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Awareness of Stroke Risk Factors and Warning Signs in Nigerian Adolescents Compared with Adults
Awareness of Stroke Risk Factors and Warning Signs in Nigerian Adolescents Compared with Adults Morenikeji A. Komolafe, MBBS, FWACP,*† Adebimpe O. Obembe, PhD,‡ Matthew O. Olaogun, MS, FNSP,‡ Ayoade M. Adebiyi, MBChB,† Theresa Ugalahi, MBBS,† Olumuyiwa Dada, MBBS,† Alfred Kanu, MBBS,† Olubunmi C. Adebiyi, MBChB,† Folarin Akilo, MBChB,† Bukola Ogunkoya, MBChB,† and Bimbo Fawale, MBBS*†
Background: Stroke, a significant health problem affecting adults, is increasing among younger age groups, particularly because of changing lifestyles. The aim of the study was to compare the awareness of stroke risk factors and warning signs among students and teachers in selected secondary schools in Osun State, Nigeria. Methods: This was a cross-sectional survey involving 703 (589 students and 114 teachers) respondents in selected secondary schools in Osun, Nigeria. Information on the awareness of stroke risk factors and warning signs was collected with the aid of a structured questionnaire. Results: Hypertension (69.4%) was the most commonly identified stroke risk factor, with more teachers (79.8%) identifying correctly than the students (67.4%). Weakness (51.9%) was the most commonly identified warning sign of stroke with more students (53.8%) identifying correctly than the teachers (42.1%). There were significant differences in the awareness of some risk factors (age, obesity, family history, alcohol use, diet, transient ischemic attack, and hyperlipidemia) and warning signs (dizziness, weakness, and vision problems) between students and teachers. Predictors for adequate awareness of risk factors were being a teacher, not being obese and being hypertensive, whereas predictors for adequate awareness of warning signs were stroke in the family and being hypertensive. Conclusions: There was inadequate awareness of risk factors and warning signs among the respondents with students having better awareness of warning signs and teachers having better awareness of risk factors. Stroke campaigns should emphasize stroke risk factors particularly among adolescents and warning signs in adults. The use of media, particularly television, is recommended. Key Words: Stroke—risk factors—awareness—warning signs—adolescents—Nigeria. Ó 2015 by National Stroke Association
From the *Department of Medicine, Faculty of Clinical Sciences, College of Health Sciences, Obafemi Awolowo University, Ile-Ife, Osun State; †Neurology Unit, Department of Medicine, Obafemi Awolowo University Teaching Hospitals Complex, Ile-Ife, Osun State; and ‡Department of Medical Rehabilitation, Faculty of Basic Medical Sciences, College of Health Sciences, Obafemi Awolowo University, Ile-Ife, Osun State, Nigeria. Received August 13, 2014; revision received November 5, 2014; accepted November 14, 2014.
Address correspondence to Morenikeji Komolafe, MBBS, FWACP, Department of Medicine, Faculty of Clinical Sciences, College of Health Sciences, Obafemi Awolowo University, Ile-Ife, Osun State, Nigeria. E-mail: [email protected]. 1052-3057/$ - see front matter Ó 2015 by National Stroke Association http://dx.doi.org/10.1016/j.jstrokecerebrovasdis.2014.11.013
Journal of Stroke and Cerebrovascular Diseases, Vol. 24, No. 3 (March), 2015: pp 687-693
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Introduction The burden of stroke is increasing in developing countries, with huge financial costs on the individual, family, and the health care system.1 In Nigeria, stroke is the leading cause of death and disability, and it is responsible for up to half of neurologic admissions and 5%-17% of medical deaths.2 Previous studies have shown that lack of knowledge about stroke warning signs may contribute to late presentation to the hospital.3 Nigerians with hypertension or diabetes have been reported to have poor awareness of stroke warning signs.4,5 Other Nigeria studies also found similar gaps in knowledge among university students6 and hospital workers.7 About 15% of all ischemic strokes occur in adolescents and young adults.8 Studies carried out among adolescents in developed countries regarding knowledge of cardiovascular diseases (CVDs) show that they lack knowledge of the risk factors and do not perceive themselves to be at a risk of CVD.9,10 Apart from the vascular risk factors, sickle cell disease11 is also a common cause of stroke in the adolescent age group; hence, it is important to assess level of awareness of risk factors and warning signs in them. There has been no previous study on knowledge of stroke risk factors and warning signs among adolescents; hence, we carried out this study as part of the World Stroke Day 2013 campaign in Osun State, Nigeria.
Aims The aims of the study were to assess the level of awareness of stroke risk factors and warning signs in secondary school students and teachers and to compare the level of awareness between the 2 groups.
Materials and Methods This was a cross-sectional survey conducted in 5 secondary schools in Ile-Ife and Ilesa, 2 towns in the state of Osun, southwest of Nigeria. The protocol was approved by the Health Research Ethics Committee of the Institute of Public Health, Obafemi Awolowo University. The questionnaire was administered to students in their respective classrooms and to teachers in the staff rooms/offices. Informed consent were sought and obtained from all the respondents. Respondents were informed about the purpose and protocol of the study before filling the questionnaires, which were collected immediately. Data were collected from 5 schools, 4 in Ile-Ife, and 1 from Ilesha, State of Osun, Nigeria. All the teachers were included, whereas a simple random sample was used to select students from both Junior Secondary School (JSS) and Senior Secondary School (SSS) classes. The questionnaire used in this survey was developed to assess the recognition of stroke risk factors and early
warning signs. It had been previously used and validated by previous workers.6 The questionnaire used is available as a Supplemental data. Basic demographic information collected include sex, age, occupational status (student, teacher), educational status (eg, tertiary, postgraduate), class of students (JSSs 1-3 and SSSs 1-3), history of smoking (past and current smokers), family history of heart disease, and histories of diabetes, hypertension, and stroke. The study was conducted over a period of 4 weeks (October 7 to November 4, 2013). List of important warning signs of stroke by the American Stroke Association, American National Stroke Association, and National Institute of Neurological Disorders and Stroke was used in this study. Respondents were asked to indicate if they recognized any of 7 warning signs of stroke and any of 11 risk factors of stroke. Adequate level of awareness was defined as identifying at least half of the listed risk factors (7) and warning signs (4) correctly. Respondents were also asked what they would do first, if someone were having a stroke near them. The authors visited each of the schools a week before data collection to identify a convenient time in the school timetable to administer questionnaire and assess weight and height. Students who filled the questionnaire were asked to assemble at the sick bay at break time where the measurements were taken. The measurements for the teachers were taken in the staff rooms. The body weight in kilograms was assessed with a bathroom scale and height in meters measured with a tape measure placed against a wall. The body mass index was then calculated. Descriptive statistics of frequency and percentage were used to summarize data. Inferential statistics of the Mann–Whitney U test was used to compare the awareness between groups, and the Kruskal–Wallis test was used to compare awareness among groups. Odds ratio analysis was done to determine the predictors of awareness. Alpha level was set at P less than .05. All statistical procedures were performed with the Statistical Package for Social Sciences, version 20.0 (SPSS, Chicago, IL).
