Elucidating the environmental risk factors for rheumatic diseases: An umbrella review of meta-analyses
Lazaros Belbasis
Department of Hygiene and Epidemiology, University of Ioannina Medical School, Ioannina, Greece
Search for more papers by this authorVasilios Dosis
Department of Hygiene and Epidemiology, University of Ioannina Medical School, Ioannina, Greece
Search for more papers by this authorCorresponding Author
Evangelos Evangelou
Department of Hygiene and Epidemiology, University of Ioannina Medical School, Ioannina, Greece
Department of Epidemiology and Biostatistics, School of Public Health, Imperial College London, London, UK
Correspondence: Evangelos Evangelou, Department of Hygiene and Epidemiology, University of Ioannina Medical School, Ioannina 45110, Greece ([email protected]).Search for more papers by this authorLazaros Belbasis
Department of Hygiene and Epidemiology, University of Ioannina Medical School, Ioannina, Greece
Search for more papers by this authorVasilios Dosis
Department of Hygiene and Epidemiology, University of Ioannina Medical School, Ioannina, Greece
Search for more papers by this authorCorresponding Author
Evangelos Evangelou
Department of Hygiene and Epidemiology, University of Ioannina Medical School, Ioannina, Greece
Department of Epidemiology and Biostatistics, School of Public Health, Imperial College London, London, UK
Correspondence: Evangelos Evangelou, Department of Hygiene and Epidemiology, University of Ioannina Medical School, Ioannina 45110, Greece ([email protected]).Search for more papers by this authorAbstract
Aims
Although rheumatic diseases constitute a leading cause of disability, the environmental risk factors for these diseases are not clarified. In the present study, we aim to systematically appraise the epidemiological credibility of the environmental risk factors for rheumatic diseases.
Methods
We systematically searched PubMed to capture meta-analyses of observational studies on environmental risk factors for the most prevalent rheumatic diseases. For each association, we estimated the summary effect size estimate, the 95% confidence and prediction intervals, and the I2 metric. We further examined the presence of small-study effects and excess significance bias.
Results
Overall, we identified 30 eligible papers describing 42 associations. Thirty-three associations were statistically significant at P < 0.05, whereas 13 of them were statistically significant at P < 1 × 10−6. Thirty-two associations had large or very large between-study heterogeneity. In 12 associations, evidence of small-study effects and/or excess significance bias was found. Six risk factors (nine associations) presented convincing or highly suggestive evidence of association: smoking and pack-years of smoking for rheumatoid arthritis; BMI (per 5 kg/m2 increase) for gout and hip osteoarthritis; alcohol consumption for gout; BMI (overweight vs lean, obese vs lean), knee injury and participation in heavy work for knee osteoarthritis.
Conclusion
Our umbrella review indicated that a narrow range of risk factors has been examined for rheumatic diseases. Current evidence strongly supports that smoking, obesity, alcohol consumption, knee injury, and work activities are associated with risk for at least one rheumatic disease.
CONFLICT OF INTERESTS
None.
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REFERENCES
- 1Gourley M, Miller FW. Mechanisms of disease: environmental factors in the pathogenesis of rheumatic disease. Nat Clin Pract Rheumatol. 2007; 3(3): 172-180.
- 2Palazzo C, Ravaud J-FJ, Papelard A, Ravaud P, Poiraudeau S. The burden of musculoskeletal conditions. PLoS One. 2014; 9(3): e90633.
- 3Stahl EA, Raychaudhuri S, Remmers EF, et al. Genome-wide association study meta-analysis identifies seven new rheumatoid arthritis risk loci. Nat Genet. 2010; 42: 508-514.
- 4Okada Y, Wu D, Trynka G, et al. Genetics of rheumatoid arthritis contributes to biology and drug discovery. Nature. 2014; 506(7488): 376-381.
- 5Orozco G, Viatte S, Bowes J, et al. Novel rheumatoid arthritis susceptibility locus at 22q12 identified in an extended UK genome-wide association study. Arthritis Rheumatol. 2014; 66(1): 24-30.
