On-line version ISSN 1678-4464
Print version ISSN 0102-311X
Cad. Saúde Pública vol.28 n.8 Rio de Janeiro Aug. 2012
Nível de escolaridade e dependência funcional em sobreviventes de acidente vascular cerebral isquêmico
Tiótrefis G. FernandesI, II; Alessandra C. GoulartI, III; Waldyr R. Santos-JuniorI; Airlane P. AlencarIV; Isabela M. BenseñorI, III; Paulo A. LotufoI, III
IFaculdade de Medicina, Universidade de São Paulo, São Paulo, Brasil
IIInstituto de Saúde e Biotecnologia, Universidade Federal do Amazonas, Coari, Brasil
IIIHospital Universitário, Universidade de São Paulo, São Paulo, Brasil
IVInstituto de Matemática e Estatística, Universidade de São Paulo, São Paulo, Brasil
We evaluated the functional dependence of stroke survivors from the Study of Stroke Mortality and Morbidity, using the Rankin Scale. Out of 355 ischemic stroke survivors (with a mean age of 67.9 years), 40% had some functional dependence at 28 days and 34.4% had some functional dependence at 6 months. Most predictors of physical dependence were identified at 28 days. These predictors were: low levels of education [illiterate vs. > 8 years of education, multivariate odds ratio (OR) = 3.7; 95% confidence interval (95%CI): 1.60-8.54] and anatomical stroke location (total anterior circulation infarct, OR = 16.9; 95%CI: 2.93-97.49). Low levels of education and ischemic brain injury influenced functional dependence in these stroke survivors. Our findings reinforce the necessity of developing strategies for the rehabilitation of stroke patients, more especially in formulating specific strategies for care and treatment of stroke survivors with low socioeconomic status.
Stroke; Educational Status; Outcome Assessment (Health Care)
Foi avaliada a dependência funcional em sobreviventes de acidente vascular cerebral (AVC) do Estudo da Mortalidade e Morbidade do Acidente Vascular Cerebral, utilizando a Escala de Rankin. De 355 sobreviventes com AVC isquêmico (idade média de 67,9 anos), 40% tinham dependência funcional em 28 dias e 34,4% em 6 meses. Os principais indicadores de dependência física foram identificados em 28 dias, e eram: baixa escolaridade (analfabetos vs. > 8 anos de educação, RC = 3,7; IC95%: 1,60-8,54) e localização do AVC (infarto circulação total anterior, RC = 16,9; IC95%: 2,93-97,49). Baixo nível educacional e insulto cerebral isquêmico influenciaram o grau de dependência funcional nesses sobreviventes de AVC. Nossos achados reforçam a necessidade de desenvolvimento de estratégias para reabilitação de pacientes com AVC e formulação de estratégias específicas de atenção e tratamento para essas pessoas, especialmente na população com baixo nível socioeconômico.
Acidente Vascular Cerebral; Escolaridade; Avaliação de Resultados (Cuidados de Saúde)
The financial and social burden of functional dependence due to cerebrovascular disease is an important focus of discussion in public health, particularly among countries with resource-poor settings. Although stroke mortality rates vary greatly, low-income countries are the most affected 1. Despite fast economic growth in some regions, Brazil has the highest stroke mortality rates in the Americas 2. A recent review of socioeconomic status and stroke reveals evidence that suggests a strong relationship between socioeconomic status and an increased risk of stroke mortality. It also suggested that low socioeconomic status may be associated with more severe stroke, as well as an increase of dependence in daily activities, increased disability and handicap 3. Others predictors of post-stroke disability that have been reported previously are advanced age, recurrent stroke, stroke severity, the anatomical location of brain damage, and having a high level of functional dependence at hospital discharge 4,5.
Many studies have used the modified Rankin Scale (mRS) to investigate short- and long-term disability after stroke. Some reports from developed countries describe functional dependence rates of around 30%, three months after acute stroke 6,7. Other long-term studies found higher frequencies (in the range of 34%-47%) of poor functional outcomes (mRS 3-5), six months after stroke 8,9. Data on post-stroke disability in middle and low income countries is scarce. Two population based studies conducted in Latin America, including Brazil, reported functional dependence rates between 18% and 30% six months after stroke 10,11.