Results A total of 703 respondents (589 students and 114 teachers, 315 men and 388 women) were involved in this survey. The mean age of the students was 13.9 6 2, whereas most teachers (87.7%) were between 20 and 50 years. The distribution of the characteristics of respondents is listed in Table 1. The response rate was 95.6% for the teachers and 94.1% for the students. Hypertension (69.4%) was the most commonly identified risk factor, and hyperlipidemia (21.1%) was the least commonly identified (Table 2). There were significant differences in the awareness of some stroke risk factors (smoking, obesity, family history of stroke, alcohol use, diet, transient ischemic attack, and hyperlipidemia) with
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Table 1. Characteristics of respondents Variable Age (y) 10-19 20-30 31-40 41-50 .50 Sex Male Female Educational level (teachers) Tertiary Postgraduate Educational level (students) JSS 1 JSS 2 JSS 3 SSS 1 SSS 2 SSS 3 Family history of stroke Family history of heart disease Smoking history Past smokers Current smokers History of stroke History of diabetes History of hypertension Income (Naira) 10,000-19,000 20,000-29,000 30,0000-50,000 .50,000 BMI (kg/m2) Underweight (,18.5) Normal (18.5-24.9) Overweight (25-29.9) Obese (.30)
Overall (N 5 703)
Students (n 5 589)
Teachers (n 5 114) 12 (10.5) 43 (37) 36 (31.6) 21 (18.4) 2 (1.8)
315 (44.8) 388 (55.2)
264 (44.8) 325 (55.2)
51 (44.7) 63 (55.3) 83 (72.8) 31 (27.2)
48 (6.8) 26 (3.7)
24 (4.1) 111 (18.8) 206 (35) 71 (12.1) 59 (10) 118 (20) 40 (6.8) 25 (4.2)
8 (7) 1 (.9)
7 (1) 7 (1) 1 (.9) 2 (1.8) 13 (11.4)
4 (.7) 6 (1) — — —
3 (2.6) 1 (.9) 1 (.9) 2 (1.8) 13 (11.4)
4 (3.5) 10 (8.8) 38 (33.3) 62 (54.4)
— — — —
4 (3.5) 10 (8.8) 38 (33.3) 62 (54.4)
246 (35) 373 (53.1) 45 (6.4) 39 (5.5)
240 (40.7) 327 (55.5) 16 (2.7) 6 (1)
6 (5.3) 46 (40.4) 29 (25.4) 33 (28.9)
Abbreviations: BMI, body mass index; JSS, Junior Secondary School; SSS, Senior Secondary School.
the teachers having better awareness in 4 (obesity, family history of stroke, alcohol use, diet). Weakness (51.9%) was the most commonly recognized warning sign, whereas shortness of breath was the least commonly identified. There were significant differences in the awareness of 3 (dizziness, weakness, and visual problem) of the 8 warning signs listed: students had better awareness of 2 warning signs, weakness and visual problem (Table 3). There were significant differences in the awareness of some risk factors (hypertension, stress, and alcohol use) and 3 warning signs (slurred speech, vision problems, and shortness of breath) among students in different classes (Table 3). Students in SSSs had better knowledge about some risk factors (hypertension, stress, and alcohol
use) and warning signs (slurred speech, vision problem and shortness of breath) than those in JSSs. The level of education of teachers did not affect the level of awareness as there was no statistically significant difference in the awareness of all risk factors and warning signs among teachers with tertiary and postgraduate education (Table 4). The age of the teachers did not affect the level of awareness of all the risk factors (P 5.80) or the warning signs (P 5 .39). There was no difference among men and women regarding the level of awareness of stroke risk factors; however, female teachers had better knowledge of 2 warning signs, headache and shortness of breath (Table 2). The field of study of the teachers was not included in the questionnaires.
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Table 2. Teachers awareness of stroke risk factors and warning signs and gender Response Risk factors Age Hypertension Stress Cholesterol Smoking Obesity Lack of exercise Family history of stroke Diabetes Alcohol use Diet Increased salt intake TIA Hyperlipidemia Zero risk factors $7 Risk factors All risk factors Warning signs Slurred speech Dizziness Numbness Weakness Headache Vision problem Difficulty understanding Shortness of breath Zero warning signs All warning signs
Overall, n (%), n 5 114
Males, n (%), n 5 51
Females, n (%), n 5 63
P value
50 (43.9) 91 (79.8) 75 (65.8) 58 (50.9) 56 (49.6) 56 (49.1) 65 (57.0) 60 (52.6) 54 (47.4) 60 (52.6) 113 (99.1) 37 (32.5) 54 (47.8) 26 (22.8) 15 (13.2) 50 (43.9) 109 (95.6)
25 (49.0) 41 (80.4) 32 (62.7) 27 (52.9) 25 (49.0) 24 (47.1) 26 (51.0) 27 (52.9) 22 (43.1) 26 (51.0) 51 (100) 17 (33.3) 21 (41.2) 11 (21.6) 8 (15.7) 23 (45.1) 47 (92.2)
25 (39.7) 50 (54.9) 43 (68.3) 31 (49.2) 31 (50.0) 32 (50.8) 39 (61.9) 33 (52.4) 32 (50.8) 34 (54.0) 62 (98.4) 20 (31.7) 33 (53.2) 15 (23.8) 7 (11.1) 27 (42.9) 62 (98.4)
.318 .892 .538 .692 .917 .692 .241 .953 .416 .751 .336 .857 .202 .777 .472 .811 .098
57 (50.0) 31 (27.2) 38 (33.3) 48 (42.1) 42 (36.8) 23 (20.2) 38 (33.3) 37 (32.5) 27 (23.7) 4 (3.5)
23 (45.1) 15 (29.4) 15 (29.4) 19 (37.3) 13 (25.5) 11 (21.6) 11 (21.6) 16 (31.4) 11 (21.6) 2 (3.9)
34 (54.0) 16 (25.4) 23 (36.5) 29 (46.0) 29 (46.0) 12 (19.0) 27 (42.9) 21 (33.3) 16 (25.4) 2 (3.2)
.346 .632 .424 .345 .024 .739 .017 .824 .633 .951
Being a teacher, having a history of hypertension, and not being obese were significant predictors of knowing at least half of the listed risk factors. Although family history of stroke and having a history of hypertension were significant predictors of knowing at least half of the listed warning signs (Table 5). Four hundred ninety-three (41.4%) respondents indicated that they would take the person to the hospital, with the percentage of teachers higher than that of students (Table 6). The television was the most common source of information (72.8%), followed by literature (magazines and newspaper, 58.3%). Having seen family (11.7%) or friend (13.9%) with stroke were the least popular sources of information among the students (Table 7). The sources of information differed among students and teachers with the former getting information from literature and the Internet and the later from the doctor; 12 teachers (10.5%) obtained information about stroke from more than 2 sources compared with 43 (7.3%) students.
