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The clinical importance of white matter hyperintensities on brain magnetic resonance imaging
AbstractObjectives To review the evidence for an association of white matter hyperintensities with risk of stroke, cognitive decline, dementia, and death.Study selection Prospective longitudinal studies that used magnetic resonance imaging and assessed the impact of white matter hyperintensities on risk of incident stroke, cognitive decline, dementia, and death, and, for the meta analysis, studies that provided risk estimates for a categorical measure of white matter hyperintensities, assessing the impact of these lesions on risk of stroke, dementia, and death.Data extraction Population studied, duration of follow up, method used to measure white matter hyperintensities, definition of the outcome, and measure of the association of white matter hyperintensities with the outcome.Data synthesis 46 longitudinal studies evaluated the association of white matter hyperintensities with risk of stroke (n=12), cognitive decline (n=19), dementia (n=17), and death (n=10). 22 studies could be included in a meta analysis (nine of stroke, nine of dementia, eight of death). White matter hyperintensities were associated with an increased risk of stroke (hazard ratio 3.3, 95% confidence interval 2.6 to 4.4), dementia (1.9, 1.3 to 2.8), and death (2.0, 1.6 to 2.7). An association of white matter hyperintensities with a faster decline in global cognitive performance, executive function, and processing speed was also suggested.Conclusion White matter hyperintensities predict an increased risk of stroke, dementia, and death. Therefore white matter hyperintensities indicate an increased risk of cerebrovascular events when identified as part of diagnostic investigations, and support their use as an intermediate marker in a research setting. Their discovery should prompt detailed screening for risk factors of stroke and dementia.IntroductionAs magnetic resonance imaging has become widely available and brain magnetic resonance imaging is increasingly being carried out in various clinical settings, clinicians often have to deal with the incidental discovery of white matter lesions, appearing as hyperintensities on T2 weighted images (fig 1). In the general population the prevalence of white matter hyperintensities ranges from 11 21% in adults aged around 64 to 94% at age 82.1 2 Pathological findings in regions of white matter hyperintensity include myelin pallor, tissue rarefaction associated with loss of myelin and axons, and mild gliosis.3 4 These lesions are located in the deep white matter, typically sparing subcortical U fibres, and are often seen together with vessels affected by small vessel disease.5 The affected vessels are presumed to induce the lesions in deep white matter through chronic hypoperfusion of the white matter and disruption of the blood brain barrier, leading to chronic leakage of plasma into the white matter.3 6 7 White matter hyperintensities are more common and extensive in patients with cardiovascular risk factors and symptomatic cerebrovascular disease.8 White matter hyperintensities can be measured quantitatively and non invasively on large population samples and have been proposed as an intermediate marker, which could be used for the identification of new risk factors and potentially as a surrogate end point in clinical trials.9Fig 1 matter hyperintensities on magnetic resonance imaging (axial fluid attenuated inversion recovery sequence) in two 80 year old patients: (left) minor white matter hyperintensities; (right) extensive white matter hyperintensities predominating in periventricular region. White matter lesions are considered present if hyperintense on T2 weighted, fluid attenuated inversion recovery, and proton density images, without prominent hypointensity on T1 weighted imagesOpen in new tabSeveral studies have assessed the relation between white matter hyperintensities and risk of stroke, dementia, and death, with partly conflicting results. We systematically reviewed and meta analysed all published longitudinal studies that tested the association of white matter hyperintensities with risk of stroke, dementia, and death, both in the general population and in a hospital based setting.MethodsUsing predefined search terms we identified references through searches of PubMed from 1966 to 23 November 2009 (see web extra methods 1). We also identified papers by reviewing the reference lists of relevant articles.Study selectionStudies were limited to those in adults. We included only prospective studies with longitudinal data on the association of white matter hyperintensities with risk of stroke, dementia, cognitive decline, and death. We excluded studies if they evaluated white matter lesions only by computed tomography (because of the lower sensitivity of this method for measuring white matter lesions compared with magnetic resonance imaging10); carried out magnetic resonance imaging at the end of follow up instead of at baseline; or had a sample size of