Previous reports have tried to identify factors associated with stroke functional prognosis after hospital discharge, but often with contradictory results 12,13,14. A previous cohort study performed in stroke surveillance, the EMMA study (Study of Stroke Mortality and Morbidity), identified almost 85% of stroke survivors as being ischemic subtype 15. In addition to occupation and income, education is considered one of the most reliable markers of socioeconomic status in many epidemiological studies 3. Moreover, educational level can be applied equally to both genders. It is also a more reliable indicator of socioeconomic status for economically inactive people. Thus, our aim was to verify the influence of educational levels as an index for socioeconomic status. We also verified the influence of preexisting co-morbidities and hospital care, for functional dependence at 28 days and at six months among ischemic stroke survivors in the EMMA study.
Population and study area
This is an ancillary study of functional disability using data from the cohort EMMA study, which has been ongoing since April 2006 in a teaching community hospital, the University Hospital of São Paulo University (Hospital Universitário, Universidade de São Paulo). Details of the EMMA study have previously been described elsewhere 16. The University Hospital is a teaching community hospital (260 beds) in Butantan, a neighborhood on the west side of the city with 424,377 inhabitants (2009). This hospital offers the sole support for emergencies from primary care units and also for paramedic ambulances in the area. The neurological referral for this community facility is the Clinics Hospital, a tertiary-care hospital located eight kilometers away. The district of Butantan includes several social contrasts with rich and poor areas located side by side. Cardiovascular disease represents 40% of all deaths in Butantan and the city of São Paulo. Stroke mortalities account for one-quarter of all circulatory disease deaths and are concentrated in the poorer areas.
All individuals for whom functional status information was available at 28 days and at six months after an acute event were included in this analysis. We evaluated data from 355 consecutive ischemic stroke survivors older than 35 years of age who were admitted, up until December 2009.
We performed the analysis from the in-hospital phase (step 1) of the EMMA study, which was based on the WHO STEPwise approach to stroke surveillance. Data collection was performed by trained interviewers and medical researchers according to the instructions in the STEPwise approach to stroke surveillance manual 17. The socio-demographic data (gender, age, educational level, and marital status), acute stroke information (stroke subtype, onset of neurological symptoms, and pre-stroke clinical conditions), hospital care (stroke neuro-imaging diagnosis, delay from onset to hospitalization, and hospital length of stay), and functional information (mRS at 28 days and at six months after stroke) were documented. Written informed consent was obtained from all potential stroke patients admitted to the hospital, who agreed to participate in this study, and each subject received a copy of the consent form. Among those who had severe stroke or any impairment of language abilities, the consent form was obtained from their parent/legal guardian or legally authorized representative. The research protocol was approved by the institutional review board of the University Hospital of São Paulo University.
The stroke diagnosis was confirmed based on the clinical and radiological (computed tomography) assessments of a neurologist during hospitalization and validated by a medical practitioner. Additionally, an evaluation of ischemic stroke subtypes was performed from among those who had computed tomography information in the first 48 hours of hospital admission. Diagnoses were further subdivided into total anterior circulation infarct (TACI), partial anterior circulation infarct (PACI), lacunar infarct (LACI), posterior circulation infarct (POCI), and, when there was no visible infarction, (normal).
Due to a higher proportion of individuals with low levels of education, we categorized educational levels in the following categories: 0 or < 1 year, 1 to 7 years, and > 8 years. The pre-stroke clinical data wasbased on self-reported history of the following cerebrovascular risk factors (yes/no): high blood pressure, diabetes mellitus, heart disease, current smoking, and alcohol consumption. Self-reported history of high blood pressure and diabetes mellitus, as well as hospital characteristics (onset, delay to hospitalization, length of stay and stroke diagnosis confirmed by computed tomography) were further confirmed by medical record.