Discussion The results of this study showed that hypertension (69.4%) was the most correctly identified stroke risk
factor, whereas weakness of 1 side of the body (51.9%) was the most correctly identified warning sign among the students and teachers in selected secondary schools in Osun State. Previous studies have reported hypertension as the most commonly identified risk factor6,7,12 and weakness as the most commonly identified warning sign5-7 among Nigerian adults. Our findings among the teachers that the level of education and gender did not affect the level of awareness of stroke risk factors is contrary to the findings from previous Nigerian studies6,13 that men with higher education had better knowledge about risk factors and warning signs compared with women with lower education. This might be because the level of education among the teachers is better than that of the population as all of them had at least tertiary education. However, we could not assess the effect of field of study of the teachers on the levels of awareness as this information was not included in the questionnaire. Students, who were mostly (98.1%) adolescents (mean age 5 13.9 6 2 years) had better awareness of some warning signs than teachers who were all adults (.20 years), whereas teachers had better knowledge of risk factors than students. The occurrence of stroke has been reported
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Table 3. Students’ awareness of stroke risk factors and warning signs according to class
Risk factors Age Hypertension Stress Cholesterol Smoking Obesity Lack of exercise Family history Diabetes Alcohol use Diet Increased salt intake TIA Hyperlipidemia Warning signs Slurred speech Dizziness Numbness Weakness Headache Vision problem Difficulty understanding Shortness of breath
JSS, n (%) (n 5 341)
SSS, n (%) (n 5 248)
P value
102 (29.9) 198 (58.1) 178 (52.2) 84 (24.6) 166 (48.7) 85 (24.9) 140 (41.1) 62 (18.2) 79 (23.2) 112 (32.8) 102 (29.9) 79 (23.2)
89 (35.9) 199 (80.2) 162 (65.3) 87 (35.1) 140 (56.5) 73 (29.4) 104 (41.9) 47 (19.0) 60 (24.2) 113 (45.6) 66 (26.6) 58 (23.4)
.127 .000 .001 .006 .062 .224 .831 .812 .777 .002 .380 .950
71 (20.8) 70 (20.5)
59 (23.8) 60 (24.2)
.392 .291
85 (24.9) 86 (25.2) 80 (23.5) 175 (51.3) 101 (29.6) 76 (22.3) 105 (30.8)
102 (41.1) 61 (24.8) 67 (27.0) 142 (57.3) 67 (27.4) 78 (31.5) 93 (37.5)
.000 .863 .326 .153 .560 .013 .089
70 (20.5)
69 (27.8)
.040
Abbreviations: JSS, Junior Secondary School; SSS, Senior Secondary School; TIA, transient ischemic attack.
to increase with age.14 Because stroke occurs mostly in adults, it is expected of adults to have better awareness of stroke warning signs. Adequate information about the warning signs of stroke may reduce the median presentation time of 3 days with a range of 1-90 days reported among Nigerians.13 The phase that the most improvement can be achieved is the time from symptom recognition to the decision to seek medical care.15 When a stroke occurs, the time of presentation to the hospital is important in its management as delays often result in poor outcome.6 Rapid access to medical care is an important predictor of treatment and rehabilitation outcome. The findings in our study, which show a low level of stroke warning signs, brings to fore the fact that Nigerian adults urgently need more information about stroke warning signs. This will enable them to recognize the symptoms when they are having a stroke or when a stroke is occurring near them. Stroke education campaign should also emphasize the importance of early presentation for medical care.
Table 4. Teachers’ awareness of stroke risk factors and warning signs by educational levels Tertiary, n (%) (n 5 83) Risk factors Age Hypertension Stress Cholesterol Smoking Obesity Lack of exercise Family history Diabetes Alcohol use Diet Increased salt intake TIA Hyperlipidemia Warning signs Slurred speech Dizziness Numbness Weakness Headache Vision problem Difficulty understanding Shortness of breath
Postgraduate, N (%) (n 5 31) P value
32 (38.6) 66 (79.5) 48 (66.3) 40 (48.2) 43 (51.8) 47 (56.6) 43 (51.8) 51 (61.4) 41 (49.4) 36 (43.4) 28 (33.7) 39 (47.0)
18 (58.1) 25 (80.6) 20 (64.5) 16 (51.6) 13 (41.9) 18 (58.1) 17 (54.8) 19 (61.3) 19 (61.3) 13 (41.9) 9 (29) 15 (48.4)
.062 .894 .861 .745 .348 .890 .773 .988 .258 .890 .424 .105
23 (27.7) 17 (20.5)
3 (9.7) 4 (12.9)
.424 .961
41 (49.4) 22 (26.5) 25 (30.1) 34 (41.0) 32 (38.6) 16 (19.3) 29 (34.9)
16 (51.6) 9 (29) 13 (41.9) 14 (45.2) 10 (32.3) 7 (22.6) 9 (29)
.833 .787 .234 .686 .535 .696 .552
28 (33.7)
9 (29)
.633
Abbreviations: TIA, transient ischemic attack.