- 6Radstake TRDJ, Gorlova O, Rueda B, et al. Genome-wide association study of systemic sclerosis identifies CD247 as a new susceptibility locus. Nat Genet. 2010; 42(5): 426-429.
- 7Allanore Y, Saad M, Dieudé P, et al. Genome-wide scan identifies TNIP1, PSORS1C1, and RHOB as novel risk loci for systemic sclerosis. PLoS Genet. 2011; 7(7): e1002091.
- 8Gorlova O, Martin J-E, Rueda B, et al. Identification of novel genetic markers associated with clinical phenotypes of systemic sclerosis through a genome-wide association strategy. PLoS Genet. 2011; 7(7): e1002178.
- 9Terao C, Kawaguchi T, Dieude P, et al. Transethnic meta-analysis identifies GSDMA and PRDM1 as susceptibility genes to systemic sclerosis. Ann Rheum Dis. 2017; 76(6): 1150-1158.
- 10Taylor KE, Wong Q, Levine DM, et al. Genome-wide association analysis reveals genetic heterogeneity of Sjögren's syndrome according to ancestry. Arthritis Rheumatol. 2017; 69(6): 1294-1305.
- 11Bentham J, Morris DL, Graham DSC, et al. Genetic association analyses implicate aberrant regulation of innate and adaptive immunity genes in the pathogenesis of systemic lupus erythematosus. Nat Genet. 2015; 47(12): 1457-1464.
- 12Lessard CJ, Sajuthi S, Zhao J, et al. Identification of a systemic lupus erythematosus risk locus spanning ATG16L2, FCHSD2, and P2RY2 in Koreans. Arthritis Rheumatol. 2016; 68(5): 1197-1209.
- 13Morris DL, Sheng Y, Zhang Y, et al. Genome-wide association meta-analysis in Chinese and European individuals identifies ten new loci associated with systemic lupus erythematosus. Nat Genet. 2016; 48(8): 940-946.
- 14 Australo-Anglo-American Spondyloarthritis Consortium (TASC), Reveille JD, Sims A-M, et al. Genome-wide association study of ankylosing spondylitis identifies non-MHC susceptibility loci. Nat Genet. 2010; 42(2): 123-127.
- 15Carmona FD, Vaglio A, Mackie SL, et al. A genome-wide association study identifies risk alleles in plasminogen and P4HA2 associated with giant cell arteritis. Am J Hum Genet. 2017; 100(1): 64-74.
- 16Matsuo H, Yamamoto K, Nakaoka H, et al. Genome-wide association study of clinically defined gout identifies multiple risk loci and its association with clinical subtypes. Ann Rheum Dis. 2016; 75(4): 652-659.
- 17Nakayama A, Nakaoka H, Yamamoto K, et al. GWAS of clinically defined gout and subtypes identifies multiple susceptibility loci that include urate transporter genes. Ann Rheum Dis. 2017; 76(5): 869-877.
- 18 arcOGEN Consortium, arcOGEN Collaborators, Zeggini E, et al. Identification of new susceptibility loci for osteoarthritis (arcOGEN): a genome-wide association study. Lancet. 2012; 380(9844): 815-823.
- 19Evangelou E, Kerkhof HJ, Styrkarsdottir U, et al. A meta-analysis of genome-wide association studies identifies novel variants associated with osteoarthritis of the hip. Ann Rheum Dis. 2014; 73(12): 2130-2136.
- 20Oliver JE, Silman AJ. What epidemiology has told us about risk factors and aetiopathogenesis in rheumatic diseases. Arthritis Res Ther. 2009; 11(3): 223.
- 21Ioannidis JPA. Integration of evidence from multiple meta-analyses: a primer on umbrella reviews, treatment networks and multiple treatments meta-analyses. CMAJ. 2009; 181(8): 488-493.
- 22Belbasis L, Bellou V, Evangelou E, Ioannidis JPA, Tzoulaki I. Environmental risk factors and multiple sclerosis: an umbrella review of systematic reviews and meta-analyses. Lancet Neurol. 2015; 14(3): 263-273.