fewer than 50 patients. For studies with more than one publication describing results among overlapping groups of participants and with the same outcome measure, we included only the dataset replica van cleef and arpels necklace with the longest follow up. If the follow up period was identical we included only the dataset with the largest number of patients (see web extra methods 2).Data extractionFrom the studies we extracted data on number of participants, general population versus high risk participants, mean age, duration of follow up, characteristics of magnetic resonance imaging and definition of white matter hyperintensities, outcome definition (all strokes versus intracerebral haemorrhage or ischaemic stroke; all types of dementia versus Alzheimer's disease, vascular dementia, mixed vascular and Alzheimer's dementia; and neuropsychological measurements used to assess cognitive decline), and number of events that occurred during follow up. For the measure of the association between white matter hyperintensities and the outcome we recorded, when available, hazard ratios, odds ratios, and adjustment variables when applicable.Variable definitionWe defined studies as being in high risk populations if they were carried out in people selected for the presence of prevalent disease such as mild cognitive impairment, stroke, or other vascular events, or for the presence of a high risk factor profile. (See web extra tables 1 5 for the inclusion criteria for each study.) Stroke was defined as an acute onset focal neurological deficit of presumed vascular cause lasting at least 24 hours or interrupted by death within 24 hours. Web extra tables 1 5 show the number of events by stroke type (ischaemic versus haemorrhagic), when available. Unless specified differently (see web extra tables 1 5) we defined dementia according to the criteria van cleef and arpel necklace fake of the Diagnostic and Statistical Manual of Mental Disorders, third or fourth editions11 12; Alzheimer's disease based on the criteria of the National Institute of Neurological and Communicative Disorders and Stroke and the Alzheimer's Disease and Related Disorders Association for definite, probable, or possible Alzheimer's disease13; and vascular dementia according to the National Institute of Neurological Disorders and Stroke and copy van cleef & arpels necklace the Association Internationale pour la Recherche et l'Enseignement en Neurosciences criteria.14 Cognitive decline was defined as worsening performance on repeated neuropsychological tests. In the absence of consensus on which neuropsychological test was the most appropriate, we did not apply restrictions on type of test used. We examined separately tests of global cognitive function and tests assessing performances in specific cognitive domains (see web extra tables 1 5 for types of test used in each study).Web extra table 6 details study quality criteria, including loss to follow up, surveillance carried out for the diagnosis of incident events, description of the definition used for these events, and event subtypes. We also report the availability of effect estimates and whether the analysis took into account time to event. We calculated pooled hazard ratios using the random effects inverse variance method. In a few studies only odds ratios were available despite the longitudinal design,15 16 17 therefore we considered the odds ratios as approximations of hazard ratios.18 Significant heterogeneity was defined by a P value 2 >50%. We carried out meta analysis when at least three studies were available for the same outcome; we included only studies that used a categorical measure of white matter hyperintensities. When more than two categories were present we used the hazard ratio for the highest category compared with the lowest category. Studies for which the association of white matter hyperintensities with the outcome was studied solely in a continuous fashion (per unit increase or standard deviation increase in quantitative volume of white matter hyperintensities or semiquantitative grade for white matter hyperintensities) were not included in the meta analysis. Indeed, white matter hyperintensities were measured on completely different scales in the various cohorts, using either automated quantitative volume measures or different types of visual semiquantitative non linear volume measures. Although a sample size weighted meta analysis could be done, this would not provide a pooled effect estimate. When both adjusted and unadjusted values were available for the hazard ratio, we included the value adjusted for vascular risk factors. For studies that measured deep white matter hyperintensities and periventricular hyperintensities separately and did not provide a global risk estimate for white matter hyperintensities, we meta analysed the results for periventricular hyperintensities (see web extra methods 3). In a secondary analysis we reran the meta analysis replacing the results for periventricular hyperintensities with those for deep white matter hyperintensities. All meta analyses were