|Year : 2015 | Volume
| Issue : 2 | Page : 82-88
Neuroimaging of young adults with stroke in Ilorin Nigeria
Olalekan Oyinloye1, Donald Nzeh1, Olusola Adesiyun1, Mohammed Ibrahim1, Halimat Akande1, Emmanuel Sanya2
1 Department of Radiology, University of Ilorin, University of Ilorin Teaching Hospital, Ilorin, Nigeria
2 Department of Neurology, University of Ilorin, University of Ilorin Teaching Hospital, Ilorin, Nigeria
|Date of Web Publication||19-Feb-2015|
Department of Radiology, University of Ilorin, Ilorin
Source of Support: None, Conflict of Interest: None
| Abstract|| |
Background: Stroke in young adults is relatively uncommon. Computed tomography (CT) and magnetic resonance imaging (MRI) are the most valuable tools for the diagnosis of stroke. Recent data on stroke in young adults in Nigeria is sparse. The aim of this study is to document the imaging pattern in young patients aged 15-45 years with suspected cerebrovascular accidents (CVA) in the Nigerian environment.
Materials and Methods: This was a retrospective study of 69 patients aged 15-45 years, with clinical diagnosis of stroke, referred for neuro-imaging, from October 2008 to November 2013. All patients with the clinical diagnosis of stroke within this age group were recruited into the study. Images were obtained from a four slice channel general electric CT machine and a 0.2 Tesla Siemens Magnetom Concerto MRI scanner.
Results: A total of 69 patients (44 males and 25 females) were studied. Sixty out of 69 (87.0%) patients were accurately diagnosed with CVA, with 9 (13.0) cases of misdiagnoses. A total of 21 (35%) out of the 60 cases confirmed on imaging had intracerebral hemorrhage (ICH), 10 (16.7%) had subarachnoid hemorrhage (SAH) and 29 (48.3%) had cerebral infarct (CI). Hypertension was the common risk factor for all stroke subtypes. The most common location for ICH, was the basal ganglia in 8 (38.8%), while the commonest pattern for CI, was lacunar infarct in the basal ganglia (51.7%).
Conclusion: The incidence of hemorrhagic CVA (ICH and SAH combined) was slightly higher than ischemic CVA in this study. Lacunar infarcts in the basal ganglia and also ICH in the basal ganglia were the most common patterns, both are strongly linked to hypertension. A diagnostic protocol of stroke in young adults, to include neuroimaging and other ancillary investigations is advocated for stroke in young adults as some of the etiologies are treatable.
| Abstract in French|| |
Contexte: Cιrιbral chez les jeunes adultes est relativement rare. Une tomodensitomιtrie (CT) et l'imagerie par rιsonance magnιtique (IRM) sont les plus prιcieux outils pour le diagnostic d'accident vasculaire cιrιbral. Des donnιes rιcentes sur les accidents vasculaires cιrιbraux chez les jeunes adultes au Nigeria sont clairsemιes. Le but de cette ιtude est de documenter le modθle de l'imagerie dans les patients jeunes βgιs de 15 ΰ 45 ans avec prιsumιs accidents vasculaires cιrιbraux (AVC) dans le milieu nigιrian.
Matιriaux et Mιthodes: il s'agissait d'une ιtude rιtrospective de 69 patients βgιs de 15 ΰ 45 ans, avec un diagnostic clinique d'un AVC, visι pour la neuro-imagerie, entre octobre 2008 et novembre 2013. Tous les patients prιsentant le diagnostic clinique de course au sein de ce groupe d'βge ont ιtι recrutιs dans l'ιtude. Des images ont ιtι extraites d'un mιcaniques d'ordre gιnιral CT ιlectrique quatre tranche canaux et un scanner Siemens Magnetom Concerto MRI de 0,2 Tesla.