The functional outcomes at 28 days and at six months after the stroke event were assessed using the mRS 6 by telephone interview. The mRS is a useful tool for a global assessment of stroke outcomes 18, and it is accepted as a measure of functioning activity, disability, and health regards in accordance with WHO international classifications 19. The scale is defined categorically with seven different grades: 0, no symptoms; 1, no significant disability despite symptoms; 2, slight disability; 3, moderate disability; 4, moderately severe disability; 5, severe disability; and 6, death. Although the mRS has been shown to be less reliable when performed by telephone, its use is recommended for dichotomized data analyses 20,21, and it is widely used in stroke trials 19. In the present study, the functional outcome was dichotomized into anindependent state (rankin score of 0-2) and a dependent state (rankin score of 3-5). The outcome of death was considered elsewhere. Just six participants responded the scale category interview, 28 days after the event, while they were inpatients. Among those who had severe stroke or any impairment of language abilities, the information for the mRS was obtained from their caregiver.
Categorical and continuous variables were compared according to gender using the chi-square test and Student's t-test, respectively. Age was analyzed in continuous and dichotomous variables (35-64 years and > 65 years). We performed multivariate regression considering all variables that were significant at p < 0.10 in the age-adjusted analysis at 28 days and at six months, respectively. In the final model, we retained all of the variables that allowed a better fit according to the Hosmer-Lemeshow test. Results were expressed as odds ratio (OR), and 95% confidence intervals (95%CI) were calculated. All tests were two-tailed and the confidence interval was set at p < 0.05. SPSS software, version 16.0 (SPSS Inc., Chicago, USA) was used for the statistical analyses.
From April 2006 to December 2009, 678 patients > 35 years old with a confirmed diagnosis of ischemic stroke (first and recurrent events) were enrolled in this study. Of these, 160 died before the 6 month follow-up and were not included in the analysis. A complete follow-up was possible with 355 out of 518 survivors, and they were included in the present analysis. It was not possible to carry out 28 day and/or 180 day follow-ups in a total of 163 cases. We compared the 355 cases included in the analysis with the 163 missing cases, regarding: age (65 years and over: cases 65.4% vs. missing 62%; p = 0.46); gender (men: cases 52.4% vs. missing 52.8%; p = 0.94); years of education (illiterate: cases 20.3% vs. missing 19.5%; p = 0.21); event stroke (first stroke: cases 70.3% vs. missing 68.8%; p = 0.74); history of high blood pressure (cases 81.4% vs. missing 81.6%; p = 0.96). Thus, there are no statistically significant differences between the groups. The baseline characteristics are shown in Table 1. Among ischemic stroke survivors, 52.4% were male and their mean age was 67.9 years. Most patients had < eight years of schooling (elementary school). In comparing genders, we found that women were three years older than men, most of them lived alone (single or widowed), and they took more antihypertensive drugs than men. There also was a higher frequency of smokers and higher alcohol intake among men, in comparison to women.
The most common ischemic area recognized by computed tomography was LACI (30.2%). Most cases were classified as the first ever event (70.3%), 76.9% arrived at the hospital < 24 hours after the stroke, and 57.5% remained in the hospital for two to 10 days. According to the mRS assessment of functional dependence after the acute event, there were similar rates of dependence at both intervals: 28 days (40%) and at six months (34.3%).
In age-adjusted analyses, ischemic stroke survivors without formal education or with one to seven years of education had an approximately two de four-fold risk of functional dependence compared to those with > 8 years of education at the six month follow up (Table 2). As expected, patients with the worst functional dependence at both intervals after the stroke had experienced a longer hospital stay (> 11 days). The ischemic stroke subtype diagnosed by computed tomography was also associated with increased risk of disability during the six month follow-up. We found the highest risk of functional dependence, among those who had a TACI both at 28 days and at six months after the event. PACI and LACI represented an increased risk of disability only after six months. We observed a trend of increased risk of disability at 28 days among patients who had a previous diagnosis of hypertension and stroke recurrence. Other variables were not significantly associated with functional status.
