Association of Symptoms of Chronic Bronchitis and Frequent Flu-Like Illnesses With Stroke
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Association of Symptoms of Chronic Bronchitis and Frequent Flu-Like Illnesses With Stroke Armin J. Grau, MD, PhD; Michael R. Preusch, MD; Frederik Palm, MD; Christoph Lichy, MD; Heiko Becher, PhD; Florian Buggle, MD Background and Purpose—Acute and several chronic infectious diseases increase the risk of stroke. We tested the hypothesis that chronic bronchitis and frequent flu-like illnesses are independently associated with the risk of stroke or transient ischemic attack (TIA). Methods—We assessed symptoms of chronic bronchitis, frequency of flu-like illnesses, and behavior during acute febrile infection in 370 consecutive patients with ischemic or hemorrhagic stroke or TIA and 370 age- and sex-matched control subjects randomly selected from the population. Results—Cough with phlegm during ⱖ3 months per year (grade 2 symptoms of chronic bronchitis) was associated with stroke or TIA independent from smoking history, other risk factors, and school education (odds ratio [OR] 2.63, 95% confidence interval [CI] 1.17 to 5.94; P⫽0.021). There was also an independent association between frequent flu-like infections (⬎2 per yr) and stroke/TIA (OR 3.54; 95% CI 1.52 to 8.27; P⫽0.003). Simultaneous assessment of chronic bronchitis and frequent flu-like infections did not attenuate the effect of either factor. Patients reported more often than control subjects to continue to work despite febrile infection (OR 3.68, 95% CI 1.80 to 7.52, multivariate analysis). Conclusions—Our results suggest that chronic bronchitis is among those chronic infections that increase the risk of stroke. Independent from chronic bronchitis, a high frequency of flu-like illnesses may also be a stroke risk factor. Infection-related behavior may differ between stroke patients and control subjects. (Stroke. 2009;40:3206-3210.) Key Words: stroke 䡲 prevention 䡲 risk factor 䡲 infection S everal studies convincingly show that acute infection and particularly respiratory tract infection temporarily in- creases the risk of stroke.1 Common chronic infections such Methods We investigated 370 consecutive patients admitted to the Neurology Department of the University of Heidelberg for ischemic or hemor- rhagic stroke or TIA and 370 control subjects randomly selected as periodontitis or infection with Helicobacter pylori may from the general population between November 2001 and April also increase stroke risk.2 In a large cohort study, symptoms 2003. Exclusion criteria were age ⬎80 years (⬎75 years after the of chronic bronchitis independently predicted both incidence first 6 months of the study), residence outside the study area (city of and mortality of coronary heart disease.3 Data on chronic Heidelberg and the neighboring county), and inability to give informed consent. Among 385 eligible patients, 370 (96.1%) agreed respiratory infection and stroke are scarce. Two previous to study participation. All patients received a cranial CT or MRI case– control studies reported that a history of recurrent or scan, extra- and transcranial Doppler sonography, ECG, and in most chronic bronchitis is associated with stroke risk.4,5 cases transthoracic or transesophageal echocardiography and Holter Chronic bronchitis is characterized by excessive tracheo- monitoring. Ischemic stroke was defined as either a central nervous deficit lasting ⱖ24 hours without evidence for nonvascular cause or bronchial mucus production sufficient to cause cough with cerebral hemorrhage or by a new ischemic lesion on neuroimaging expectoration for at least 3 months of the year. Bronchitic (including abnormalities on diffusion-weighted images unless only inflammation predominantly consists of neutrophils and is detected after the first hours post ischemia) corresponding to acute associated with systemic inflammation. There is a continuum neurological symptoms regardless of duration of symptoms. Diag- nosis of intracerebral hemorrhage was based on neuroradiological and overlap between chronic bronchitis and chronic obstruc- evidence. TIA was diagnosed if a neurological deficit of vascular tive lung disease (COLD), emphysema, or asthma.6 origin lasted ⬍24 hours without new corresponding vascular lesion We performed a