Rιsultats: Un total de 69 patients (44 hommes et 25 femmes) ont ιtι ιtudiιs. Soixante hors 69 (87,0 %) patients diagnostiquιs avec prιcision avec CVA, avec 9 (13.0) cas des ιchogrammes. Un total de 21 (35 %) sur les 60 cas confirmιs sur l'imagerie avait hιmorragie intracιrιbrale (ICH), 10 (16,7 %) avait hιmorragie sous-arachnoοdienne (HSA) et 29 (48,3 %) avait un infarctus cιrιbral (CI). L'hypertension est le facteur de risque commun pour tous les sous-types de l'accident vasculaire cιrιbral. L'emplacement plus courante pour ICH, a les ganglions de la base 8 (38,8 %), tandis que le modθle plus frιquente pour CI, Infarctus lacunaire dans les noyaux gris centraux (51,7 %).
Conclusion: L'incidence d'AVC hιmorragique (ICH et SAH combinιs) ιtait lιgθrement supιrieure ΰ l'AVC ischιmique dans cette ιtude. Infarctus lacunaire dans les noyaux gris centraux et aussi ICH dans le noyaux gris centraux ont ιtι les patrons les plus frιquents, les deux sont fortement liιs ΰ l'hypertension. Un protocole de diagnostic d'accident vasculaire cιrιbral chez les jeunes adultes, pour inclure la neuro-imagerie et autres auxiliaires enquκtes est prιconisιe pour les accidents vasculaires cιrιbraux chez les jeunes adultes comme certains des ιtiologies sont traitables.
Mots-clιs: Nigeria, neuro-imagerie, accident vasculaire cιrιbral, jeunes adultes
Keywords: Nigeria, neuroimaging, stroke, young adults
|How to cite this article:|
Oyinloye O, Nzeh D, Adesiyun O, Ibrahim M, Akande H, Sanya E. Neuroimaging of young adults with stroke in Ilorin Nigeria. Ann Afr Med 2015;14:82-8
| Introduction|| |
Stroke in young adults are relatively uncommon. The disease tends to occur in middle age patients and the elderly.  Stroke is an important cause of morbidity and mortality in young adults, especially in developing countries.  The causes of stroke in young adults involves diverse pathologies, which are less common in the older population, hence the need for thorough investigations. This is important since many of the etiologies are treatable, and early identification provides opportunity to modify some of the risk factors. ,
Recent updated definition of stroke requires neuroimaging or pathological evidence.  Confirmation that the patient had a stroke, and not a stroke mimic depends heavily on brain imaging. It is able to exclude stroke mimics such as brain tumors and subdural hematomas and to separate brain ischemia from hemorrhage. 
Computed tomography (CT) and magnetic resonance imaging (MRI) are the most valuable tools for the diagnosis of stroke. , Clinical examination alone cannot distinguish ischemic from hemorrhagic stroke or stroke mimics. CT or MRI brain imaging is required.  Brain imaging determines management decisions such as antiplatelet or thrombolytic drugs for acute stroke.  Early stroke intervention is now a practical reality in many developed countries with a significant reduction in associated morbidity and mortality,  however, this is not yet the case in many developing countries, including Nigeria. Recent data on stroke in young adults in Nigeria are scanty. Neuroimaging, especially CT is now more available in many tertiary institutions in Nigeria, including private diagnostic centers.
The aim of this study is to document the imaging pattern in young patients aged 15-45 years with suspected cerebrovascular accidents (CVA) in our environment, with a view to providing data, which can assist in developing preventive strategies and evolving therapeutic options in the management of stroke in these patients.
| Materials and Methods|| |
This was a retrospective study of 69 patients aged 15-45 years, with clinical diagnosis of stroke, referred for neuro imaging, from October 2008 to November 2013. All patients with the clinical diagnosis of stroke within this age group were recruited into the study. Patients were mainly referred from the Medical Emergency Unit of the University of Ilorin, Teaching Hospital, Nigeria. Images were obtained from a four slice channel General Electric CT machine and a 0.2 Tesla Siemens Magnetom Concerto MRI Scanner. Fifty nine patients had CT examination, 6 MRI, 4 had both CT and MRI examinations. Noncontrast brain scans were performed, and contrast injected when indicated, with 5 mm contiguous transverse sections. CT angiograms were performed in some cases of sub-arachnoid hemorrhage.
For the MRI examinations, T1- and T2-weighted spin echo and fluid attenuating inversion recovery sequences were routinely done, and time of flight when indicated. All scans were interpreted by consultant radiologists. The clinical records of patients were also retrieved from the case notes.