The results of our study also showed that teachers had better awareness of stroke risk factors than students. Emerging data have raised public health concerns about the increasing prevalence of traditional vascular risk factors in young individuals and their potential role in
Table 5. Significant predictors of knowing at least half of the listed stroke warning signs or risk factors Factor Warning signs (#4) Stroke in family History of hypertension Risk factors (#7) Not obese Teacher History of hypertension
OR
95% CI
P value
.435 .188
.218-.868 .054-.657
.015 .007
2.339 .338 .088
1.221-4.479 .225-.510 .071-.706
.008 .000 .004
Abbreviations: CI, confidence interval; OR, odds ratio.
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Table 6. Actions to be taken by respondents when a stroke occurs near them Action to be taken
Students (n 5 589), n (%)
Teachers (n 5 114), n (%)
Total (N 5 703), n (%)
Call a doctor Take the person to the hospital Call family, friends, or neighbors Seek spiritual attention Do nothing
183 (31.1) 230 (39) 32 (5.4) 19 (3.2) 7 (1.2)
16 (14) 61 (53.5) 1 (.9) 1 (.9) —
199 (28.3) 291 (41.4) 33 (4.7) 20 (2.8) 7 (1)
increasing the risk of ischemic stroke, stroke recurrence, and poststroke mortality.8 A previous study9 has reported that adolescents in their study population were not aware of the high prevalence and mortality of CVD and did not perceive themselves at risk for CVD. Singhal et al7 reported that between 532,000 and 852,000 people aged 18 to 44 years in the United States have had a stroke. Hospital discharges for stroke in the United States from 1995 to 1996 and 2007 to 2008 among patients aged 15 to 44 years increased by 23%-53%, depending on age and gender of the group. Although the causes and risk factors for stroke in the young are often rare or undetermined, young adults with stroke also have a high burden of known cardiovascular risk factors, which include hypertension, diabetes, obesity, and substance abuse.16 Typically, CVDs occur in middle age or later, but risk factors are determined to a great extent by behaviors learnt in childhood and continued into adulthood, such as dietary habits and smoking.17 More emphasis should be placed on stroke education (adequate and appropriate information) about the risk factors targeting young people in secondary schools. This is to prevent the occurrence of avoidable risk factors among adolescents who are the majority among students in Nigerian secondary schools. Stroke educational programs should also entail information about prevention of stroke, which include control of established stroke risk factors, such as hypertension, obesity, diabetes, and smoking.
Stroke education campaigns targeted at high school youths could yield favorable results. Promotion of healthy lifestyle habits could be implemented during a crucial period by targeting this younger age group, that is, a time in which CVD risk factors and atherosclerotic plaques are in the early stages of development, and cardioprotective practices can be ingrained.18 Educational intervention is needed to raise awareness about risk factors in the adolescent population.10 Many respondents (41.4%) indicated that they would take the person having a stroke near them to the hospital. The television was the most common source of information for both students and teachers. This is followed by literature among the students (59.4%) and health practitioners (doctors) among the teachers (61.4%). The finding that majority of teachers had information from their doctors shows that there should be educational program for medical practitioners and primary care physicians, focused on the need to screen for cardiovascular risk factors in all adults presenting to health care facilities and also to give information on the need to adopt a healthy life style and how to recognize stroke warning signs. Also, awareness programs for students should focus on giving adequate and appropriate information on stroke in form of literature or on social media such as the Internet. The predictive factors for awareness included a family history of stroke, hypertension, and not being obese. Obese persons in our study were less aware of important
Table 7. Respondents’ sources of information about stroke Source of information*
Students (n 5 589), n (%)
Teachers (n 5 114), n (%)
Total (N 5 703), n (%)
Television Radio Literature Health practitioners Stroke campaigns Internet Public library Relatives Others Learned in school Seen stroke in family Seen a friend with stroke
426 (72.3) 311 (52.8) 350 (59.4) 269 (45) 199 (33.8) 238 (40.4) 132 (22.4) 161 (27.3) 3 (.5) 228 (38.7) 82 (13.9) 98 (16.6)
86 (75.4) 64 (56.1) 60 (32.6) 70 (61.4) 37 (32.5) 37 (32.5) 19 (16.7) 29 (25.4) — — — —
512 (72.8) 375 (53.3) 410 (58.3) 339 (48.2) 236 (33.6) 275 (39.1) 151 (21.5) 190 (27) 3 (.4) 228 (32.4) 82 (11.7) 98 (13.9)
*Multiple responses allowed.
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stroke risk factors and warning signs. Generally, obesity in the southern part of Nigeria is considered as a sign of good living. This possibly might be an explanation for the lower level of awareness among obese persons in this study. There is a need for stroke educational programs emphasizing the need for regular screening for obesity, especially for people who are overweight. Adequate information about stroke risk factors and warning signs should also be given to obese persons. Also, personal risk factors should be assessed as part of stroke awareness programs. This study concluded that there was inadequate awareness of stroke risk factors and warning signs among the respondents. Students had better awareness of warning signs than teachers, whereas teachers had better awareness of risk factors than the students. There is a need for more stroke education with emphasis on adequate information about stroke risk factors to prevent occurrence especially among students and warning signs especially among at-risk adults so that they can act promptly and appropriately by seeking immediate medical attention.
Supplementary Data Supplementary data related to this article can be found at http://dx.doi.org/10.1016/j.jstrokecerebrovas dis.2014.11.013.
References 1. Truelsen T. Stroke incidence studies in Africa. Lancet Neurol 2010;9:755-757. 2. Ojinni FI, Danesi MA. Pattern of neurological admissions at the Lagos University Teaching Hospital. Nig J Clin Prac 2003;5:38-41. 3. Pandian JD, Kalra G, Jaison A, et al. Public awareness of warning symptoms, risk factors, and treatment of stroke in northwest India. Stroke 2005;36:644. 4. Ajayi AO, Ojo OO. Knowledge and perception of stroke among at risk medical out-patients in a tertiary health institution in Nigeria. Ann Afr Med 2007;6:51-53. 5. Wahab KW, Okokhere PO, Ugheoke AJ, et al. Awareness of warning signs among suburban Nigerians at high risk for stroke is poor: a cross-sectional study. BMC Neurol 2008;8:18.