done separately for population based studies and studies in a high risk population, and overall.ResultsThe initial search identified 958 articles, of which 53 met the inclusion criteria.15 16 17 19 20 21 22 23 24 25 26 27 28 29 30 31 32 33 34 35 36 37 38 39 40 41 42 43 44 45 46 47 48 49 50 51 52 53 54 55 56 57 58 59 60 61 62 63 64 65 66 67 68 This included 14 studies for stroke,15 16 19 20 21 22 23 24 25 26 27 28 29 30 20 for dementia,29 31 32 33 34 35 36 37 38 39 40 41 42 43 44 45 46 47 48 49 21 for cognitive decline,17 22 23 29 39 46 48 50 51 52 53 54 55 56 57 58 59 60 61 62 63 and 11 for mortality.15 16 23 25 28 29 64 65 66 67 68 Some studies contained data on more than one outcome. Because of an overlap with another larger study carried out in the same population on the same outcome, seven studies were excluded: two on stroke,27 28 three on dementia,43 44 45 two on cognitive decline,51 59 and one on mortality.28 Hence a total of 46 studies was included in this systematic review15 16 17 19 20 21 22 23 24 25 26 29 30 31 32 33 34 35 36 37 38 39 40 41 42 46 47 48 49 50 52 53 54 55 56 57 58 60 61 62 63 64 65 66 67 68; 12 for stroke,15 16 19 20 21 22 23 24 25 26 29 30 17 for dementia,17 29 31 32 33 34 35 36 37 38 39 40 41 42 47 48 49 19 for cognitive decline,17 22 23 29 39 46 48 50 52 53 54 55 56 57 58 60 61 62 63 and 10 for mortality.15 16 23 25 29 64 65 66 67 68White matter hyperintensities and incident strokeIncident stroke overallSix population based studies15 19 20 21 29 30 and six studies in high risk populations16 22 23 24 25 26 examined the relation between white matter hyperintensities and incident stroke (see web extra table 1). All six population based studies could be included in the meta analysis (fig 2), which showed a significant association of white matter hyperintensities with risk of stroke (hazard ratio 3.1, 95% confidence interval 2.3 to 4.1, P16 24 26 Three studies in high risk populations could not be included in the meta analysis, two because white matter hyperintensities were studied continuously only,23 25 and a third because only intracerebral haemorrhage was studied as an outcome (see web extra table 1).22 All three found a significant association of white matter hyperintensities with incident stroke.The meta analysis combining the data from population based and high risk populations yielded a significant association of white matter hyperintensities with incident stroke (3.5, 2.5 to 4.9, PIncident stroke typesFew data existed on the association of white matter hyperintensities with specific stroke types (intracerebral haemorrhage, ischaemic stroke). One community based study21 found a significant association of white matter hyperintensities with incident ischaemic stroke; another study did not observe any association of white matter hyperintensities with recurrent intracerebral haemorrhage in patients with lobar haemorrhage (see web extra table 1).22Progression of white matter hyperintensities and incident strokeOnly one study assessed the relation between progression of white matter hyperintensities and incident stroke, in 89 patients with a history of lacunar stroke, headache, or dizziness: a significantly increased risk of stroke was observed in patients with progression of white matter hyperintensities after 4.3 years compared with those with no progression.16White matter hyperintensities and incident dementiaIncident dementia overallThree population based studies29 31 32 and 11 studies in high risk populations17 34 35 36 37 38 39 40 41 47 48 examined the relation between white matter hyperintensities and incident dementia overall (see web extra table 2). Meta analysing the three population based studies yielded a significant association of white matter hyperintensities with the occurrence of all types of dementia (2.9, 1.3 to 6.3, P=0.008; fig 3).29 31 32 Six of the 11 studies done in high risk populations could be included in the meta analysis,17 37 39 41 47 48 yielding no significant association of white matter hyperintensities with incident dementia (1.4, 0.9 to 2.3, P=0.14). Four of these six studies included patients with mild cognitive impairment37 39 41 47: meta analysing these separately also did not yield any significant association (1.1, 0.8 to 1.6, P=0.46; see web extra fig 2). Not all quality criteria were satisfied for several of the studies (see web extra table 6).34 37 38 48When combining data from population based studies and high risk populations the risk of dementia associated with white matter hyperintensities was increased overall (1.9, 1.3 to 2.8, P=0.002; fig 3, also see web extra fig 3).Incident subtypes of dementiaThree population based studies31 32 33 and three studies in high risk populations41 42 49 investigated the relation between white matter hyperintensities and incident Alzheimer's disease (see web extra table 2). Only one population based study31 and two studies in high risk populations41 49 fulfilled our predefined criteria for meta analysis. Meta analysis of these yielded a significant association of white matter hyperintensities with the risk of Alzheimer's disease (see web extra fig 4).