Information collected from patients records include: Age, sex, risk factors for stroke, such as hypertension, diabetes mellitus, history of smoking, illicit drugs, alcohol abuse, stroke in first degree relatives, heart disease associated with stroke, atrial fibrillation, congestive cardiac failure and valvular lesions.
Premature atherosclerosis was assumed if there were two or more risk factors for atherosclerotic disease in the absence of other identifiable causes of cerebral infarction (CI). All strokes were classified based on neuroimaging findings as CI, intracerebral hemorrhage (ICH) or subarachnoid hemorrhage (SAH). The location of the lesions was identified on either MRI or CT. CI were further classified as Cortical, large subcortical, or small deep (lacunar) or mixed.
Small deep infarcts (lacunar) and large subcortical infarcts were diagnosed if they were located in the basal ganglia, internal capsule, or corona radiata, with a diameter of 15 mm or less for small deep infarcts, and >15 mm for subcortical infarcts. Cortical infarcts were defined as wedge-shaped, superficial ischemic lesions in the territory of one of the major cerebral arteries or lesions in a border zone; the underlying white matter might be involved as well. Cortical infarcts are regarded as mixed if more than one pattern of lesion was seen. Descriptive statistical analysis was performed using Statistical Package for Social sciences (SSPS) version 17.
| Results|| |
A total of 69 patients (44 males and 25 females) between age 15 and 45 years were referred for imaging for clinical suspicion of stroke from October 2008 to November 2013. Mean age was 37.8 ± 7.2 years. The highest frequency of stroke occurred in the 41-45 years age category; 35 patients (50.7%) as shown in [Table 1]. Sixty out of 69 (87.0%) patients diagnosed clinically as CVD, were confirmed with either CT or MRI. and 9 (13.0) cases were false positive diagnosis clinically
Twenty-one (35%) out of the 60 cases confirmed on imaging had ICH, 10 (16.7%) had SAH and 29 (48.3%) presented with CI [Table 2]. [Figure 1] represents a case of ICH in a 40 years old hypertensive, with intraventricular extension.
|Figure 1: Axial computed tomography image showing intracerebral hemorrhage in the right basal ganglia with intraventricular extension in a 40 years old hypertensive|
Click here to view
The 29 patients with CI was further classified into subtypes of infarcts., Lacunar infarcts was noted in 15 cases (51.7%), large vessel infarcts occurred in 10 (34.4%), sub-cortical infarcts 2 (6.9%) and mixed in 2 (6.9%).
[Figure 2] represents a case of lacunar infarct in the right basal ganglia in a 45-year-old obese woman, who is diabetic, hypertensive and has hyperlipidemia.
|Figure 2: Axial computed tomography image showing lacunar infarct in the right basal ganglia 45-year-old obese female, who's diabetic, hypertensive and has hyperlipidemia|
Click here to view
Risk factors among stroke subtype are summarized in [Table 2]. Hypertension was the commonest risk factor for hemorrhagic CVA occurring in (71.4%) of patients with ICH and 34.5% of patients with CI. Diabetes was the next most common risk factor in patients with CI. Underlying heart disease was the list common risk factor identified in only 1 (3.5%) patient with CI.
Etiology of hemorrhagic cerebrovascular accidents and subarachnoid haemorrhage
The suspected etiology for ICH and SAH are summarized in [Table 3]. Hypertension was the most common etiology for ICH occurring in 71.4% of patients and aneurysm the most common in patients with SAH, occurring in 50% of patients.
Etiology for ischemic cerebrovascular accidents
The findings are summarized in [Table 4]. 44.8% of the etiology of CI were atherosclerotic, 29% of the cases were undetermined.
Location of intracerebral hemorrhage
The commonest location was in the basal ganglia 8 (38.3%), [Table 5].
Nine (13%) of patients were misdiagnosed. The commonest finding was cystic gliomas (33.3%). Two of the patients had histological confirmation. Other findings are listed in [Table 6].