693 6. Obembe AO, Olaogun MO, Bamikole AA, et al. Awareness of stroke risk factors and warning signs in a Nigeria university. J Stroke Cerebrovasc Dis 2014;17: 749-758. 7. Akinyemi RO, Ogah OS, Ogundipe RF, et al. Knowledge and perception of stroke amongst hospital workers in an African community. Eur J Neurol 2009; 16:998-1003. 8. Singhal AB, Biller J, Elkind MS, et al. Recognition and management of stroke in young adults and adolescents. Neurology 2013;81:1089-1097. 9. Lynch EB, Liu K, Kiefe CI, et al. Cardiovascular disease risk factor knowledge in young adults and 10-year change in risk factors. The Coronary Artery Risk Development in Young Adults (CARDIA) study. Am J Epidemiol 2006;164:1171-1179. 10. Vanhecke TE, Miller WM, Franklin BA, et al. Awareness, knowledge and perception of heart disease among adolescents. Eur J Cardiovasc Prev Rehabil 2006;13: 718-723. 11. Lagunju IA, Brown BJ. Adverse neurological outcomes in Nigerian children with sickle cell disease. Int J Hematol 2012;96:710-718. 12. Obiabo Y. Stroke awareness among adults in SouthSouth, Nigeria. Delta State. Neurology 2013;80:P03.166 (Meeting Abstracts 1). 13. Wahab KW, Sani MU, Samaila AA, et al. Stroke at a tertiary medical institution in northern Nigeria: patients’ profile and predictors of outcome. Sahel Med J 2007; 10:6-10. 14. Desalu OO, Wahab KW, Fawale B, et al. A review of stroke admissions at a tertiary hospital in rural Southwestern Nigeria. Ann Afr Med 2011;10:80-85. 15. Moser DK, Kimble LP, Alberts MJ, et al. Reducing delay in seeking treatment by patients with acute coronary syndrome and stroke. A scientific statement from the American Heart Association Council on cardiovascular nursing and stroke council. Circulation 2006; 114:168-182. 16. Sultan S, Elkind MS. The growing problem of stroke among young adults. Curr Cardiol Rep 2013; 15:421. 17. Yadav KD, Wagle RR. Knowledge and attitude regarding major risk factors of cardiovascular diseases among 15-19 year old students of Kathmandu District. Health Prospect 2012;11:7-10. 18. Hayman LL, Williams CL, Daniels SR, et al. Cardiovascular health promotion in the schools. Circulation 2004; 110:2266-2275.
Background: Stroke, a significant health problem affecting adults, is increasing among younger age groups, particularly because of changing lifestyles. The aim of the study was to compare the awareness of stroke risk factors and warning signs among students and teachers in selected secondary schools in Osun State, Nigeria. Methods: This was a cross-sectional survey involving 703 (589 students and 114 teachers) respondents in selected secondary schools in Osun, Nigeria. Information on the awareness of stroke risk factors and warning signs was collected with the aid of a structured questionnaire. Results: Hypertension (69.4%) was the most commonly identified stroke risk factor, with more teachers (79.8%) identifying correctly than the students (67.4%). Weakness (51.9%) was the most commonly identified warning sign of stroke with more students (53.8%) identifying correctly than the teachers (42.1%). There were significant differences in the awareness of some risk factors (age, obesity, family history, alcohol use, diet, transient ischemic attack, and hyperlipidemia) and warning signs (dizziness, weakness, and vision problems) between students and teachers. Predictors for adequate awareness of risk factors were being a teacher, not being obese and being hypertensive, whereas predictors for adequate awareness of warning signs were stroke in the family and being hypertensive. Conclusions: There was inadequate awareness of risk factors and warning signs among the respondents with students having better awareness of warning signs and teachers having better awareness of risk factors. Stroke campaigns should emphasize stroke risk factors particularly among adolescents and warning signs in adults. The use of media, particularly television, is recommended. Key Words: Stroke—risk factors—awareness—warning signs—adolescents—Nigeria. Ó 2015 by National Stroke Association
From the *Department of Medicine, Faculty of Clinical Sciences, College of Health Sciences, Obafemi Awolowo University, Ile-Ife, Osun State; †Neurology Unit, Department of Medicine, Obafemi Awolowo University Teaching Hospitals Complex, Ile-Ife, Osun State; and ‡Department of Medical Rehabilitation, Faculty of Basic Medical Sciences, College of Health Sciences, Obafemi Awolowo University, Ile-Ife, Osun State, Nigeria. Received August 13, 2014; revision received November 5, 2014; accepted November 14, 2014.
Address correspondence to Morenikeji Komolafe, MBBS, FWACP, Department of Medicine, Faculty of Clinical Sciences, College of Health Sciences, Obafemi Awolowo University, Ile-Ife, Osun State, Nigeria. E-mail: [email protected]. 1052-3057/$ - see front matter Ó 2015 by National Stroke Association http://dx.doi.org/10.1016/j.jstrokecerebrovasdis.2014.11.013
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Introduction The burden of stroke is increasing in developing countries, with huge financial costs on the individual, family, and the health care system.1 In Nigeria, stroke is the leading cause of death and disability, and it is responsible for up to half of neurologic admissions and 5%-17% of medical deaths.2 Previous studies have shown that lack of knowledge about stroke warning signs may contribute to late presentation to the hospital.3 Nigerians with hypertension or diabetes have been reported to have poor awareness of stroke warning signs.4,5 Other Nigeria studies also found similar gaps in knowledge among university students6 and hospital workers.7 About 15% of all ischemic strokes occur in adolescents and young adults.8 Studies carried out among adolescents in developed countries regarding knowledge of cardiovascular diseases (CVDs) show that they lack knowledge of the risk factors and do not perceive themselves to be at a risk of CVD.9,10 Apart from the vascular risk factors, sickle cell disease11 is also a common cause of stroke in the adolescent age group; hence, it is important to assess level of awareness of risk factors and warning signs in them. There has been no previous study on knowledge of stroke risk factors and warning signs among adolescents; hence, we carried out this study as part of the World Stroke Day 2013 campaign in Osun State, Nigeria.
Aims The aims of the study were to assess the level of awareness of stroke risk factors and warning signs in secondary school students and teachers and to compare the level of awareness between the 2 groups.