case– control study7,8 to investigate on neuroimaging. The TOAST criteria were used for further subtyp- ing cerebral ischemia.9 whether symptoms of chronic bronchitis or frequent acute From the Inhabitant Registration Administration of our area we flu-like illnesses are independently associated with the risk of received a list containing name, age, sex, and address of a random stroke or TIA. sample of 2% of all adult inhabitants aged ⱕ80 years. All inhabitants Received June 19, 2009; accepted July 10, 2009. From the Department of Neurology (A.J.G., F.P., F.B.), Klinikum der Stadt Ludwigshafen a.Rh; and the Departments of Internal Medicine III (M.R.P.), Neurology (C.L.), and Tropical Hygiene and Public Health (H.B.), University of Heidelberg, Germany. Correspondence to Armin J. Grau, MD, PhD, Department of Neurology, Klinikum der Stadt Ludwigshafen a.Rh., Bremserstr. 79, 67063 Ludwigshafen a.Rh., Germany. E-mail graua@klilu.de © 2009 American Heart Association, Inc. Stroke is available at http://stroke.ahajournals.org DOI: 10.1161/STROKEAHA.109.561019 3206 Downloaded from http://stroke.ahajournals.org/ by guest on February 3, 2015
Grau et al Chronic Bronchitis, Frequent Respiratory Infection, and Stroke Risk 3207 have to be registered there according to German law. Control Table 1. Demographic Data, Risk Factors and Previous subjects were randomly selected from this sample and matched to Diseases in Patients and Control Subjects patients one-to-one for age (⫾2 years), sex, and area of residence. Within 1 week after a patient was included the first matching subject Parameter Patients Control Subjects P Value that could be identified in the random sample was contacted by mail Age, mean y⫾SD 60.7⫾12.8 60.6⫾12.7 and thereafter by phone. Among 430 subjects who could be con- tacted by phone, 370 (86.0%) agreed to study participation. The Female sex 115/370 (31.1%) 115/370 (31.1%) Neurology Department of University of Heidelberg is the only Symptoms of chronic 63/367 (17.2%) 33/368 (9.0%) 0.001 neurological hospital in the area, and most younger patients with bronchitis (grade 1) stroke/TIA (⬍75 years) are admitted there. Therefore, the patients Symptoms of chronic 37/367 (10.1%) 18/368 (4.9%) 0.008 examined are reflective of the population of the surrounding area. All bronchitis (grade 2) subjects were interviewed by trained interviewers using a structured questionnaire. Interviews were performed face-to-face in patients Self-estimated mean and by phone in control subjects. To avoid any classification bias annual episodes of between groups, self-reported risk factors and diseases were ac- flu-like illness or cold knowledged if subjects affirmed that a physician had made the ⬍1 66 (19.4 %) 59 (16.8%) 0.36 respective diagnosis before stroke or interview. The ethics commit- 1 158 (46.5%) 186 (52.8%) 0.09 tee approved the study protocol. All subjects gave informed consent. Symptoms of chronic bronchitis were assessed by 3 questions 2 83 (24.4%) 89 (25.3%) 0.79 using the modification by Jousilahti and coworkers of the respiratory ⬎2 33 (9.7 %) 18 (5.1%) 0.021 questionnaire by Rose and Blackburn: (1) Do you usually have Behavior in febrile ⬍0.001 cough with phlegm in the mornings in the winter? (2) Do you usually have cough with phlegm during the day or at night in the winter? (3) infection‡ And do you cough like this on most days or nights as much as 3 Visit a physician 80 (22.2%) 65 (17.8%) 0.14 months each year? Positive answers in either or both of the 2 first Start self-treatment 161 (44.6%) 223 (61.4%) ⬍0.0001 questions were classified as grade-1 symptoms, positive answers in and rest the third question were classified as grade-2 symptoms of chronic bronchitis.3 Participants were furthermore asked how often they Rest without any 69 (19.1%) 57 (15.6%) 0.21 suffered from acute respiratory tract infection or flu-like illness on treatment average during the last 5 years. Acute respiratory tract infection or Continue to work 51 (14.1%) 19 (5.2%) ⬍0.0001 flu-like illness was defined as any combination of fever or shivering, Arterial hypertension 217/369 (58.8%) 151/370 (40.8%) ⬍0.0001 cough, hoarseness, running nose, or sore throat lasting ⱖ3 days. To assess infection-related behavior, subjects were asked the following Diabetes mellitus 81/369 (22.0%) 49/370 (13.2%) 0.0019 question: Imagine you develop symptoms of a flu with fever of 39°C, Hyperlipidemia 143/370 (38.7%) 114/370 (30.8%) 0.025 malaise, and arthralgia on one evening. What would you do if Previous stroke 69/370 (18.7%) 21/370 (5.7%) ⬍0.0001 symptoms have not resolved the next morning? Subjects had to select 1 of the following 4 answers: (1) I go and see a physician; (2) I take Previous TIA 74/327 (22.6%) 17/363 (4.7%) ⬍0.0001 my house medication and rest; (3) I rest and wait at least 1 further Myocardial infarction 37/370 (10.0%) 24/370 (6.5%) 0.082 day before any further action; (4) I continue as usual (eg, I go to Angina pectoris 42/352 (11.9%) 30/365 (8.2%) 0.098 work) expecting that symptoms resolve soon. Peripheral arterial 70/368 (18.9%) 45/370 (12.2%) 0.011 Statistical Analysis disease Dichotomous variables were compared using 2 test. Odds ratios and Current smoking 105/369 (28.5%) 70/370 (18.9%) 0.0023 95% confidence intervals (CI) are given for all risk factors. Condi- Previous smoking 126/337 (37.4%) 131/362 (36.2%) 0.74 tional logistic regression analysis for matched pairs was used to adjust for other variables and included all generally accepted stroke Never smoking 106/337 (31.5%) 161/362 (44.5%) 0.0004 risk factors and associated diseases (hypertension, diabetes mellitus, Alcohol consumption 0.0002 smoking, previous stroke/TIA, hyperlipidemia, coronary heart dis- Never 90 (24.4%) 57 (15.4%) 0.0022 ease) plus all those factors that were significant (P⬍0.05) in univariate analysis. For analyses of an interaction between parame- ⬍1 portion per 173 (46.9%) 215 (58.1%) ters, an interaction term was introduced into the model. Because of day lower numbers of subjects, a reduced model was used for subgroup 1 portion per day 65 (17.6%) 77 (20.8%) analyses containing only those risk factors that were significant in ⬎1 portion per 41 (11.1%) 21 (5.7%) 0.0077 multivariable analyses with all subjects. Patients with missing values day were excluded from the analyses. Data were analyzed using the software package SAS. Body mass index 199/362 (55.0%) 180/368 (48.9%) 0.10 ⬎25 Results Family history of 123/370 (33.2%) 79/370 (21.4%) 0.0003 Among the 370 patients, 244 had ischemic stroke, 76 had a stroke TIA, and 44 suffered from hemorrhagic stroke. As compared School education* 0.0050 to control subjects patients reported more often grade 1 Lower level 256 (71.3%) 219 (60.0%) symptoms (OR 2.35, 95% CI 1.44 to 3.83; P⫽0.001) and Medium level 44 (12.3%) 57 (15.6%) grade 2 symptoms (OR 2.67; 95% CI 1.37 to 5.18; P⫽0.008) Higher level 59 (16.4%) 89 (24.4%) of chronic bronchitis (Table 1). Table 1 also depicts other risk *Final school exam after 9 school years (lower level), 10 school years factors and diseases, many of which show significant differ- (medium level), or ⬎10 school years (higher level). ences between groups. After adjustment for all covariables, grade 2 symptoms of chronic bronchitis were significantly associated with stroke or TIA (OR 2.63, 95% CI 1.17 to 5.94; Downloaded from http://stroke.ahajournals.org/ by guest on February 3, 2015
3208 Stroke October 2009 Table 2. Multivariate Analysis With Symptoms of Chronic was lower in women than in men in both groups, and chronic Bronchitis and Other Variables bronchitis was associated with stroke/TIA in men but not in Odds 95% confidence women (Table 3). Risk Factor Ratio Interval P Value Symptoms of chronic bronchitis increased the odds of Chronic bronchitis 2.63 1.17–5.94 0.020 stroke/TIA independent of current or previous smoking and (Grade 2 symptoms) within the model of Table 2 current smoking and symptoms Hypertension 1.98 1.32–2.98 0.001 of chronic bronchitis did not interact with each other Diabetes mellitus 1.14 0.63–2.04 0.67 (P⫽0.89). Frequency of chronic bronchitis was highest in current smokers and lowest in never smokers among patients, Hyperlipidemia 1.23 0.81–1.87 0.33 and a similar trend was seen in control subjects (Table 3). The Previous stroke/TIA 6.29 3.36–11.8 ⬍0.0001 mean number of cigarettes currently smoked by patients Peripheral arterial 0.97 0.54–1.72 0.91 (19.4⫾11.7 per day) and control subjects (16.5⫾11.3 per disease day) was not different (P⫽0.10). Symptoms of chronic Current smoking 1.74 1.05–2.91 0.033 bronchitis tended to be associated with increased odds of Previous smoking 0.98 0.59–1.63 0.94 stroke/TIA in