[Figure 3] represents a case cystic glioma in the left parietal lobe, which was confirmed on histology in a 35 years old presenting with right hemiparesis.
|Figure 3: Axial T1-weighted magnetic resonance imaging in a 38-year-old male with 2 months history of seizures and 2 weeks history of right hemiparesis showing a left cystic glioma which was histologically confirmed|
Click here to view
| Discussion|| |
Like in older adults, stroke in younger adults is categorized as ischemic or hemorrhagic. Ischemic etiologies include cardioembolic, atherosclerotic disease, and nonatherosclerotic cerebral vasculopathies. Hemorrhagic strokes include subarachnoid and intraparenchymal types. Classification of strokes into these various subtypes accurately is through neuroimaging.  This sub typing is clearly important, because the different subtypes may have different risk factors and pathogenesis. Stroke in young adults is generally considered separately from stroke in the general population because the two generally differ in risk factor stroke etiology and prognosis.  The causes of stroke in young adults are widely diverse, and these patients need more extensive and thorough diagnostic testing than older adults.  This is important since some of the etiologies can be treated.
Hemorrhagic CVA is classified according to anatomic compartments as ICH (approximately two-thirds) or SAH (approximately one-third).  A similar pattern was observed in this study, with approximately two thirds (21 patients) with ICH and one-third, (10 patients) with SAH.
This study demonstrates a relatively high proportion of ICH (35%) in young adult patients, compared with European based studies, where ICH accounted for about 10% of all strokes in persons younger than 45 years.  This is similar to the observation of Qureshi et al.,  who observed an incidence of 30% in young black adults in the USA based study, with a similar age incidence.
Ten patients (16.7%) in this study had SAH, which is slightly higher than that observed in young black adults with CVA, in Atlanta USA with a prevalance of 12%.  More recent studies in young adults in Nigeria, did not classify hemorrhagic CVA into ICH and SAH, hence it is difficult to compare the prevalence based on these subtypes.
Owolabi and Ibrahim in Kano North Western Nigeria,  observed an incidence of 40.8% of hemorrhagic CVA in young adults and 59.2% for ischemic CVA. In this study, hemorrhagic CVA was not subdivided into SAH and ICH. This may be because only 46% had neuro-imaging. The remaining patients were classified into stroke subtypes using The World Health Organization criteria with diagnostic accuracy of 71%. 
Mustapha et al.  analyzed 27 young adults with CVA in Osogbo, Nigeria and observed a slightly higher frequency of hemorrhagic CVA. Only three patients had neuro-imaging, while others were assessed using the World Health Organization criteria. Again, hemorrhagic CVA was not sub-divided into SAH and ICH, perhaps since only few patients had neuro-imaging. However, Onwuchekwa et al. in Port Harcout found a higher incidence of ischemic CVA than hemorrhagic CVA in young adults. 
Some studies involving all age groups of patients, in which CT imaging was used, showed predominance of ischemic stroke subtype as reported by Bello et al. in Osogbo,  Ogunseyinde and Atalabi in Ibadan.  These studies corroborate predominant ischemic CVA in studies involving all age groups.
Hypertension was the commonest risk factor identified in young patients with lCH, occurring in 71.4% of patients. This is in keeping with findings in studies done in other parts of the country. ,. However, hypertension accounted for 15.2% of ICH, in studies by Bevan et al. in Vermont USA and 11% by Ruνz-Sandoval et al. in Mexico.  The etiology of ICH is linked to the location, and hypertension is strongly linked to a nonlobar location, , as was observed in this study. The commonest location of ICH (38.1%) occurring in the basal ganglia.
Furthermore, the incidence of hypertensive ICH seems to be commoner in the basal ganglia than the lobar location in young adults compared to older patients. Conversely, Bevan et al.  and Ruνz-Sandoval et al.  found the greatest frequency to occur in the lobar location, and the commonest causes were ruptured aneurysm and vascular malformation. , The lack of association between hypertension and lobar ICH is notable and suggests that lobar and nonlobar hemorrhage have different causes.  Vascular malformation, underlying tumor, underlying cavernous malformation, and hypertensive crisis induced by exogenous sympathomimetic drugs, should be excluded when ICH is lobar. 
