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Published in: Journal of Neurology 8/2018

01-08-2018 | Original Communication

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

Authors: Yih-Ru Chen, Fang-I Hsieh, Li-Ming Lien, Chaur-Jong Hu, Jiann-Shing Jeng, Giia-Sheun Peng, Sung-Chun Tang, Nai-Fang Chi, Yueh-Feng Sung, Hung-Yi Chiou

Published in: Journal of Neurology | Issue 8/2018

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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.
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Literature
2.
go back to reference 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 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
3.
go back to reference 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 66:641–646CrossRefPubMed 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 66:641–646CrossRefPubMed
4.
go back to reference Jorgensen HS, Nakayama H, Reith J, Raaschou HO, Olsen TS (1997) Stroke recurrence: predictors, severity, and prognosis. The Copenhagen Stroke Study. Neurology 48:891–895CrossRefPubMed Jorgensen HS, Nakayama H, Reith J, Raaschou HO, Olsen TS (1997) Stroke recurrence: predictors, severity, and prognosis. The Copenhagen Stroke Study. Neurology 48:891–895CrossRefPubMed
5.
go back to reference 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 30:338–349CrossRefPubMed 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 30:338–349CrossRefPubMed
8.
go back to reference Kahlenberg JM, Kaplan MJ (2013) Mechanisms of premature atherosclerosis in rheumatoid arthritis and lupus. Annu Rev Med 64:249–263CrossRefPubMed Kahlenberg JM, Kaplan MJ (2013) Mechanisms of premature atherosclerosis in rheumatoid arthritis and lupus. Annu Rev Med 64:249–263CrossRefPubMed
9.
go back to reference Cavagna L, Boffini N, Cagnotto G, Inverardi F, Grosso V, Caporali R (2012) Atherosclerosis and rheumatoid arthritis: more than a simple association. Mediators Inflamm 2012:147354CrossRefPubMedPubMedCentral Cavagna L, Boffini N, Cagnotto G, Inverardi F, Grosso V, Caporali R (2012) Atherosclerosis and rheumatoid arthritis: more than a simple association. Mediators Inflamm 2012:147354CrossRefPubMedPubMedCentral
10.
go back to reference 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 39:2226–2230CrossRefPubMed 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 39:2226–2230CrossRefPubMed
11.
go back to reference 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.e1042CrossRefPubMed 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.e1042CrossRefPubMed
13.
go back to reference 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 122:1116–1123CrossRefPubMed 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 122:1116–1123CrossRefPubMed
14.
go back to reference 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 16:223–242CrossRefPubMed 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 16:223–242CrossRefPubMed
15.
go back to reference 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 4:5110CrossRefPubMedPubMedCentral 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 4:5110CrossRefPubMedPubMedCentral
16.
go back to reference 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:e0166339CrossRefPubMedPubMedCentral 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:e0166339CrossRefPubMedPubMedCentral
17.
go back to reference 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 7:913–920CrossRefPubMed 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 7:913–920CrossRefPubMed
18.
go back to reference 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 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
19.
go back to reference 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 161:2685–2692CrossRefPubMed 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 161:2685–2692CrossRefPubMed
20.
go back to reference 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 19:89–94PubMed 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 19:89–94PubMed
21.
go back to reference 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 18:499–502PubMed 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 18:499–502PubMed
22.
go back to reference 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 269:232–236CrossRefPubMed 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 269:232–236CrossRefPubMed
23.
go back to reference Fine JP, Gray RJ (1999) A proportional hazards model for the subdistribution of a competing risk. J Am Stat Assoc 94:496–509CrossRef Fine JP, Gray RJ (1999) A proportional hazards model for the subdistribution of a competing risk. J Am Stat Assoc 94:496–509CrossRef
24.
27.
go back to reference 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 72:541–546CrossRefPubMed 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 72:541–546CrossRefPubMed
28.
go back to reference 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 109:636–641CrossRefPubMed 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 109:636–641CrossRefPubMed
29.
go back to reference 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 364:127–135CrossRefPubMedPubMedCentral 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 364:127–135CrossRefPubMedPubMedCentral
30.
go back to reference 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 13:37CrossRefPubMedPubMedCentral 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 13:37CrossRefPubMedPubMedCentral
31.
go back to reference 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 14:29CrossRefPubMedPubMedCentral 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 14:29CrossRefPubMedPubMedCentral
32.
go back to reference Matsuzawa Y, Guddeti RR, Kwon TG, Lerman LO, Lerman A (2015) Secondary prevention strategy of cardiovascular disease using endothelial function testing. Circ J 79:685–694CrossRefPubMed Matsuzawa Y, Guddeti RR, Kwon TG, Lerman LO, Lerman A (2015) Secondary prevention strategy of cardiovascular disease using endothelial function testing. Circ J 79:685–694CrossRefPubMed
33.
go back to reference Hong JB, Leonards CO, Endres M, Siegerink B, Liman TG (2016) Ankle-brachial index and recurrent stroke risk: meta-analysis. Stroke 47:317–322CrossRefPubMed Hong JB, Leonards CO, Endres M, Siegerink B, Liman TG (2016) Ankle-brachial index and recurrent stroke risk: meta-analysis. Stroke 47:317–322CrossRefPubMed
34.
go back to reference 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 38:1752–1758CrossRefPubMed 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 38:1752–1758CrossRefPubMed
35.
go back to reference 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 80:1012–1018CrossRefPubMed 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 80:1012–1018CrossRefPubMed
36.
go back to reference 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 43:3173–3178CrossRefPubMed 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 43:3173–3178CrossRefPubMed
38.
go back to reference 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 2014:138653PubMedPubMedCentral 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 2014:138653PubMedPubMedCentral
39.
go back to reference Gall SL, Dewey HM, Thrift AG (2009) Smoking cessation at 5 years after stroke in the North East Melbourne stroke incidence study. Neuroepidemiology 32:196–200CrossRefPubMed Gall SL, Dewey HM, Thrift AG (2009) Smoking cessation at 5 years after stroke in the North East Melbourne stroke incidence study. Neuroepidemiology 32:196–200CrossRefPubMed
Metadata
Title
Rheumatoid arthritis significantly increased recurrence risk after ischemic stroke/transient ischemic attack
Authors
Yih-Ru Chen
Fang-I Hsieh
Li-Ming Lien
Chaur-Jong Hu
Jiann-Shing Jeng
Giia-Sheun Peng
Sung-Chun Tang
Nai-Fang Chi
Yueh-Feng Sung
Hung-Yi Chiou
Publication date
01-08-2018
Publisher
Springer Berlin Heidelberg
Published in
Journal of Neurology / Issue 8/2018
Print ISSN: 0340-5354
Electronic ISSN: 1432-1459
DOI
https://doi.org/10.1007/s00415-018-8885-9

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