Multivariate analyses found the same higher risks of dependence in patients with low levels of education and among those who had suffered from a total anterior circulation infarct. In particular, in patients with no formal education, the risk of dependence after ischemic stroke was persistently higher during the six month follow-up. Finally, the association between functional disability and longer hospitalization after stroke was confirmed (Table 3). Table 4 analyzed patients who died in the same period. The results did not materially change the association between education and functional dependence.
In the present study, 40% of the participants, who were assisted at a community hospital, had functional impairment 28 days after an ischemic event. Although post-stroke functional status was influenced by many factors, the most important disability predictors were practically the same at 28 days and at six months after hospital discharge. In addition to advanced age, a low level of education, TACI and a hospital stay of > 11 days were also associated with higher functional dependence among stroke survivors.
As expected, disability rates after an acute event tended to decrease over time. This may occur due to the natural history of disease and rehabilitation, as well as survival bias 8,22. Compared to previous studies performed in developed countries that used the mRS as a measure of functional outcome, we found higher proportions of dependence at 28 days and at six months after stroke (40% and 34.4%, respectively) 6,7,23. Data from a population-based study conducted in Martinique 24 that evaluated two age groups, very old (mean age of 88.8 years) and younger individuals (mean age of 65.8 years) 28 days after stroke, reported 78% and 48% functional impairment, respectively. The highest rate of functional impairment was reported by Dalal et al. 25 in a population-based study performed in Mumbai, India. In this study, a poor functional outcome was observed in approximately 60% of stroke survivors at 28 days after an acute event. A hospital-based study conducted in Antalya (Turkey) evaluated the one year functional outcome after ischemic stroke and found that 26% of stroke survivors (mean age of 61.2 years) were functionally dependent 26. Consistent with our findings, the PISCIS project, a stroke community-based study performed in Iquique (Chile), also found a six month disability rate of about 30% after acute stroke 10. Our findings diverged from those of a study in Joinville (Santa Catarina State, Brazil) 11, which found a 18% poor functional outcome rate among first-stroke survivors (mean age of 65 years), similar to the rate reported in Italy 23. Although the Joinville region and the region included in our study have similar per capita incomes, in Joinville there is a smaller social gap compared to our sample population. In addition to the educational level, differences in access to medical services and rehabilitation can also exert an influence on recovery, as discussed below. Furthermore, advanced age and some characteristics, such as stroke subtypes and recurrent stroke events, may partially explain differences in functional outcome after an acute stroke event. Overall, ischemic functionally dependent patients had a longer survival than intracerebral hemorrhage functionally dependent patients, and those who had their first-ever stroke event survived longer than those who had recurrent strokes 27.
Similar to other epidemiological studies of stroke survivors, we found high frequencies of cardiovascular risk factors, such as hypertension, diabetes, and heart disease 11,26,28. However, they were not predictors for long-term disability as previously described 29,30. A low level of education, as a marker of socioeconomic status, was the most important risk factor for functional dependence in our sample. Overall, our patients had low levels of education (< 8 years) and, as previously reported 3,31, we found an inverse association between education and functional outcome, indicating a dose-response effect. In particular, among stroke survivors with no formal education, the risk of disability was progressively higher during the follow-ups. There are several possible explanations for this relationship, such as difficulties related to; access of rehabilitation centers, adherence to treatment, comorbidities and a lack of knowledge about cardiovascular health 32. The University Hospital facility belongs to the Brazilian Unified National Health System (SUS) which offers universal healthcare coverage 33, including emergency care and hospitalizations that are totally free of charge. The majority of our study patients lived in the poorest areas on the west side of the city, and had few specialized services to help with their recovery process. Knowledge about stroke risk factors, symptoms and treatment is an important outcome predictor. It has been reported that people with low levels of education and income have less knowledge about stroke, even among those who have experienced a previous event or who have had a family historyof stroke 34,35. Previous studies performed in Brazil reinforce our findings about the relationship between socioeconomic and functional outcome 36,37. Moreover, low levels of education may interfere with treatment adherence and medical recommendations.