Arteriovenous malformation and sickle cell disease were other risk factors for ICH, with the hemorrhages occurring in a lobar location, frontal and parietal lobe respectively. Eclampsia is associated with high incidence of ICH. It can occur in either the antepartum or postpartum period. The two patients with eclampsia in this study had ICH in the postpartum period. 
The majority of patients with SAH presented with aneurysmal SAH (confirmed by CT angiography), seen in 50% of cases, this is similar to findings in most studies. , The risk factors identified in this study include hypertension, smoking and alcohol abuse, which are similar to risk factors identified in other studies. ,, One of the patients had associated adult polycystic kidney disease. Though autosomal dominant polycystic kidney disease is the most common heritable disorder associated with SAH, it is found in only 2% of all patients with SAH. ,
Ischemic cerebrovascular accidents
Finding the etiology of an ischemic stroke in a young person is a true challenge for physicians. The causes of stroke in young adults are widely diverse, and these patients usually require more extensive and thorough diagnostic testing than older adults to determine the cause of underlying ischemic infarction. ,
Hypertension, smoking and diabetes were the commonest risk factors, which are pointers to premature atherosclerosis,  this is similar to patterns observed in most studies in Nigeria. , Lacunar infarcts were the commonest ischemic subtype occurring in 51.7% of patients. Large vessel infarcts occurred in 34.4%, sub-cortical infarcts 6.9% and mixed in 6.9%. Development of small-vessel occlusion at a young age in blacks may be due to enhanced susceptibility to hypertensive arteriolar damage early-onset hypertension, or delayed therapy.  This may account for the high incidence of lacunar infarcts in young adults in this study. Hypertension constituted a risk factor for just 5% of ischemic strokes, and substance abuse, arterial dissection and migraine were commoner etiologies in western countries. ,,,
Sickle cell disease was identified in four patients. Three were ischemic CVA, occurring in pediatric age group <16 years and hemorrhagic stroke in a 24 years old. Frequency of strokes in patients with sickle cell disease has been estimated to be 8-17%, and tend to occur in children and adolescent.  Infarctions can be large and involve most vascular territories, watershed infarcts and small infarcts can occur, involving the deep grey or deep white matter. ,, All the three patients in this study with ischemic stroke from sickle cell disease were imaged, with MRI and had infarcts in the carotid territories and the basal ganglia region.
Transcranial Doppler has been shown to predict children who are most at risk of stroke; it is of relatively low cost and high sensitivity. Hence it is being advocated as a routine evaluation for children with sickle cell disease. 
Three patients had HIV in this study. HIV is known to cause an intracranial small vessel vasculopathy as well as an extra-cranial large artery vasculitis. ,,, There is fairly convincing evidence that HIV is an independent risk for stroke. Potential etiologies for vascular disease among HIV-infected patients include an underlying viral myocarditis, congestive cardiomyopathy, infective endocarditis, atheroma, and thromboembolism from arterial plaques. ,,
Use of marijuana was elicited in only one patient who had extensive basal ganglia infarct. Marijuana has been linked to ischemic stroke in several case reports and seems to have a predilection for the basal ganglia. Perhaps the most convincing evidence was, illustrated by Maeto et al. who demonstrated recurrent ischemic CVA in 35-year-old male adult, with recurrent episodes of ischemic stroke after heavy smoking of marijuana, over a period of 30 months interval.
The risk factors were not identified in eight (27.5%) patients. It is difficult to identify definitive etiologies in some cases of ischaemic stroke. Moreover, some of the necessary imaging modalities and ancillary laboratory investigations are not available in our environment.
State-of-the-art diffusion weighted imaging (DWI), is not currently available as a protocol on the low field strength MRI scanner at UITH. DWI has a high sensitivity (88-100%) and specificity (86-100%) to detect ischemia, within 30 min of occurrence.
Other novel techniques, such as CT perfusion and MRI perfusion maps of relative cerebral blood flow, relative cerebral blood volume and mean transit time. These imaging methods can predict the presence of penumbra tissue that is potentially salvageable with adequate therapy.  Hence in this environment in the absence of these new imaging modalities, it is difficult to adequately diagnose and manage cases of ischemic stroke in the early phase in which thrombolytic therapy is beneficial.