AbstractObjectives To review the evidence for an association of white matter hyperintensities with risk of stroke, cognitive decline, dementia, and death.Study selection Prospective longitudinal studies that used magnetic resonance imaging and assessed the impact of white matter hyperintensities on risk of incident stroke, cognitive decline, dementia, and death, and, for the meta analysis, studies that provided risk estimates for a categorical measure of white matter hyperintensities, assessing the impact of these lesions on risk of stroke, dementia, and death.Data extraction Population studied, duration of follow up, method used to measure white matter hyperintensities, definition of the outcome, and measure of the association of white matter hyperintensities with the outcome.Data synthesis 46 longitudinal studies evaluated the association of white matter hyperintensities with risk of stroke (n=12), cognitive decline (n=19), dementia (n=17), and death (n=10). 22 studies could be included in a meta analysis (nine of stroke, nine of dementia, eight of death). White matter hyperintensities were associated with an increased risk of stroke (hazard ratio 3.3, 95% confidence interval 2.6 to 4.4), dementia (1.9, 1.3 to 2.8), and death (2.0, 1.6 to 2.7). An association of white matter hyperintensities with a faster decline in global cognitive performance, executive function, and processing speed was also suggested.Conclusion White matter hyperintensities predict an increased risk of stroke, dementia, and death. Therefore white matter hyperintensities indicate an increased risk of cerebrovascular events when identified as part of diagnostic investigations, and support their use as an intermediate marker in a research setting. Their discovery should prompt detailed screening for risk factors of stroke and dementia.IntroductionAs magnetic resonance imaging has become widely available and brain magnetic resonance imaging is increasingly being carried out in various clinical settings, clinicians often have to deal with the incidental discovery of white matter lesions, appearing as hyperintensities on T2 weighted images (fig 1). In the general population the prevalence of white matter hyperintensities ranges from 11 21% in adults aged around 64 to 94% at age 82.1 2 Pathological findings in regions of white matter hyperintensity include myelin pallor, tissue rarefaction associated with loss of myelin and axons, and mild gliosis.3 4 These lesions are located in the deep white matter, typically sparing subcortical U fibres, and are often seen together with vessels affected by small vessel disease.5 The affected vessels are presumed to induce the lesions in deep white matter through chronic hypoperfusion of the white matter and disruption of the blood brain barrier, leading to chronic leakage of plasma into the white matter.3 6 7 White matter hyperintensities are more common and extensive in patients with cardiovascular risk factors and symptomatic cerebrovascular disease.8 White matter hyperintensities can be measured quantitatively and non invasively on large population samples and have been proposed as an intermediate marker, which could be used for the identification of new risk factors and potentially as a surrogate end point in clinical trials.9Fig 1 matter hyperintensities on magnetic resonance imaging (axial fluid attenuated inversion recovery sequence) in two 80 year old patients: (left) minor white matter hyperintensities; (right) extensive white matter hyperintensities predominating in periventricular region. White matter lesions are considered present if hyperintense on T2 weighted, fluid attenuated inversion recovery, and proton density images, without prominent hypointensity on T1 weighted imagesOpen in new tabSeveral studies have assessed the relation between white matter hyperintensities and risk of stroke, dementia, and death, with partly conflicting results. We systematically reviewed and meta analysed all published longitudinal studies that tested the association of white matter hyperintensities with risk of stroke, dementia, and death, both in the general population and in a hospital based setting.MethodsUsing predefined search terms we identified references through searches of PubMed from 1966 to 23 November 2009 (see web extra methods 1). We also identified papers by reviewing the reference lists of relevant articles.Study selectionStudies were limited to those in adults. We included only prospective studies with longitudinal data on the association of white matter hyperintensities with risk of stroke, dementia, cognitive decline, and death. We excluded studies if they evaluated white matter lesions only by computed tomography (because of the lower sensitivity of this method for measuring white matter lesions compared with magnetic resonance imaging10); carried out magnetic resonance imaging at the end of follow up instead of at baseline; or had a sample size of fewer than 50 patients. For studies with more than one publication describing results among overlapping