Materials and Methods This was a cross-sectional survey conducted in 5 secondary schools in Ile-Ife and Ilesa, 2 towns in the state of Osun, southwest of Nigeria. The protocol was approved by the Health Research Ethics Committee of the Institute of Public Health, Obafemi Awolowo University. The questionnaire was administered to students in their respective classrooms and to teachers in the staff rooms/offices. Informed consent were sought and obtained from all the respondents. Respondents were informed about the purpose and protocol of the study before filling the questionnaires, which were collected immediately. Data were collected from 5 schools, 4 in Ile-Ife, and 1 from Ilesha, State of Osun, Nigeria. All the teachers were included, whereas a simple random sample was used to select students from both Junior Secondary School (JSS) and Senior Secondary School (SSS) classes. The questionnaire used in this survey was developed to assess the recognition of stroke risk factors and early
warning signs. It had been previously used and validated by previous workers.6 The questionnaire used is available as a Supplemental data. Basic demographic information collected include sex, age, occupational status (student, teacher), educational status (eg, tertiary, postgraduate), class of students (JSSs 1-3 and SSSs 1-3), history of smoking (past and current smokers), family history of heart disease, and histories of diabetes, hypertension, and stroke. The study was conducted over a period of 4 weeks (October 7 to November 4, 2013). List of important warning signs of stroke by the American Stroke Association, American National Stroke Association, and National Institute of Neurological Disorders and Stroke was used in this study. Respondents were asked to indicate if they recognized any of 7 warning signs of stroke and any of 11 risk factors of stroke. Adequate level of awareness was defined as identifying at least half of the listed risk factors (7) and warning signs (4) correctly. Respondents were also asked what they would do first, if someone were having a stroke near them. The authors visited each of the schools a week before data collection to identify a convenient time in the school timetable to administer questionnaire and assess weight and height. Students who filled the questionnaire were asked to assemble at the sick bay at break time where the measurements were taken. The measurements for the teachers were taken in the staff rooms. The body weight in kilograms was assessed with a bathroom scale and height in meters measured with a tape measure placed against a wall. The body mass index was then calculated. Descriptive statistics of frequency and percentage were used to summarize data. Inferential statistics of the Mann–Whitney U test was used to compare the awareness between groups, and the Kruskal–Wallis test was used to compare awareness among groups. Odds ratio analysis was done to determine the predictors of awareness. Alpha level was set at P less than .05. All statistical procedures were performed with the Statistical Package for Social Sciences, version 20.0 (SPSS, Chicago, IL).
Results A total of 703 respondents (589 students and 114 teachers, 315 men and 388 women) were involved in this survey. The mean age of the students was 13.9 6 2, whereas most teachers (87.7%) were between 20 and 50 years. The distribution of the characteristics of respondents is listed in Table 1. The response rate was 95.6% for the teachers and 94.1% for the students. Hypertension (69.4%) was the most commonly identified risk factor, and hyperlipidemia (21.1%) was the least commonly identified (Table 2). There were significant differences in the awareness of some stroke risk factors (smoking, obesity, family history of stroke, alcohol use, diet, transient ischemic attack, and hyperlipidemia) with
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Table 1. Characteristics of respondents Variable Age (y) 10-19 20-30 31-40 41-50 .50 Sex Male Female Educational level (teachers) Tertiary Postgraduate Educational level (students) JSS 1 JSS 2 JSS 3 SSS 1 SSS 2 SSS 3 Family history of stroke Family history of heart disease Smoking history Past smokers Current smokers History of stroke History of diabetes History of hypertension Income (Naira) 10,000-19,000 20,000-29,000 30,0000-50,000 .50,000 BMI (kg/m2) Underweight (,18.5) Normal (18.5-24.9) Overweight (25-29.9) Obese (.30)
Overall (N 5 703)
Students (n 5 589)
Teachers (n 5 114) 12 (10.5) 43 (37) 36 (31.6) 21 (18.4) 2 (1.8)
315 (44.8) 388 (55.2)
264 (44.8) 325 (55.2)
51 (44.7) 63 (55.3) 83 (72.8) 31 (27.2)
48 (6.8) 26 (3.7)
24 (4.1) 111 (18.8) 206 (35) 71 (12.1) 59 (10) 118 (20) 40 (6.8) 25 (4.2)
8 (7) 1 (.9)
7 (1) 7 (1) 1 (.9) 2 (1.8) 13 (11.4)
4 (.7) 6 (1) — — —
3 (2.6) 1 (.9) 1 (.9) 2 (1.8) 13 (11.4)
4 (3.5) 10 (8.8) 38 (33.3) 62 (54.4)
— — — —
4 (3.5) 10 (8.8) 38 (33.3) 62 (54.4)
246 (35) 373 (53.1) 45 (6.4) 39 (5.5)
240 (40.7) 327 (55.5) 16 (2.7) 6 (1)
6 (5.3) 46 (40.4) 29 (25.4) 33 (28.9)
Abbreviations: BMI, body mass index; JSS, Junior Secondary School; SSS, Senior Secondary School.
the teachers having better awareness in 4 (obesity, family history of stroke, alcohol use, diet). Weakness (51.9%) was the most commonly recognized warning sign, whereas shortness of breath was the least commonly identified. There were significant differences in the awareness of 3 (dizziness, weakness, and visual problem) of the 8 warning signs listed: students had better awareness of 2 warning signs, weakness and visual problem (Table 3). There were significant differences in the awareness of some risk factors (hypertension, stress, and alcohol use) and 3 warning signs (slurred speech, vision problems, and shortness of breath) among students in different classes (Table 3). Students in SSSs had better knowledge about some risk factors (hypertension, stress, and alcohol
use) and warning signs (slurred speech, vision problem and shortness of breath) than those in JSSs. The level of education of teachers did not affect the level of awareness as there was no statistically significant difference in the awareness of all risk factors and warning signs among teachers with tertiary and postgraduate education (Table 4). The age of the teachers did not affect the level of awareness of all the risk factors (P 5.80) or the warning signs (P 5 .39). There was no difference among men and women regarding the level of awareness of stroke risk factors; however, female teachers had better knowledge of 2 warning signs, headache and shortness of breath (Table 2). The field of study of the teachers was not included in the questionnaires.