One-fifth to one-third of strokes in the young may be caused by cardioembolic phenomena. Only five patients had transthoracic echocardiography in this study, with only one having a positive finding of rheumatic heart disease with clots in the left atrium. Trans esophageal-echocardiography (TEE) is usually the investigation of choice. Causes include congenital heart disease, valvular disease (including endocarditis) and arrhythmias, mitral valve prolapse and patent foramen ovale. Although some of the patients had echocardiography, TEE is not currently available in our institution. Other ancillary laboratory investigations, like detailed coagulation profile (anticardiolipin antibodies, lupus anticoagulants, protein S, protein C, activated protein C resistance, antithrombin III) may be necessary in patients without a firmly identified cause of stroke or if the patient or family members have a history of thromboses.
Alternative diagnoses or mimics based on the initial working diagnosis of stroke after history and physical examination only, will differ from final diagnoses when the true cause is discovered after neuroimaging as observed in this study. The incidence of mis-diagnosis was 13% and findings were largely brain tumors (gliomas), and cerebral abscess/effusion. Gliomas, meningiomas and hypophyseal adenomas are among the commonest primary tumors that may mimic a stroke. , The rate of stroke mimics varies between 8% and 19% in young adults with CVA.  Prevalence of stroke mimics in the general population in Nigeria is high. Bello et al. in Oshogbo, recorded 24.4%,  and an incidence as high as 42% was recorded by Ogun et al. in Ibadan.  The reasons for the high rate of misdiagnosis includes referral from nonspecialist or lack of neuro imaging facility.
| Conclusion|| |
The incidence of hemorrhagic CVA was slightly higher than ischemic CVA in this study. Hypertension was the commonest risk factor for both ischemic and hemorrhagic CVA. This may account for the relatively high incidence of lacunar infarcts and hemorrhagic CVA in the basal ganglia, which are strongly linked to hypertension. The rate of stroke misdiagnosis is high implying that diagnostic errors based solely on clinical features is significant and level of accuracy is insufficient to guide treatment decisions.
It is advocated that a well-established stroke imaging protocol be established in Nigeria, which will include neuroinaging for all patients with suspected CVA, especially young adults who have diverse stroke etiologies.
| References|| |
Bevan H, Sharma K, Bradley W. Stroke in young adults. Stroke 1990;21:382-6.
Nallino MB, Ojeda A, Uriarte AM. Ischemic stroke in young adults, A diagnostic challenge. Neuroradiology 2011;75:1-4.
Sacco RL, Kasner SE, Broderick JP, Caplan LR, Connors JJ, Culebras A, et al.
An updated definition of stroke for the 21 st
century: A statement for healthcare professionals from the American Heart Association/American Stroke Association. Stroke 2013;44:2064-89.
Weir CJ, Murray GD, Adams FG, Muir KW, Grosset DG, Lees KR. Poor accuracy of stroke scoring systems for differential clinical diagnosis of intracranial haemorrhage and infarction. Lancet 1994;344:999-1002.
Chen ZM, Sandercock P, Pan HC, Counsell C, Collins R, Liu LS, et al.
Indications for early aspirin use in acute ischemic stroke: A combined analysis of 40 000 randomized patients from the Chinese acute stroke trial and the international stroke trial. On behalf of the CAST and IST collaborative groups. Stroke 2000;31:1240-9.
Smith EE, Rosand J, Greenberg SM. Imaging of hemorrhagic stroke. Magn Reson Imaging Clin N Am 2006;14:127-40, v.
Franck G, Doyen P, Grisar T, Moonen G. Cerebral ischemic accidents in young patients, less than 45 years of age. Sem Hop 1983;59:2642-4.
Qureshi AI, Safdar K, Patel M, Janssen RS, Frankel MR. Stroke in young black patients. Risk factors, subtypes, and prognosis. Stroke 1995;26:1995-8.
Owolabi LF, Ibrahim A. Stroke in young adults: A prospective study from Northwestern Nigeria. ISRN Neurol 2012;2012:468706.
Aho K, Harmsen P, Hatano S, Marquardsen J, Smirnov VE, Strasser T. Cerebrovascular disease in the community: Results of a WHO collaborative study. Bull World Health Organ 1980;58:113-30.