- 23Bellou V, Belbasis L, Tzoulaki I, Evangelou E, Ioannidis JPA. Environmental risk factors and Parkinson's disease: an umbrella review of meta-analyses. Parkinsonism Relat Disord. 2016; 23: 1-9.
- 24Belbasis L, Bellou V, Evangelou E. Environmental risk factors and amyotrophic lateral sclerosis: an umbrella review and critical assessment of current evidence from systematic reviews and meta-analyses of observational studies. Neuroepidemiology. 2016; 46(2): 96-105.
- 25Bellou V, Belbasis L, Tzoulaki I, Middleton LT, Ioannidis JPA, Evangelou E. Systematic evaluation of the associations between environmental risk factors and dementia: an umbrella review of systematic reviews and meta-analyses. Alzheimers Dement. 2017; 13(4): 406-418.
- 26Belbasis L, Stefanaki I, Stratigos AJ, Evangelou E. Non-genetic risk factors for cutaneous melanoma and keratinocyte skin cancers: an umbrella review of meta-analyses. J Dermatol Sci. 2016; 84(3): 330-339.
- 27Belbasis L, Savvidou MD, Kanu C, Evangelou E, Tzoulaki I. Birth weight in relation to health and disease in later life: an umbrella review of systematic reviews and meta-analyses. BMC Med. 2016; 14(1): 147.
- 28Belbasis L, Köhler CAA, Stefanis N, et al. Risk factors and peripheral biomarkers for schizophrenia spectrum disorders: an umbrella review of meta-analyses. Acta Psychiatr Scand. 2018; 137(2): 88-97.
- 29Bellou V, Belbasis L, Tzoulaki I, Evangelou E. Risk factors for type 2 diabetes mellitus: an exposure-wide umbrella review of meta-analyses. PLoS One. 2018; 13(3): e0194127.
- 30Helmick CG, Felson DT, Lawrence RC, et al. Estimates of the prevalence of arthritis and other rheumatic conditions in the United States: Part I. Arthritis Rheum. 2008; 58(1): 15-25.
- 31Lawrence RC, Felson DT, Helmick CG, et al. Estimates of the prevalence of arthritis and other rheumatic conditions in the United States: Part II. Arthritis Rheum. 2008; 58(1): 26-35.
- 32DerSimonian R, Laird N. Meta-analysis in clinical trials. Control Clin Trials. 1986; 7(3): 177-188.
- 33Lau J, Ioannidis JP, Schmid CH. Quantitative synthesis in systematic reviews. Ann Intern Med. 1997; 127(9): 820-826.
- 34Higgins JPT, Thompson SG. Quantifying heterogeneity in a meta-analysis. Stat Med. 2002; 21(11): 1539-1558.
- 35Higgins JPT, Thompson SG, Deeks JJ, Altman DG. Measuring inconsistency in meta-analyses. BMJ. 2003; 327(7414): 557-560.
- 36Higgins JPT, Thompson SG, Spiegelhalter DJ. A re-evaluation of random-effects meta-analysis. J R Stat Soc Ser A Stat Soc. 2009; 172(1): 137-159.
- 37Higgins JPT. Commentary: heterogeneity in meta-analysis should be expected and appropriately quantified. Int J Epidemiol. 2008; 37(5): 1158-1160.
- 38Sterne JAC, Sutton AJ, Ioannidis JPA, et al. Recommendations for examining and interpreting funnel plot asymmetry in meta-analyses of randomised controlled trials. BMJ. 2011; 343: d4002.
- 39Egger M, Davey Smith G, Schneider M, Minder C. Bias in meta-analysis detected by a simple, graphical test. BMJ. 1997; 315(7109): 629-634.
- 40Ioannidis JPA, Trikalinos TA. An exploratory test for an excess of significant findings. Clin Trials. 2007; 4(3): 245-253.
- 41Ioannidis JPA. Clarifications on the application and interpretation of the test for excess significance and its extensions. J Math Psychol. 2013; 57(5): 184-187.
