Skip to main content

Advertisement

Log in

Rheumatoid arthritis significantly increased recurrence risk after ischemic stroke/transient ischemic attack

  • Original Communication
  • Published:
Journal of Neurology Aims and scope Submit manuscript

Abstract

The effect of RA on recurrent stroke is unknown. Therefore, we examined effects of rheumatoid arthritis (RA) on risk of stroke recurrence and investigated the interaction between RA and traditional cardiovascular risk factors on recurrence risk after ischemic stroke (IS) or transient ischemic attack (TIA). Of 3190 patients with IS or TIA recruited in this cohort study, 638 were comorbid with RA and 2552 without RA. Stroke recurrence, RA, lifestyle, lipid variables and other comorbidities were identified through linkage between a nationwide stroke database in Taiwan and the National Health Insurance claims database. Cox proportional hazard models with competing risk adjustment were used to evaluate the relationship between RA and recurrent stroke. Patients with RA showed a significantly increased risk of recurrent stroke, particular in recurrent IS/TIA. The increased risk of recurrent IS/TIA in RA patients may through the changes of triglycerides (TG)/high-density lipoprotein cholesterol (HDL-C) ratio. A positive additive interaction was observed between RA and current smoking on the risk of recurrent IS/TIA. Significantly increased risks for recurrent IS/TIA were observed among RA patients who smoked > 40 years or those who smoked > 20 cigarettes/day. This study provides the first evidence that RA significantly increased recurrence IS/TIA risk. The changes of TG/HDL-C ratio may play some roles in the recurrence IS/TIA risk in RA patients. In addition, our results suggest that smoking increases the risk of recurrent IS/TIA in RA patients and reinforces the need for aggressive smoking cessation efforts in RA patients.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1

Similar content being viewed by others

References

  1. Di Carlo A (2009) Human and economic burden of stroke. Age Ageing 38:4–5

    Article  PubMed  Google Scholar 

  2. Lloyd-Jones D, Adams R, Carnethon M, De Simone G, Ferguson TB, Flegal K, Ford E, Furie K, Go A, Greenlund K, Haase N, Hailpern S, Ho M, Howard V, Kissela B, Kittner S, Lackland D, Lisabeth L, Marelli A, McDermott M, Meigs J, Mozaffarian D, Nichol G, O’Donnell C, Roger V, Rosamond W, Sacco R, Sorlie P, Stafford R, Steinberger J, Thom T, Wasserthiel-Smoller S, Wong N, Wylie-Rosett J, Hong Y (2009) Heart disease and stroke statistics–2009 update: a report from the American Heart Association Statistics Committee and Stroke Statistics Subcommittee. Circulation 119:e21–e181

    Google Scholar 

  3. Dhamoon MS, Sciacca RR, Rundek T, Sacco RL, Elkind MS (2006) Recurrent stroke and cardiac risks after first ischemic stroke: the Northern Manhattan Study. Neurology 66:641–646

    Article  PubMed  CAS  Google Scholar 

  4. Jorgensen HS, Nakayama H, Reith J, Raaschou HO, Olsen TS (1997) Stroke recurrence: predictors, severity, and prognosis. The Copenhagen Stroke Study. Neurology 48:891–895

    Article  PubMed  CAS  Google Scholar 

  5. Samsa GP, Bian J, Lipscomb J, Matchar DB (1999) Epidemiology of recurrent cerebral infarction: a medicare claims-based comparison of first and recurrent strokes on 2-year survival and cost. Stroke 30:338–349

    Article  PubMed  CAS  Google Scholar 

  6. Jin R, Yang G, Li G (2010) Inflammatory mechanisms in ischemic stroke: role of inflammatory cells. J Leukoc Biol 87:779–789

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  7. Suresh E (2004) Diagnosis of early rheumatoid arthritis: what the non-specialist needs to know. J R Soc Med 97:421–424

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  8. Kahlenberg JM, Kaplan MJ (2013) Mechanisms of premature atherosclerosis in rheumatoid arthritis and lupus. Annu Rev Med 64:249–263

    Article  PubMed  CAS  Google Scholar 

  9. Cavagna L, Boffini N, Cagnotto G, Inverardi F, Grosso V, Caporali R (2012) Atherosclerosis and rheumatoid arthritis: more than a simple association. Mediators Inflamm 2012:147354

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  10. Welsh P, Lowe GD, Chalmers J, Campbell DJ, Rumley A, Neal BC, MacMahon SW, Woodward M (2008) Associations of proinflammatory cytokines with the risk of recurrent stroke. Stroke 39:2226–2230

    Article  PubMed  CAS  Google Scholar 

  11. Rodriguez-Carrio J, Alperi-Lopez M, Lopez P, Lopez-Mejias R, Alonso-Castro S, Abal F, Ballina-Garcia FJ, Gonzalez-Gay MA, Suarez A (2017) High triglycerides and low high-density lipoprotein cholesterol lipid profile in rheumatoid arthritis: a potential link among inflammation, oxidative status, and dysfunctional high-density lipoprotein. J Clin Lipidol 11:1043–1054.e1042