Regarding the severity of stroke, and in agreement with previous studies, we found that TACI was the most important predictor of poor functional recovery during the six month follow-up 12,38,39. Finally, longer hospitalizations were associated with a higher risk of disabilitiesin our study. As inour findings, previous reports found that patients with severe injuries, delay from onset to hospitalization and complications from the disease resulted in a worse functional outcome 4,40.
Our study has some limitations, such as the use of dichotomized mRS as the only measure of functional outcome, which may not be sensitive enough to capture small functional improvements. Considering the complexity involved in predicting disability after stroke, it is important to examine other variables of interest, such as the National Institutes of Health Stroke Scale (NIHSS) score at admission, atrial fibrillation and patient access to rehabilitation information. Community-based studies using standardized diagnostic criteria with verified diagnoses are an ideal means of studying the burden of disease in general and stroke in particular. Hospital-based studies of stroke are also useful, but are more prone to selection bias and are influenced to varying degrees in different countries by factors like wealth, health insurance, stroke specialization of the receiving center, confidence in diagnosis by the referring physician and proximity to health care facilities. However, our study has some strength, such as the use of the WHO STEPwise approach to stroke surveillance method, which has been characterized as a good tool for collecting reliable and easily comparable data in less-developed countries.
In conclusion, we found that the most important post-stroke predictors of functional disability were low levels of education and the anatomical location of cerebral injury. Our findings reinforce the necessity of developing strategies to reduce social inequalities, which will result in more suitable management of stroke patients in developing countries.
T. G. Fernandes participated in the design of study, performed statistical analyses, wrote the first draft of the manuscript and reformulated subsequent revisions.
A. C. Goulart, I. M. Benseñor and P. A. Lotufo participated in the design of study, performed statistical analyses and revised the final version of manuscript. W. R. Santos-Junior revised the final version of manuscript. A. P. Alencar performed statistics analyses and revised the final version of manuscript.
We are grateful to all interviewers, the research staff involved in the EMMA study and CNPq and FAPESP for their financial support.
1. Johnston SC, Mendis S, Mathers CD. Global variation in stroke burden and mortality: estimates from monitoring, surveillance, and modelling. Lancet Neurol 2009; 8:345-54. [ Links ]
2. Rodriguez T, Malvezzi M, Chatenoud L, Bosetti C, Levi F, Negri E, et al. Trends in mortality from coronary heart and cerebrovascular diseases in the Americas: 1970-2000. Heart 2006; 92:453-60. [ Links ]
3. Cox AM, McKevitt C, Rudd AG, Wolfe CD. Socioeconomic status and stroke. Lancet Neurol 2006; 5:181-8. [ Links ]
4. Macciocchi SN, Diamond PT, Alves WM, Mertz T. Ischemic stroke: relation of age, lesion location, and initial neurologic deficit to functional outcome. Arch Phys Med Rehabil 1998; 79:1255-7. [ Links ]
5. Ng YS, Stein J, Ning M, Black-Schaffer RM. Comparison of clinical characteristics and functional outcomes of ischemic stroke in different vascular territories. Stroke 2007; 38:2309-14. [ Links ]