- 42Louati K, Vidal C, Berenbaum F, Sellam J. Association between diabetes mellitus and osteoarthritis: systematic literature review and meta-analysis. RMD Open. 2015; 1(1): e000077.
- 43Øiestad BE, Juhl CB, Eitzen I, Thorlund JB. Knee extensor muscle weakness is a risk factor for development of knee osteoarthritis. A systematic review and meta-analysis. Osteoarthr Cartil. 2015; 23(2): 171-177.
- 44Hammer PEC, Shiri R, Kryger AI, Kirkeskov L, Bonde JP. Associations of work activities requiring pinch or hand grip or exposure to hand-arm vibration with finger and wrist osteoarthritis: a meta-analysis. Scand J Work Environ Health. 2014; 40(2): 133-145.
- 45Sugiyama D, Nishimura K, Tamaki K, et al. Impact of smoking as a risk factor for developing rheumatoid arthritis: a meta-analysis of observational studies. Ann Rheum Dis. 2010; 69(1): 70-81.
- 46Johnson VE. Revised standards for statistical evidence. Proc Natl Acad Sci USA. 2013; 110(48): 19313-19317.
- 47Benjamin DJ, Berger JO, Johannesson M, et al. Redefine statistical significance. Nat Hum Behav. 2018; 2: 6-10.
- 48Dalbeth N, Merriman TR, Stamp LK. Gout. Lancet. 2016; 388(10055): 2039-2052.
- 49Aune D, Norat T, Vatten LJ. Body mass index and the risk of gout: a systematic review and dose-response meta-analysis of prospective studies. Eur J Nutr. 2014; 53(8): 1591-1601.
- 50Choi HK, Curhan G. Beer, liquor, and wine consumption and serum uric acid level: the Third National Health and Nutrition Examination Survey. Arthritis Rheum. 2004; 51(6): 1023-1029.
- 51Di Giuseppe D, Discacciati A, Orsini N, Wolk A. Cigarette smoking and risk of rheumatoid arthritis: a dose-response meta-analysis. Arthritis Res Ther. 2014; 16(2): R61.
- 52Glyn-Jones S, Palmer AJR, Agricola R, et al. Osteoarthritis. Lancet. 2015; 386(9991): 376-387.
- 53Jiang F, Li S, Jia C. Smoking and the risk of systemic lupus erythematosus: an updated systematic review and cumulative meta-analysis. Clin Rheumatol. 2015; 34(11): 1885-1892.
- 54Handel AE, Williamson AJ, Disanto G, Dobson R, Giovannoni G, Ramagopalan SV. Smoking and multiple sclerosis: an updated meta-analysis. PLoS One. 2011; 6(1): e16149.
- 55McCormic ZD, Khuder SS, Aryal BK, Ames AL, Khuder SA. Occupational silica exposure as a risk factor for scleroderma: a meta-analysis. Int Arch Occup Environ Health. 2010; 83(7): 763-769.
- 56Gold LS, Ward MH, Dosemeci M, De Roos AJ. Systemic autoimmune disease mortality and occupational exposures. Arthritis Rheum. 2007; 56(10): 3189-3201.
- 57Ungprasert P, Thongprayoon C, Warrington KJ. Lower body mass index is associated with a higher risk of giant cell arteritis: a systematic review and meta-analysis. Ann Transl Med. 2015; 3(16): 232.
- 58Wang M, Jiang X, Wu W, Zhang D. A meta-analysis of alcohol consumption and the risk of gout. Clin Rheumatol. 2013; 32(11): 1641-1648.
- 59Hui M, Doherty M, Zhang W. Does smoking protect against osteoarthritis? Meta-analysis of observational studies. Ann Rheum Dis. 2011; 70(7): 1231-1237.
- 60Tran G, Smith TO, Grice A, Kingsbury SR, McCrory P, Conaghan PG. Does sports participation (including level of performance and previous injury) increase risk of osteoarthritis? A systematic review and meta-analysis. Br J Sports Med. 2016; 50(23): 1459-1466.
- 61Jiang L, Rong J, Wang Y, et al. The relationship between body mass index and hip osteoarthritis: a systematic review and meta-analysis. Joint Bone Spine. 2011; 78(2): 150-155.