current smokers, previous smokers, and never Alcohol abstinence 1.81 1.06–3.10 0.031 smokers, however a significant association was only found in High alcohol 2.71 1.18–6.24 0.019 previous smokers in univariate analysis (Table 3). consumption Symptoms of chronic bronchitis increased the odds of Family history of 1.65 1.04–2.61 0.032 stroke/TIA in subjects with lower level school education in stroke univariate analysis and a strong trend was present after School education 1.53 1.01–2.33 0.046 adjustment for potential confounders, whereas no such effect ⬍10 years was present in better educated subjects (Table 3). Grade 2 symptoms of chronic bronchitis were associated with in- P⫽0.020; Table 2). Grade 1 symptoms of chronic bronchitis creased odds of ischemic stroke and of stroke/TIA attribut- were also independently correlated with stroke/TIA (OR able to large artery atherosclerosis and tended to increase the 3.11; 95% CI 1.64 to 5.91; P⫽0.0005). Effect size of odds of cardioembolic stroke/TIA (Table 3). symptoms of chronic bronchitis was not different between Addition of influenza or pneumococcal vaccination during younger and older patients. Prevalence of chronic bronchitis the last year to the model in Table 2 attenuates the risk Table 3. Symptoms (Grade 2) of Chronic Bronchitis and Risk of Stroke/TIA: Subgroup Analyses Prevalence of Chronic Bronchitis Control Odds Ratio Odds Ratio* Group of Subjects Patients Subjects (Univariate Analysis) (Multivariate Analysis) Age ⬍60 years (n⫽149) 10.1% 4.1% 3.00 (0.97–9.30) 3.02 (0.90 –10.1) Age ⱖ60 years (n⫽221) 10.1% 5.4% 2.37 (1.04–5.42) 2.24 (0.91–5.51) Women (n⫽115) 4.4% 3.5% 1.33 (0.30–5.96) 1.02 (0.21–5.06) Men (n⫽155) 12.7% 5.5% 3.11 (1.47–6.59) 3.25 (1.43–7.41) Current smokers (n⫽105) 15.2% 10.0% 1.62 (0.63–4.16) 1.78 (0.65–4.86) Prev. smokers (n⫽126) 11.2% 3.9% 3.13 (1.09–8.96) 2.66 (0.86–8.26) Never smokers (n⫽106) 5.1% 3.6% 1.55 (0.49–4.94) 1.48 (0.44–4.97) Low-level school education (n⫽256) 11.0% 5.5% 2.12 (1.05–4.27) 1.93 (0.92–4.05) Medium-/high–level school education (n⫽103) 7.8% 4.1% 1.33 (0.46–3.84) 1.06 (0.31–3.57) Etiologic subgroups Ischemic stroke (n⫽244) 11.5% 6.2% 2.30 (1.09–4.83) 2.45 (1.10–5.46) TIA (n⫽76) 5.3% 1.3% 4.00 (0.45–35.8) 3.32 (0.23–48.4) Hemorrhagic stroke (n⫽44) 12.5% 5.0% 4.99 (0.58–42.8) 8.66 (0.52–144) Etiologic subgroups of ischemic stroke/TIA Large artery atherosclerosis (n⫽130) 11.5% 5.4% 3.00 (0.97–9.3) 4.77 (1.18–19.3) Cardioembolism (n⫽63) 12.7% 1.6% 8.00 (1.00–64) 6.75 (0.76–59.9) Microangiopathy (n⫽30) 6.7% 3.3% 2.00 (0.18–22.1) 1.85 (0.09–39.9) Other etiologies (n⫽25) 4.0% 12.0% 0.33 (0.04–3.21) 0.27 (0.019–3.93) Cryptogenic (n⫽72) 8.5% 5.6% 2.00 (0.37–10.9) 1.45 (0.19–10.9) *Adjusted for arterial hypertension, current smoking, alcohol abstinence, high alcohol consumption, family history of stroke, school education. Downloaded from http://stroke.ahajournals.org/ by guest on February 3, 2015
Grau et al Chronic Bronchitis, Frequent Respiratory Infection, and Stroke Risk 3209 associated with grade 2 symptoms of chronic bronchitis to a Lower socioeconomic status may be associated with higher borderline significant level (OR 2.31; 95% CI 0.99 to 5.38). risk of respiratory infections.14 Our data suggest that chronic Symptoms of chronic bronchitis were associated with in- bronchitis may play a more important role as stroke risk creased risk of stroke/TIA during winter months (November factor in subjects with lower than in those with higher through April, n⫽261; OR 4.58; 95% CI 1.73 to 12.1) but not education levels. Less educated subjects may reside in areas significantly with those during summer months (n⫽106; OR with more disadvantageous living conditions (eg, with higher 2.39; 95% CI 0.53 to 10.8) in multivariate analysis. air pollution). Air pollution is an important risk factor for Patients reported more often than control subjects to suffer chronic bronchitis,6 and an association with stroke was also on average from ⬎2 episodes of flu-like illnesses annually shown recently.15 during the last 5 years (OR 2.14; 95% CI 1.14 to 4.04; Symptoms of chronic bronchitis were independently asso- P⫽0.019; Table 1). High frequency of flu-like illnesses was ciated with ischemic stroke but not with TIA and intracere- independently associated with the odds of stroke/TIA after bral hemorrhage who both