6. Weimar C, Kurth T, Kraywinkel K, Wagner M, Busse O, Haberl RL, et al. Assessment of functioning and disability after ischemic stroke. Stroke 2002; 33:2053-9. [ Links ]
7. Hong KS, Saver JL. Quantifying the value of stroke disability outcomes: WHO global burden of disease project disability weights for each level of the modified Rankin Scale. Stroke 2009; 40:3828-33. [ Links ]
8. Slot KB, Berge E, Dorman P, Lewis S, Dennis M, Sandercock P. Impact of functional status at six months on long term survival in patients with ischaemic stroke: prospective cohort studies. BMJ 2008; 336:376-9. [ Links ]
9. de Haan R, Limburg M, van der Meulen J, van denBos GA. Use of health care services after stroke. Qual Health Care 1993; 2:222-7. [ Links ]
10. Lavados PM, Sacks C, Prina L, Escobar A, Tossi C, Araya F, et al. Incidence, 30-day case-fatality rate, and prognosis of stroke in Iquique, Chile: a 2-year community-based prospective study (PISCIS project). Lancet 2005; 365:2206-15. [ Links ]
11. Cabral NL, Gonçalves AR, Longo AL, Moro CH, Costa G, Amaral CH, et al. Incidence of stroke subtypes, prognosis and prevalence of risk factors in Joinville, Brazil: a 2 year community based study. J Neurol Neurosurg Psychiatry 2009; 80:755-61. [ Links ]
12. Turhan N, Atalay A, Muderrisoglu H. Predictors of functional outcome in first-ever ischemic stroke: a special interest to ischemic subtypes, comorbidity and age. NeuroRehabilitation 2009; 24:321-6. [ Links ]
13. Ali M, Sacco RL, Lees KR. Primary end-point times, functional outcome and adverse event profile after acute ischaemic stroke. Int J Stroke 2009; 4:432-42. [ Links ]
14. Kong FY, Tao WD, Hao ZL, Liu M. Predictors of one-year disability and death in Chinese hospitalized women after ischemic stroke. Cerebrovasc Dis 2010; 29:255-62. [ Links ]
15. Goulart AC, Benseñor IM, Fernandes TG, Alencar AP, Fedeli LM, Lotufo PA. Early and one-year stroke case fatality in São Paulo, Brazil: applying the World Health Organization's stroke STEPS. J Stroke Cerebrovasc Dis 2011; [Epub ahead of print] [ Links ].
16. Goulart AC, Bustos IR, Abe IM, Pereira AC, Fedeli LM, Benseñor IM, et al. A stepwise approach to stroke surveillance in Brazil: the EMMA (Estudo de Mortalidade e Morbidade do Acidente Vascular Cerebral) study. Int J Stroke 2010; 5:284-9. [ Links ]
17. World Health Organization. WHO STEPS stroke manual: the WHO STEPwise approach to stroke surveillance. Geneva: World Health Organization; 2005. [ Links ]
18. Duncan PW, Jorgensen HS, Wade DT. Outcome measures in acute stroke trials: a systematic review and some recommendations to improve practice. Stroke 2000; 31:1429-38. [ Links ]
19. Quinn TJ, Dawson J, Walters MR, Lees KR. Functional outcome measures in contemporary stroke trials. Int J Stroke 2009; 4:200-5. [ Links ]
20. Wilson JT, Hareendran A, Hendry A, Potter J, Bone I, Muir KW. Reliability of the modified Rankin Scale across multiple raters: benefits of a structured interview. Stroke 2005; 36:777-81. [ Links ]
21. Newcommon NJ, Green TL, Haley E, Cooke T, Hill MD. Improving the assessment of outcomes in stroke: use of a structured interview to assign grades on the modified Rankin Scale. Stroke 2003; 34:377-8. [ Links ]
22. Kelley RE, Borazanci AP. Stroke rehabilitation. Neurol Res 2009; 31:832-40. [ Links ]
23. Sacco S, Totaro R, Toni D, Marini C, Cerone D, Carolei A. Incidence, case-fatalities and 10-year survival of subarachnoid hemorrhage in a population-based registry. Eur Neurol 2009; 62:155-60. [ Links ]