    Article  PubMed  Google Scholar 

  12. Park JH, Lee J, Ovbiagele B (2014) Nontraditional serum lipid variables and recurrent stroke risk. Stroke 45:3269–3274

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  13. Hsieh FI, Lien LM, Chen ST, Bai CH, Sun MC, Tseng HP, Chen YW, Chen CH, Jeng JS, Tsai SY, Lin HJ, Liu CH, Lo YK, Chen HJ, Chiu HC, Lai ML, Lin RT, Sun MH, Yip BS, Chiou HY, Hsu CY (2010) Get with the Guidelines-Stroke performance indicators: surveillance of stroke care in the Taiwan Stroke Registry: get with the Guidelines-Stroke in Taiwan. Circulation 122:1116–1123

    Article  PubMed  Google Scholar 

  14. Chen L, Yip W, Chang MC, Lin HS, Lee SD, Chiu YL, Lin YH (2007) The effects of Taiwan’s National Health Insurance on access and health status of the elderly. Health Econ 16:223–242

    Article  PubMed  CAS  Google Scholar 

  15. Liou TH, Huang SW, Lin JW, Chang YS, Wu CW, Lin HW (2014) Risk of stroke in patients with rheumatism: a nationwide longitudinal population-based study. Sci Rep 4:5110

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  16. Lim CH, Lin CH, Chen DY, Chen YM, Chao WC, Liao TL, Chen HH (2016) One-year tuberculosis risk in rheumatoid arthritis patients starting their first tumor necrosis factor inhibitor therapy from 2008 to 2012 in Taiwan: a Nationwide Population-Based Cohort Study. PLoS One 11:e0166339

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  17. Elmariah S, Furlan AJ, Reisman M, Burke D, Vardi M, Wimmer NJ, Ling S, Chen X, Kent DM, Massaro J, Mauri L (2014) Predictors of recurrent events in patients with cryptogenic stroke and patent foramen ovale within the CLOSURE I (Evaluation of the STARFlex septal closure system in patients with a stroke and/or transient ischemic attack due to presumed paradoxical embolism through a patent foramen ovale) trial. JACC Cardiovasc Interv 7:913–920

    Article  PubMed  Google Scholar 

  18. Adams HP Jr, Woolson RF, Biller J, Clarke W (1992) Studies of Org 10172 in patients with acute ischemic stroke. TOAST Study Group Haemost 22:99–103

    Google Scholar 

  19. Lemieux I, Lamarche B, Couillard C, Pascot A, Cantin B, Bergeron J, Dagenais GR, Despres JP (2001) Total cholesterol/HDL cholesterol ratio vs LDL cholesterol/HDL cholesterol ratio as indices of ischemic heart disease risk in men: the Quebec Cardiovascular Study. Arch Intern Med 161:2685–2692

    Article  PubMed  CAS  Google Scholar 

  20. Panagiotakos DB, Pitsavos C, Skoumas J, Chrysohoou C, Toutouza M, Stefanadis CI, Toutouzas PK (2003) Importance of LDL/HDL cholesterol ratio as a predictor for coronary heart disease events in patients with heterozygous familial hypercholesterolaemia: a 15-year follow-up (1987–2002). Curr Med Res Opin 19:89–94

    PubMed  CAS  Google Scholar 

  21. Friedewald WT, Levy RI, Fredrickson DS (1972) Estimation of the concentration of low-density lipoprotein cholesterol in plasma, without use of the preparative ultracentrifuge. Clin Chem 18:499–502

    PubMed  CAS  Google Scholar 

  22. Kawachi I, Colditz GA, Stampfer MJ, Willett WC, Manson JE, Rosner B, Speizer FE, Hennekens CH (1993) Smoking cessation and decreased risk of stroke in women. Jama 269:232–236

    Article  PubMed  CAS  Google Scholar 

  23. Fine JP, Gray RJ (1999) A proportional hazards model for the subdistribution of a competing risk. J Am Stat Assoc 94:496–509

    Article  Google Scholar 

  24. Pintilie M (2011) An introduction to competing risks analysis. Rev Esp Cardiol 64:599–605

    Article  PubMed  Google Scholar 

  25. Kalilani L, Atashili J (2006) Measuring additive interaction using odds ratios. Epidemiol Perspect Innov 3:5

    Article  PubMed  PubMed Central  Google Scholar 

  26. Schafer JL (1999) Multiple imputation: a primer. Stat Methods Med Res 8:3–15

    Article  PubMed  CAS  Google Scholar 

  27. Holmqvist M, Gransmark E, Mantel A, Alfredsson L, Jacobsson LT, Wallberg-Jonsson S, Askling J (2013) Occurrence and relative risk of stroke in incident and prevalent contemporary rheumatoid arthritis. Ann Rheum Dis 72:541–546