represented smaller groups of adjustment for the covariables in Table 2 (OR 3.54; 95% CI 1.52 subjects. In general, subgroup analyses have to be viewed to 8.27; P⫽0.003). Chronic bronchitis (OR 2.83; 95% CI 1.16 to with caution because of insufficient statistical power and only 6.91) and frequent flu-like illnesses (OR 3.22; 95% CI 1.39 to possess hypothesis-generating character. A significant asso- 7.49) were independently associated with stroke/TIA when ciation was found for stroke/TIA attributable to large artery simultaneously entered in the model in Table 2. atherosclerosis. Atherosclerosis is an inflammatory disease, The self-estimated reaction to symptoms of febrile infec- and chronic inflammatory conditions (eg, rheumatoid arthri- tion was different between groups (Table 1). More patients tis) may promote atherogenesis and its complications.16 than control subjects reported that they would continue as Proinflammatory changes as in chronic bronchitis can cause a usual, including continuation of work despite high fever (OR procoagulant state, thereby potentially increasing the risk of 2.68, 95% CI 1.59 to 4.55), and such behavioral pattern thromboembolism (eg, cardioembolism and increased proteo- remained associated with stroke/TIA in multivariate analysis lytic activity) and potentially augmenting the risk of injury to (OR 3.68, 95% CI 1.80 to 7.52). In contrast, less patients the vascular wall and consecutive hemorrhage.2 However, reported to use self-medication and to rest (OR 0.48, 95% CI significant associations with cardioembolism and intracere- 0.35 to 0.66) and such self-reported attitude was also inde- bral hemorrhage could not be shown in our study. pendently associated with reduced odds of stroke/TIA (0.46; Acute respiratory infection transiently increases the risk of 95% CI 0.30 to 0.68). ischemic stroke.1 Therefore, a higher number of infectious episodes could augment the risk of cerebral ischemia. In our Discussion study, high frequency of respiratory infections was indepen- Our results support the hypothesis that chronic bronchial dently associated with stroke/TIA. These results are based on inflammation is a risk factor for stroke. This finding strength- subjects’ self-estimation and were not correlated with medi- ens the concept that chronic infectious diseases of different cal records. However, uncomplicated respiratory infection origin may increase stroke risk. does often not prompt a doctoral visit; therefore, verification The diagnosis of chronic bronchitis is made by history6 and may be difficult. To the best of our knowledge, an association commonly applied diagnostic criteria were used in our study. between higher rates of infection and stroke risk has not been Cough and sputum are nonspecific symptoms that can also reported before. The cause of a higher rate of infections result from other airway diseases or from cardiac disease. among patients is unknown; living conditions (eg, poorer Therefore, we use the term “symptoms of chronic bronchitis” housing), environmental factors (eg, higher air pollution), in accordance with previous epidemiological studies.3 Several lifestyle factors (eg, inappropriate clothing), or genetically confounders could explain the association between chronic determined higher susceptibility to infection are among po- bronchitis and stroke, particularly smoking and low socioeco- tential explanations. nomic status. As shown previously,10 prevalence of chronic Acute respiratory infections are a risk factor for chronic bronchitis varied along smoking status and was highest in bronchitis, and vice-versa patients with chronic bronchitis current smokers and lowest in never smokers in both groups. more often suffer from acute exacerbations of upper airway Symptoms of chronic bronchitis remained associated with disease. Therefore, high frequency of respiratory infections stroke/TIA when smoking status was adjusted for. Smoking could influence the association between chronic bronchitis and chronic obstructive airway disease both independently and stroke. However, frequent infections and chronic bron- increase the level of inflammatory markers such as C-reactive chitis remained both significantly associated with stroke/TIA protein,11 which is also a predictor of stroke.2 A genetically in a combined model indicating an independent