- 62Silverwood V, Blagojevic-Bucknall M, Jinks C, Jordan JL, Protheroe J, Jordan KP. Current evidence on risk factors for knee osteoarthritis in older adults: a systematic review and meta-analysis. Osteoarthr Cartil. 2015; 23(4): 507-515.
- 63McWilliams DF, Leeb BF, Muthuri SG, Doherty M, Zhang W. Occupational risk factors for osteoarthritis of the knee: a meta-analysis. Osteoarthr Cartil. 2011; 19(7): 829-839.
- 64Zheng H, Chen C. Body mass index and risk of knee osteoarthritis: systematic review and meta-analysis of prospective studies. BMJ Open. 2015; 5(12): e007568.
- 65Chen Q, Jin Z, Xiang C, Cai Q, Shi W, He J. Absence of protective effect of oral contraceptive use on the development of rheumatoid arthritis: a meta-analysis of observational studies. Int J Rheum Dis. 2014; 17(7): 725-737.
- 66Chen H, Wang J, Zhou W, Yin H, Wang M. Breastfeeding and risk of rheumatoid arthritis: a systematic review and metaanalysis. J Rheumatol. 2015; 42(9): 1563-1569.
- 67Khuder SA, Peshimam AZ, Agraharam S. Environmental risk factors for rheumatoid arthritis. Rev Environ Health. 2002; 17(4): 307-315.
- 68Feng J, Chen Q, Yu F, et al. Body mass index and risk of rheumatoid arthritis: a meta-analysis of observational studies. Medicine (Baltimore). 2016; 95(8): e2859.
- 69Lee YH, Bae S-C, Song GG. Coffee or tea consumption and the risk of rheumatoid arthritis: a meta-analysis. Clin Rheumatol. 2014; 33(11): 1575-1583.
- 70Scott IC, Tan R, Stahl D, Steer S, Lewis CM, Cope AP. The protective effect of alcohol on developing rheumatoid arthritis: a systematic review and meta-analysis. Rheumatology (Oxford). 2013; 52(5): 856-867.
- 71Song GG, Bae S-C, Lee YH. Association between vitamin D intake and the risk of rheumatoid arthritis: a meta-analysis. Clin Rheumatol. 2012; 31(12): 1733-1739.
- 72Ball RJ, Avenell A, Aucott L, Hanlon P, Vickers MA. Systematic review and meta-analysis of the sero-epidemiological association between Epstein-Barr virus and rheumatoid arthritis. Arthritis Res Ther. 2015; 17: 274.
- 73Di Giuseppe D, Crippa A, Orsini N, Wolk A. Fish consumption and risk of rheumatoid arthritis: a dose-response meta-analysis. Arthritis Res Ther. 2014; 16(5): 446.
- 74Wang Y, Dou H, Liu G, et al. Hepatitis C virus infection and the risk of Sjögren or sicca syndrome: a meta-analysis. Microbiol Immunol. 2014; 58(12): 675-687.
- 75Hanlon P, Avenell A, Aucott L, Vickers MA. Systematic review and meta-analysis of the sero-epidemiological association between Epstein-Barr virus and systemic lupus erythematosus. Arthritis Res Ther. 2014; 16(1): R3.
- 76Rojas-Villarraga A, Torres-Gonzalez J-V, Ruiz-Sternberg Á-M. Safety of hormonal replacement therapy and oral contraceptives in systemic lupus erythematosus: a systematic review and meta-analysis. PLoS One. 2014; 9(8): e104303.
- 77Wang J, Pan H-F, Ye D-Q, Su H, Li X-P. Moderate alcohol drinking might be protective for systemic lupus erythematosus: a systematic review and meta-analysis. Clin Rheumatol. 2008; 27(12): 1557-1563.
- 78Kettaneh A, Al Moufti O, Tiev KP, et al. Occupational exposure to solvents and gender-related risk of systemic sclerosis: a metaanalysis of case-control studies. J Rheumatol. 2007; 34(1): 97-103.