    Article  PubMed  Google Scholar 

  28. Posadas-Sanchez R, Posadas-Romero C, Mendoza-Perez E, Caracas-Portilla NA, Cardoso-Saldana G, Medina-Urrutia A, Jorge-Galarza E, Juarez-Rojas JG (2012) Cholesterol efflux and metabolic abnormalities associated with low high-density-lipoprotein-cholesterol and high triglycerides in statin-treated coronary men with low-density lipoprotein-cholesterol < 70 mg/dl. Am J Cardiol 109:636–641

    Article  PubMed  CAS  Google Scholar 

  29. Khera AV, Cuchel M, de la Llera-Moya M, Rodrigues A, Burke MF, Jafri K, French BC, Phillips JA, Mucksavage ML, Wilensky RL, Mohler ER, Rothblat GH, Rader DJ (2011) Cholesterol efflux capacity, high-density lipoprotein function, and atherosclerosis. N Engl J Med 364:127–135

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  30. Zhao W, Gong W, Wu N, Li Y, Ye K, Lu B, Zhang Z, Qu S, Li Y, Yang Y, Hu R (2014) Association of lipid profiles and the ratios with arterial stiffness in middle-aged and elderly Chinese. Lipids Health Dis 13:37

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  31. Sonmez A, Yilmaz MI, Saglam M, Unal HU, Gok M, Cetinkaya H, Karaman M, Haymana C, Eyileten T, Oguz Y, Vural A, Rizzo M, Toth PP (2015) The role of plasma triglyceride/high-density lipoprotein cholesterol ratio to predict cardiovascular outcomes in chronic kidney disease. Lipids Health Dis 14:29

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  32. Matsuzawa Y, Guddeti RR, Kwon TG, Lerman LO, Lerman A (2015) Secondary prevention strategy of cardiovascular disease using endothelial function testing. Circ J 79:685–694

    Article  PubMed  CAS  Google Scholar 

  33. Hong JB, Leonards CO, Endres M, Siegerink B, Liman TG (2016) Ankle-brachial index and recurrent stroke risk: meta-analysis. Stroke 47:317–322

    Article  PubMed  Google Scholar 

  34. Dhamoon MS, Tai W, Boden-Albala B, Rundek T, Paik MC, Sacco RL, Elkind MS (2007) Risk of myocardial infarction or vascular death after first ischemic stroke: the Northern Manhattan Study. Stroke 38:1752–1758

    Article  PubMed  Google Scholar 

  35. Mohan KM, Crichton SL, Grieve AP, Rudd AG, Wolfe CD, Heuschmann PU (2009) Frequency and predictors for the risk of stroke recurrence up to 10 years after stroke: the South London Stroke Register. J Neurol Neurosurg Psychiatry 80:1012–1018

    Article  PubMed  CAS  Google Scholar 

  36. Kim J, Gall SL, Dewey HM, Macdonell RA, Sturm JW, Thrift AG (2012) Baseline smoking status and the long-term risk of death or nonfatal vascular event in people with stroke: a 10-year survival analysis. Stroke 43:3173–3178

    Article  PubMed  Google Scholar 

  37. Shah RS, Cole JW (2010) Smoking and stroke: the more you smoke the more you stroke. Expert Rev Cardiovasc Ther 8:917–932

    Article  PubMed  PubMed Central  Google Scholar 

  38. Wang YF, Chuang MH, Chuang TL, Huang KY, Lyu SR, Huang CY, Lee CC (2014) CHADS 2 scores in the prediction of major adverse cardiovascular events in patients with Cushing’s syndrome. Int J Endocrinol 2014:138653

    PubMed  PubMed Central  Google Scholar 

  39. Gall SL, Dewey HM, Thrift AG (2009) Smoking cessation at 5 years after stroke in the North East Melbourne stroke incidence study. Neuroepidemiology 32:196–200

    Article  PubMed  Google Scholar 

Download references

Acknowledgements

The data analyzed in this study were provided by the Health and Welfare Data Science Center (HWDC) and the Health Promotion Administration, Ministry of Health and Welfare, Taiwan.

Funding

This work was supported in part by Grants from the Ministry of Health and Welfare (MOHW105-TDU-B-212-133018); Ministry of Science and Technology (NSC 100-2811-B-038-018; NSC 101-2314-B-038-043-MY3; NSC 102-2314-B-038-041; MOST 104-2314-B-038-069); the Health Promotion Administration, Ministry of Health and Welfare; Dr. Chi-Chin Huang Stroke Research Center. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Hung-Yi Chiou.

Ethics declarations

Conflicts of interest

None of the authors has any conflict of interest to disclose.

Ethical standards

This study was carried in accordance with ethical standard as set out in the Declaration of Helsinki and this study was confirmed exemption by Taipei Medical University Joint Institutional Review Board (approval no. 201411004).

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (DOC 119 KB)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Chen, YR., Hsieh, FI., Lien, LM. et al. Rheumatoid arthritis significantly increased recurrence risk after ischemic stroke/transient ischemic attack. J Neurol 265, 1810–1818 (2018). https://doi.org/10.1007/s00415-018-8885-9

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00415-018-8885-9

Keywords

Navigation