influence of determined strong inflammatory response appears to be both inflammatory conditions. linked with both stroke and COLD and also influences the The role of infections as vascular risk factor could be association between smoking and stroke.12,13 We had hypoth- influenced by the way subjects react to emerging infections. esized that chronic bronchitis and smoking interact with each Furthermore, reaction to infections may reflect subjects’ other in the sense that those current or previous smokers who health-related lifestyle. We found that more stroke patients react with stronger bronchial inflammation and develop would continue to work and fewer stroke patients would use symptoms of chronic bronchitis may have a particularly high self-medication in acute febrile illness. Self-medication risk of stroke; however, our data do not support such would not include antibiotics, as those require prescription in interaction. Germany. If such self-report is not biased by the experience Downloaded from http://stroke.ahajournals.org/ by guest on February 3, 2015
3210 Stroke October 2009 of stroke and in fact reflects prestroke behavior, it may 3. Jousilahti P, Vartiainen E, Tuomilehto J, Puska P. Symptoms of chronic represent an attitude in stroke patients that reflects greater bronchitis and the risk of coronary disease. Lancet. 1996;348:567–572. 4. Grau AJ, Buggle F, Ziegler C, Schwarz W, Meuser J, Tasman AJ, Bühler ignorance regarding health issues and less confidence in their A, Benesch C, Becher H, Hacke W. Association between acute cerebro- own medical competence but possibly also more socioeco- vascular ischemia and chronic and recurrent infection. Stroke. 1997;28: nomic pressure (eg, fear of unemployment). 1724 –1729. 5. Piñol-Ripoll G, de la Puerta I, Santos S, Purroy F, Mostacero E. Chronic Patients and control subjects originate from the same bronchitis and acute infections as new risk factors for ischemic stroke and source population, and control subjects would have become the lack of protection offered by the influenza vaccination. Cerebrovasc inpatients in the Neurology department with high probability Dis. 2008;26:339 –347. 6. Honig EG, Ingram RH Jr. Chronic bronchitis, emphysema, and airways if they suffered a stroke, constituting the comparability obstruction. In: Fauci AS, Braunwald E, Isselbacher KJ, Wilson JD, between both groups. But several limitations exist regarding Martin JB, Kasper DL, Hauser SL, Longo DL (eds). Harrison’s Prin- our study. We had to exclude severely disabled patients, ciples of Internal Medicine. 14th edition. New York: McGraw-Hill; 1998:1451–1460. therefore results cannot be generalized to very severe and 7. Grau AJ, Fischer B, Barth C, Ling P, Lichy C, Buggle F. Influenza lethal strokes. 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Association of Symptoms of Chronic Bronchitis and Frequent Flu-Like Illnesses With Stroke Armin J. Grau, Michael R. Preusch, Frederik Palm, Christoph Lichy, Heiko Becher and Florian Buggle Stroke. 2009;40:3206-3210; originally published online August 13, 2009; doi: 10.1161/STROKEAHA.109.561019 Stroke is published by the American Heart Association, 7272 Greenville Avenue, Dallas, TX 75231 Copyright © 2009 American Heart Association, Inc. All rights reserved. Print ISSN: 0039-2499. Online ISSN: 1524-4628 The online version of this article, along with updated information and services, is located on the World Wide Web at: http://stroke.ahajournals.org/content/40/10/3206 Permissions: Requests for permissions to reproduce figures, tables, or portions of articles originally published in Stroke can be obtained via RightsLink, a service of the Copyright Clearance Center, not the Editorial Office. Once the online version of the published article for which permission is being requested is located, click Request Permissions in the middle column of the Web page under Services. Further information about this process is available in the Permissions and Rights Question and Answer document. Reprints: Information about reprints can be found online at: http://www.lww.com/reprints Subscriptions: Information about subscribing to Stroke is online at: http://stroke.ahajournals.org//subscriptions/ Downloaded from http://stroke.ahajournals.org/ by guest on February 3, 2015
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