groups of participants and with the same outcome measure, we included only the dataset replica van cleef and arpels necklace with the longest follow up. If the follow up period was identical we included only the dataset with the largest number of patients (see web extra methods 2).Data extractionFrom the studies we extracted data on number of participants, general population versus high risk participants, mean age, duration of follow up, characteristics of magnetic resonance imaging and definition of white matter hyperintensities, outcome definition (all strokes versus intracerebral haemorrhage or ischaemic stroke; all types of dementia versus Alzheimer's disease, vascular dementia, mixed vascular and Alzheimer's dementia; and neuropsychological measurements used to assess cognitive decline), and number of events that occurred during follow up. For the measure of the association between white matter hyperintensities and the outcome we recorded, when available, hazard ratios, odds ratios, and adjustment variables when applicable.Variable definitionWe defined studies as being in high risk populations if they were carried out in people selected for the presence of prevalent disease such as mild cognitive impairment, stroke, or other vascular events, or for the presence of a high risk factor profile. (See web extra tables 1 5 for the inclusion criteria for each study.) Stroke was defined as an acute onset focal neurological deficit of presumed vascular cause lasting at least 24 hours or interrupted by death within 24 hours. Web extra tables 1 5 show the number of events by stroke type (ischaemic versus haemorrhagic), when available. Unless specified differently (see web extra tables 1 5) we defined dementia according to the criteria van cleef and arpel necklace fake of the Diagnostic and Statistical Manual of Mental Disorders, third or fourth editions11 12; Alzheimer's disease based on the criteria of the National Institute of Neurological and Communicative Disorders and Stroke and the Alzheimer's Disease and Related Disorders Association for definite, probable, or possible Alzheimer's disease13; and vascular dementia according to the National Institute of Neurological Disorders and Stroke and copy van cleef & arpels necklace the Association Internationale pour la Recherche et l'Enseignement en Neurosciences criteria.14 Cognitive decline was defined as worsening performance on repeated neuropsychological tests. In the absence of consensus on which neuropsychological test was the most appropriate, we did not apply restrictions on type of test used. We examined separately tests of global cognitive function and tests assessing performances in specific cognitive domains (see web extra tables 1 5 for types of test used in each study).Web extra table 6 details study quality criteria, including loss to follow up, surveillance carried out for the diagnosis of incident events, description of the definition used for these events, and event subtypes. We also report the availability of effect estimates and whether the analysis took into account time to event. We calculated pooled hazard ratios using the random effects inverse variance method. In a few studies only odds ratios were available despite the longitudinal design,15 16 17 therefore we considered the odds ratios as approximations of hazard ratios.18 Significant heterogeneity was defined by a P value 2 >50%. We carried out meta analysis when at least three studies were available for the same outcome; we included only studies that used a categorical measure of white matter hyperintensities. When more than two categories were present we used the hazard ratio for the highest category compared with the lowest category. Studies for which the association of white matter hyperintensities with the outcome was studied solely in a continuous fashion (per unit increase or standard deviation increase in quantitative volume of white matter hyperintensities or semiquantitative grade for white matter hyperintensities) were not included in the meta analysis. Indeed, white matter hyperintensities were measured on completely different scales in the various cohorts, using either automated quantitative volume measures or different types of visual semiquantitative non linear volume measures. Although a sample size weighted meta analysis could be done, this would not provide a pooled effect estimate. When both adjusted and unadjusted values were available for the hazard ratio, we included the value adjusted for vascular risk factors. For studies that measured deep white matter hyperintensities and periventricular hyperintensities separately and did not provide a global risk estimate for white matter hyperintensities, we meta analysed the results for periventricular hyperintensities (see web extra methods 3). In a secondary analysis we reran the meta analysis replacing the results for periventricular hyperintensities with those for deep white matter hyperintensities. All meta analyses were done separately for population based studies and studies in a high risk population, and