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Table 2. Teachers awareness of stroke risk factors and warning signs and gender Response Risk factors Age Hypertension Stress Cholesterol Smoking Obesity Lack of exercise Family history of stroke Diabetes Alcohol use Diet Increased salt intake TIA Hyperlipidemia Zero risk factors $7 Risk factors All risk factors Warning signs Slurred speech Dizziness Numbness Weakness Headache Vision problem Difficulty understanding Shortness of breath Zero warning signs All warning signs
Overall, n (%), n 5 114
Males, n (%), n 5 51
Females, n (%), n 5 63
P value
50 (43.9) 91 (79.8) 75 (65.8) 58 (50.9) 56 (49.6) 56 (49.1) 65 (57.0) 60 (52.6) 54 (47.4) 60 (52.6) 113 (99.1) 37 (32.5) 54 (47.8) 26 (22.8) 15 (13.2) 50 (43.9) 109 (95.6)
25 (49.0) 41 (80.4) 32 (62.7) 27 (52.9) 25 (49.0) 24 (47.1) 26 (51.0) 27 (52.9) 22 (43.1) 26 (51.0) 51 (100) 17 (33.3) 21 (41.2) 11 (21.6) 8 (15.7) 23 (45.1) 47 (92.2)
25 (39.7) 50 (54.9) 43 (68.3) 31 (49.2) 31 (50.0) 32 (50.8) 39 (61.9) 33 (52.4) 32 (50.8) 34 (54.0) 62 (98.4) 20 (31.7) 33 (53.2) 15 (23.8) 7 (11.1) 27 (42.9) 62 (98.4)
.318 .892 .538 .692 .917 .692 .241 .953 .416 .751 .336 .857 .202 .777 .472 .811 .098
57 (50.0) 31 (27.2) 38 (33.3) 48 (42.1) 42 (36.8) 23 (20.2) 38 (33.3) 37 (32.5) 27 (23.7) 4 (3.5)
23 (45.1) 15 (29.4) 15 (29.4) 19 (37.3) 13 (25.5) 11 (21.6) 11 (21.6) 16 (31.4) 11 (21.6) 2 (3.9)
34 (54.0) 16 (25.4) 23 (36.5) 29 (46.0) 29 (46.0) 12 (19.0) 27 (42.9) 21 (33.3) 16 (25.4) 2 (3.2)
.346 .632 .424 .345 .024 .739 .017 .824 .633 .951
Being a teacher, having a history of hypertension, and not being obese were significant predictors of knowing at least half of the listed risk factors. Although family history of stroke and having a history of hypertension were significant predictors of knowing at least half of the listed warning signs (Table 5). Four hundred ninety-three (41.4%) respondents indicated that they would take the person to the hospital, with the percentage of teachers higher than that of students (Table 6). The television was the most common source of information (72.8%), followed by literature (magazines and newspaper, 58.3%). Having seen family (11.7%) or friend (13.9%) with stroke were the least popular sources of information among the students (Table 7). The sources of information differed among students and teachers with the former getting information from literature and the Internet and the later from the doctor; 12 teachers (10.5%) obtained information about stroke from more than 2 sources compared with 43 (7.3%) students.
Discussion The results of this study showed that hypertension (69.4%) was the most correctly identified stroke risk
factor, whereas weakness of 1 side of the body (51.9%) was the most correctly identified warning sign among the students and teachers in selected secondary schools in Osun State. Previous studies have reported hypertension as the most commonly identified risk factor6,7,12 and weakness as the most commonly identified warning sign5-7 among Nigerian adults. Our findings among the teachers that the level of education and gender did not affect the level of awareness of stroke risk factors is contrary to the findings from previous Nigerian studies6,13 that men with higher education had better knowledge about risk factors and warning signs compared with women with lower education. This might be because the level of education among the teachers is better than that of the population as all of them had at least tertiary education. However, we could not assess the effect of field of study of the teachers on the levels of awareness as this information was not included in the questionnaire. Students, who were mostly (98.1%) adolescents (mean age 5 13.9 6 2 years) had better awareness of some warning signs than teachers who were all adults (.20 years), whereas teachers had better knowledge of risk factors than students. The occurrence of stroke has been reported
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Table 3. Students’ awareness of stroke risk factors and warning signs according to class
Risk factors Age Hypertension Stress Cholesterol Smoking Obesity Lack of exercise Family history Diabetes Alcohol use Diet Increased salt intake TIA Hyperlipidemia Warning signs Slurred speech Dizziness Numbness Weakness Headache Vision problem Difficulty understanding Shortness of breath
JSS, n (%) (n 5 341)
SSS, n (%) (n 5 248)
P value
102 (29.9) 198 (58.1) 178 (52.2) 84 (24.6) 166 (48.7) 85 (24.9) 140 (41.1) 62 (18.2) 79 (23.2) 112 (32.8) 102 (29.9) 79 (23.2)
89 (35.9) 199 (80.2) 162 (65.3) 87 (35.1) 140 (56.5) 73 (29.4) 104 (41.9) 47 (19.0) 60 (24.2) 113 (45.6) 66 (26.6) 58 (23.4)
.127 .000 .001 .006 .062 .224 .831 .812 .777 .002 .380 .950
71 (20.8) 70 (20.5)
59 (23.8) 60 (24.2)
.392 .291
85 (24.9) 86 (25.2) 80 (23.5) 175 (51.3) 101 (29.6) 76 (22.3) 105 (30.8)
102 (41.1) 61 (24.8) 67 (27.0) 142 (57.3) 67 (27.4) 78 (31.5) 93 (37.5)
.000 .863 .326 .153 .560 .013 .089
70 (20.5)
69 (27.8)
.040
Abbreviations: JSS, Junior Secondary School; SSS, Senior Secondary School; TIA, transient ischemic attack.
to increase with age.14 Because stroke occurs mostly in adults, it is expected of adults to have better awareness of stroke warning signs. Adequate information about the warning signs of stroke may reduce the median presentation time of 3 days with a range of 1-90 days reported among Nigerians.13 The phase that the most improvement can be achieved is the time from symptom recognition to the decision to seek medical care.15 When a stroke occurs, the time of presentation to the hospital is important in its management as delays often result in poor outcome.6 Rapid access to medical care is an important predictor of treatment and rehabilitation outcome. The findings in our study, which show a low level of stroke warning signs, brings to fore the fact that Nigerian adults urgently need more information about stroke warning signs. This will enable them to recognize the symptoms when they are having a stroke or when a stroke is occurring near them. Stroke education campaign should also emphasize the importance of early presentation for medical care.
