Clin Immunol 99(2):211–221CrossRefPubMed
42.
Zurück zum Zitat Mirabello L, Yu K, Kraft P, De Vivo I, Hunter DJ, Prescott J et al (2010) The association of telomere length and genetic variation in telomere biology genes. Hum Mutat 31(9):1050–1058CrossRefPubMedPubMedCentral Mirabello L, Yu K, Kraft P, De Vivo I, Hunter DJ, Prescott J et al (2010) The association of telomere length and genetic variation in telomere biology genes. Hum Mutat 31(9):1050–1058CrossRefPubMedPubMedCentral
43.
Zurück zum Zitat Bax M, Huizinga TW, Toes RE (2014) The pathogenic potential of autoreactive antibodies in rheumatoid arthritis. Semin Immunopathol 36(3):313–325CrossRefPubMed Bax M, Huizinga TW, Toes RE (2014) The pathogenic potential of autoreactive antibodies in rheumatoid arthritis. Semin Immunopathol 36(3):313–325CrossRefPubMed
44.
Zurück zum Zitat Montpetit AJ, Alhareeri AA, Montpetit M, Starkweather AR, Elmore LW, Filler K et al (2014) Telomere length: a review of methods for measurement. Nurs Res 63(4):289–299CrossRefPubMedPubMedCentral Montpetit AJ, Alhareeri AA, Montpetit M, Starkweather AR, Elmore LW, Filler K et al (2014) Telomere length: a review of methods for measurement. Nurs Res 63(4):289–299CrossRefPubMedPubMedCentral
Metadaten
Titel
Association between shortened telomere length and rheumatoid arthritis
A meta-analysis
verfasst von
Y. H. Lee, MD, PhD
S.-C. Bae
Publikationsdatum
19.09.2016
Verlag
Springer Medizin
Erschienen in
Zeitschrift für Rheumatologie / Ausgabe 2/2018
Print ISSN: 0340-1855
Elektronische ISSN: 1435-1250
DOI
https://doi.org/10.1007/s00393-016-0209-9

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