overall.ResultsThe initial search identified 958 articles, of which 53 met the inclusion criteria.15 16 17 19 20 21 22 23 24 25 26 27 28 29 30 31 32 33 34 35 36 37 38 39 40 41 42 43 44 45 46 47 48 49 50 51 52 53 54 55 56 57 58 59 60 61 62 63 64 65 66 67 68 This included 14 studies for stroke,15 16 19 20 21 22 23 24 25 26 27 28 29 30 20 for dementia,29 31 32 33 34 35 36 37 38 39 40 41 42 43 44 45 46 47 48 49 21 for cognitive decline,17 22 23 29 39 46 48 50 51 52 53 54 55 56 57 58 59 60 61 62 63 and 11 for mortality.15 16 23 25 28 29 64 65 66 67 68 Some studies contained data on more than one outcome. Because of an overlap with another larger study carried out in the same population on the same outcome, seven studies were excluded: two on stroke,27 28 three on dementia,43 44 45 two on cognitive decline,51 59 and one on mortality.28 Hence a total of 46 studies was included in this systematic review15 16 17 19 20 21 22 23 24 25 26 29 30 31 32 33 34 35 36 37 38 39 40 41 42 46 47 48 49 50 52 53 54 55 56 57 58 60 61 62 63 64 65 66 67 68; 12 for stroke,15 16 19 20 21 22 23 24 25 26 29 30 17 for dementia,17 29 31 32 33 34 35 36 37 38 39 40 41 42 47 48 49 19 for cognitive decline,17 22 23 29 39 46 48 50 52 53 54 55 56 57 58 60 61 62 63 and 10 for mortality.15 16 23 25 29 64 65 66 67 68White matter hyperintensities and incident strokeIncident stroke overallSix population based studies15 19 20 21 29 30 and six studies in high risk populations16 22 23 24 25 26 examined the relation between white matter hyperintensities and incident stroke (see web extra table 1). All six population based studies could be included in the meta analysis (fig 2), which showed a significant association of white matter hyperintensities with risk of stroke (hazard ratio 3.1, 95% confidence interval 2.3 to 4.1, P16 24 26 Three studies in high risk populations could not be included in the meta analysis, two because white matter hyperintensities were studied continuously only,23 25 and a third because only intracerebral haemorrhage was studied as an outcome (see web extra table 1).22 All three found a significant association of white matter hyperintensities with incident stroke.The meta analysis combining the data from population based and high risk populations yielded a significant association of white matter hyperintensities with incident stroke (3.5, 2.5 to 4.9, PIncident stroke typesFew data existed on the association of white matter hyperintensities with specific stroke types (intracerebral haemorrhage, ischaemic stroke). One community based study21 found a significant association of white matter hyperintensities with incident ischaemic stroke; another study did not observe any association of white matter hyperintensities with recurrent intracerebral haemorrhage in patients with lobar haemorrhage (see web extra table 1).22Progression of white matter hyperintensities and incident strokeOnly one study assessed the relation between progression of white matter hyperintensities and incident stroke, in 89 patients with a history of lacunar stroke, headache, or dizziness: a significantly increased risk of stroke was observed in patients with progression of white matter hyperintensities after 4.3 years compared with those with no progression.16White matter hyperintensities and incident dementiaIncident dementia overallThree population based studies29 31 32 and 11 studies in high risk populations17 34 35 36 37 38 39 40 41 47 48 examined the relation between white matter hyperintensities and incident dementia overall (see web extra table 2). Meta analysing the three population based studies yielded a significant association of white matter hyperintensities with the occurrence of all types of dementia (2.9, 1.3 to 6.3, P=0.008; fig 3).29 31 32 Six of the 11 studies done in high risk populations could be included in the meta analysis,17 37 39 41 47 48 yielding no significant association of white matter hyperintensities with incident dementia (1.4, 0.9 to 2.3, P=0.14). Four of these six studies included patients with mild cognitive impairment37 39 41 47: meta analysing these separately also did not yield any significant association (1.1, 0.8 to 1.6, P=0.46; see web extra fig 2). Not all quality criteria were satisfied for several of the studies (see web extra table 6).34 37 38 48When combining data from population based studies and high risk populations the risk of dementia associated with white matter hyperintensities was increased overall (1.9, 1.3 to 2.8, P=0.002; fig 3, also see web extra fig 3).Incident subtypes of dementiaThree population based studies31 32 33 and three studies in high risk populations41 42 49 investigated the relation between white matter hyperintensities and incident Alzheimer's disease (see web extra table 2). Only one population based study31 and two studies in high risk populations41 49 fulfilled our predefined criteria for meta analysis. Meta analysis of these yielded a significant association of white matter hyperintensities with the risk of Alzheimer's disease (see web extra fig 4).
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