24. Olindo S, Cabre P, Deschamps R, Chatot-Henry C, Rene-Corail P, Fournerie P, et al. Acute stroke in the very elderly: epidemiological features, stroke subtypes, management, and outcome in Martinique, French West Indies. Stroke 2003; 34:1593-7. [ Links ]
25. Dalal PM, Malik S, Bhattacharjee M, Trivedi ND, Vairale J, Bhat P, et al. Population-based stroke survey in Mumbai, India: incidence and 28-day case fatality. Neuroepidemiology 2008; 31:254-61. [ Links ]
26. Samanci N, Dora B, Kizilay F, Balci N, Ozcan E, Arman M. Factors affecting one year mortality and functional outcome after first ever ischemic stroke in the region of Antalya, Turkey (a hospital-based study). Acta Neurol Belg 2004; 104:154-60. [ Links ]
27. Eriksson SE, Olsson JE. Survival and recurrent strokes in patients with different subtypes of stroke: a fourteen-year follow-up study. Cerebrovasc Dis 2001; 12:171-80. [ Links ]
28. O'Donnell MJ, Xavier D, Liu L, Zhang H, Chin SL, Rao-Melacini P, et al. Risk factors for ischaemic and intracerebral haemorrhagic stroke in 22 countries (the INTERSTROKE study): a case-control study. Lancet 2010; 376:112-23. [ Links ]
29. Blanco M, Castellanos M, Rodriguez-Yanez M, Sobrino T, Leira R, Vivancos J, et al. High blood pressure and inflammation are associated with poor prognosis in lacunar infarctions. Cerebrovasc Dis 2006; 22:123-9. [ Links ]
30. Karatepe AG, Gunaydin R, Kaya T, Turkmen G. Comorbidity in patients after stroke: impact on functional outcome. J Rehabil Med 2008; 40:831-5. [ Links ]
31. Putman K, De Wit L, Schoonacker M, Baert I, Beyens H, Brinkmann N, et al. Effect of socioeconomic status on functional and motor recovery after stroke: a European multicentre study. J Neurol Neurosurg Psychiatry 2007; 78:593-9. [ Links ]
32. Kapral MK, Wang H, Mamdani M, Tu JV. Effect of socioeconomic status on treatment and mortality after stroke. Stroke 2002; 33:268-73. [ Links ]
33. Paim J, Travassos C, Almeida C, Bahia L, Macinko J. The Brazilian health system: history, advances, and challenges. Lancet 2011; 377:1778-97. [ Links ]
34. Travis LH, Flemming KD, Brown Jr. RD, Meissner I, McClelland RL, Weigand SD. Awareness of stroke risk factors, symptoms, and treatment is poor in people at highest risk. J Stroke Cerebrovasc Dis 2003; 12:221-7. [ Links ]
35. Jones SP, Jenkinson AJ, Leathley MJ, Watkins CL. Stroke knowledge and awareness: an integrative review of the evidence. Age Ageing 2010; 39:11-22. [ Links ]
36. Pontes-Neto OM, Silva GS, Feitosa MR, Figueiredo NL, Fiorot Jr. JA, Rocha TN, et al. Stroke awareness in Brazil: alarming results in a community-based study. Stroke 2008; 39:292-6. [ Links ]
37. Falavigna A, Teles AR, Vedana VM, Kleber FD, Mosena G, Velho MC, et al. Awareness of stroke risk factors and warning signs in southern Brazil. Arq Neuropsiquiatr 2009; 67:1076-81. [ Links ]
38. Bamford J, Sandercock P, Dennis M, Burn J, Warlow C. Classification and natural history of clinically identifiable subtypes of cerebral infarction. Lancet 1991; 337:1521-6. [ Links ]
39. Di Carlo A, Lamassa M, Baldereschi M, Pracucci G, Consoli D, Wolfe CD, et al. Risk factors and outcome of subtypes of ischemic stroke. Data from a multicenter multinational hospital-based registry. The European Community Stroke Project. J Neurol Sci 2006; 244:143-50. [ Links ]
40. Rabadi MH, Blau A. Admission ambulation velocity predicts length of stay and discharge disposition following stroke in an acute rehabilitation hospital. Neurorehabil Neural Repair 2005; 19:20-6. [ Links ]
T. G. Fernandes
Faculdade de Medicina
Universidade de São Paulo
Av. Dr. Arnaldo 455
São Paulo, SP 05508-000, Brasil
Submitted on 19/Dec/2011
Final version resubmitted on 29/Mar/2012
Approved on 03/May/2012