Mustapha AF, Sanya EO, Bello TO. Stroke among young adults at the Lautech Teaching Hospital, Osogbo, Nigeria. Nig Q J Hosp Med 2012;22:177-80.
Onwuchekwa AC, Onwuchekwa RC, Asekomeh EG. Stroke in young Nigerian adults. J Vasc Nurs 2009;27:98-102.
Bello TO, Aremu AA, Mustapha AF, Olugbenga-Bello AI. Cranial computerised tomographic assessment of cerebrovascular disease in Osogbo, Nigeria. West Afr J Med 2010;29:323-6.
Ogunseyinde AO, Atalabi OM. Cranial computerised tomography in the evaluation of stroke in Ibadan. Niger J Clin Pract 2003:6;81-3.
Ruíz-Sandoval JL, Cantú C, Barinagarrementeria F. Intracerebral hemorrhage in young people: Analysis of risk factors, location, causes, and prognosis. Stroke 1999;30:537-41.
Ruiz-Sandoval JL, Romero-Vargas S, Chiquete E, Padilla-Martínez JJ, Villarreal-Careaga J, Cantú C, et al.
Hypertensive intracerebral hemorrhage in young people: Previously unnoticed age-related clinical differences. Stroke 2006;37:2946-50.
Jackson CA, Sudlow CLM. Is hypertension a more frequent risk factor for deep than for lobar supratentorial intracerebral haemorrhage? J Neurol Neurosurg Psychiatry
Martin JN Jr, Thigpen BD, Moore RC, Rose CH, Cushman J, May W. Stroke and severe preeclampsia and eclampsia: A paradigm shift focusing on systolic blood pressure. Obstet Gynecol 2005;105:246-54.
Juvela S, Hillbom M, Numminen H, Koskinen P. Cigarette smoking and alcohol consumption as risk factors for aneurysmal subarachnoid hemorrhage. Stroke 1993;24:639-46.
Schievink WI, Torres VE, Piepgras DG, Wiebers DO. Saccular intracranial aneurysms in autosomal dominant polycystic kidney disease. J Am Soc Nephrol 1992;3:88-95.
Provenzale JM, Barboriak DP. Brain infarction in young adults: Etiology and imaging findings. AJR Am J Roentgenol 1997;169:1161-8.
Bogousslavsky J, Pierre P. Ischemic stroke in patients under age 45. Neurol Clin 1992;10:113-24.
Zimmerman RA. MRI/MRA evaluation of sickle cell disease of the brain. Pediatr Radiol 2005;35:249-57.
Cole JW, Pinto AN, Hebel JR, Buchholz DW, Earley CJ, Johnson CJ, et al.
Acquired immunodeficiency syndrome and the risk of stroke. Stroke 2004;35:51-6.
Mochan A, Modi M, Modi G. Stroke in black South African HIV-positive patients: A prospective analysis. Stroke 2003;34:10-5.
Gillams AR, Allen E, Hrieb K, Venna N, Craven D, Carter AP. Cerebral infarction in patients with AIDS. AJNR Am J Neuroradiol 1997;18:1581-5.
Mateo I, Pinedo A, Gomez-Beldarrain M, Basterretxea JM, Garcia-Monco JC. Recurrent stroke associated with cannabis use. J Neurol Neurosurg Psychiatry 2005;76:435-7.
Intracranial tumours that mimic transient cerebral ischaemia: Lessons from a large multicentre trial. The UK TIA Study Group. J Neurol Neurosurg Psychiatry 1993;56:563-6.
Komotar RJ, Keswani SC, Wityk RJ. Meningioma presenting as stroke: Report of two cases and estimation of incidence. J Neurol Neurosurg Psychiatry 2003;74:136-7.
Ogun SA, Oluwole O, Ogunseyinde AO, Fatade B, Odusote KA. Misdiagnosis of stroke - A computerised tomography scan study. West Afr J Med 2000;19:19-22.
[Figure 1], [Figure 2], [Figure 3]
[Table 1], [Table 2], [Table 3], [Table 4], [Table 5], [Table 6]
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