Table 4. Teachers’ awareness of stroke risk factors and warning signs by educational levels Tertiary, n (%) (n 5 83) Risk factors Age Hypertension Stress Cholesterol Smoking Obesity Lack of exercise Family history Diabetes Alcohol use Diet Increased salt intake TIA Hyperlipidemia Warning signs Slurred speech Dizziness Numbness Weakness Headache Vision problem Difficulty understanding Shortness of breath
Postgraduate, N (%) (n 5 31) P value
32 (38.6) 66 (79.5) 48 (66.3) 40 (48.2) 43 (51.8) 47 (56.6) 43 (51.8) 51 (61.4) 41 (49.4) 36 (43.4) 28 (33.7) 39 (47.0)
18 (58.1) 25 (80.6) 20 (64.5) 16 (51.6) 13 (41.9) 18 (58.1) 17 (54.8) 19 (61.3) 19 (61.3) 13 (41.9) 9 (29) 15 (48.4)
.062 .894 .861 .745 .348 .890 .773 .988 .258 .890 .424 .105
23 (27.7) 17 (20.5)
3 (9.7) 4 (12.9)
.424 .961
41 (49.4) 22 (26.5) 25 (30.1) 34 (41.0) 32 (38.6) 16 (19.3) 29 (34.9)
16 (51.6) 9 (29) 13 (41.9) 14 (45.2) 10 (32.3) 7 (22.6) 9 (29)
.833 .787 .234 .686 .535 .696 .552
28 (33.7)
9 (29)
.633
Abbreviations: TIA, transient ischemic attack.
The results of our study also showed that teachers had better awareness of stroke risk factors than students. Emerging data have raised public health concerns about the increasing prevalence of traditional vascular risk factors in young individuals and their potential role in
Table 5. Significant predictors of knowing at least half of the listed stroke warning signs or risk factors Factor Warning signs (#4) Stroke in family History of hypertension Risk factors (#7) Not obese Teacher History of hypertension
OR
95% CI
P value
.435 .188
.218-.868 .054-.657
.015 .007
2.339 .338 .088
1.221-4.479 .225-.510 .071-.706
.008 .000 .004
Abbreviations: CI, confidence interval; OR, odds ratio.
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Table 6. Actions to be taken by respondents when a stroke occurs near them Action to be taken
Students (n 5 589), n (%)
Teachers (n 5 114), n (%)
Total (N 5 703), n (%)
Call a doctor Take the person to the hospital Call family, friends, or neighbors Seek spiritual attention Do nothing
183 (31.1) 230 (39) 32 (5.4) 19 (3.2) 7 (1.2)
16 (14) 61 (53.5) 1 (.9) 1 (.9) —
199 (28.3) 291 (41.4) 33 (4.7) 20 (2.8) 7 (1)
increasing the risk of ischemic stroke, stroke recurrence, and poststroke mortality.8 A previous study9 has reported that adolescents in their study population were not aware of the high prevalence and mortality of CVD and did not perceive themselves at risk for CVD. Singhal et al7 reported that between 532,000 and 852,000 people aged 18 to 44 years in the United States have had a stroke. Hospital discharges for stroke in the United States from 1995 to 1996 and 2007 to 2008 among patients aged 15 to 44 years increased by 23%-53%, depending on age and gender of the group. Although the causes and risk factors for stroke in the young are often rare or undetermined, young adults with stroke also have a high burden of known cardiovascular risk factors, which include hypertension, diabetes, obesity, and substance abuse.16 Typically, CVDs occur in middle age or later, but risk factors are determined to a great extent by behaviors learnt in childhood and continued into adulthood, such as dietary habits and smoking.17 More emphasis should be placed on stroke education (adequate and appropriate information) about the risk factors targeting young people in secondary schools. This is to prevent the occurrence of avoidable risk factors among adolescents who are the majority among students in Nigerian secondary schools. Stroke educational programs should also entail information about prevention of stroke, which include control of established stroke risk factors, such as hypertension, obesity, diabetes, and smoking.
Stroke education campaigns targeted at high school youths could yield favorable results. Promotion of healthy lifestyle habits could be implemented during a crucial period by targeting this younger age group, that is, a time in which CVD risk factors and atherosclerotic plaques are in the early stages of development, and cardioprotective practices can be ingrained.18 Educational intervention is needed to raise awareness about risk factors in the adolescent population.10 Many respondents (41.4%) indicated that they would take the person having a stroke near them to the hospital. The television was the most common source of information for both students and teachers. This is followed by literature among the students (59.4%) and health practitioners (doctors) among the teachers (61.4%). The finding that majority of teachers had information from their doctors shows that there should be educational program for medical practitioners and primary care physicians, focused on the need to screen for cardiovascular risk factors in all adults presenting to health care facilities and also to give information on the need to adopt a healthy life style and how to recognize stroke warning signs. Also, awareness programs for students should focus on giving adequate and appropriate information on stroke in form of literature or on social media such as the Internet. The predictive factors for awareness included a family history of stroke, hypertension, and not being obese. Obese persons in our study were less aware of important
Table 7. Respondents’ sources of information about stroke Source of information*
Students (n 5 589), n (%)
Teachers (n 5 114), n (%)
Total (N 5 703), n (%)
Television Radio Literature Health practitioners Stroke campaigns Internet Public library Relatives Others Learned in school Seen stroke in family Seen a friend with stroke
426 (72.3) 311 (52.8) 350 (59.4) 269 (45) 199 (33.8) 238 (40.4) 132 (22.4) 161 (27.3) 3 (.5) 228 (38.7) 82 (13.9) 98 (16.6)
86 (75.4) 64 (56.1) 60 (32.6) 70 (61.4) 37 (32.5) 37 (32.5) 19 (16.7) 29 (25.4) — — — —
512 (72.8) 375 (53.3) 410 (58.3) 339 (48.2) 236 (33.6) 275 (39.1) 151 (21.5) 190 (27) 3 (.4) 228 (32.4) 82 (11.7) 98 (13.9)
*Multiple responses allowed.
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stroke risk factors and warning signs. Generally, obesity in the southern part of Nigeria is considered as a sign of good living. This possibly might be an explanation for the lower level of awareness among obese persons in this study. There is a need for stroke educational programs emphasizing the need for regular screening for obesity, especially for people who are overweight. Adequate information about stroke risk factors and warning signs should also be given to obese persons. Also, personal risk factors should be assessed as part of stroke awareness programs. This study concluded that there was inadequate awareness of stroke risk factors and warning signs among the respondents. Students had better awareness of warning signs than teachers, whereas teachers had better awareness of risk factors than the students. There is a need for more stroke education with emphasis on adequate information about stroke risk factors to prevent occurrence especially among students and warning signs especially among at-risk adults so that they can act promptly and appropriately by seeking immediate medical attention.
Supplementary Data Supplementary data related to this article can be found at http://dx.doi.org/10.1016/j.jstrokecerebrovas dis.2014.11.013.
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