(Stroke. 1995;26:2272-2276.)
© 1995 American Heart Association, Inc.
Articles |
Measurement of Infarct Size Using MRI Predicts Prognosis in Middle Cerebral Artery Infarction
From the Division of Clinical Neuroscience, St George's Hospital Medical School, London (D.E.S., M.M.B.), and the Department of Neuroradiology, Atkinson Morley's Hospital, Wimbledon (A.G.C.), UK.
Correspondence to Dr Dawn E. Saunders, Division of Clinical Neuroscience, St George's Hospital Medical School, Cranmer Terrace, Tooting, London SW17 ORE, UK.
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Abstract |
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 Top Abstract IntroductionSubjects and MethodsResultsDiscussionReferences |
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Background and Purpose An accurate measure of the severity of ischemic insult and the resulting prognosis is needed to assess the effectiveness of new treatments for acute stroke. We studied the reproducibility and accuracy of measurements of infarct volume with MRI and correlated the measurements with outcome.
Methods Infarct volume was measured on T2-weighted images with the ANALYZE image analysis software. This technique was found to be highly accurate and reproducible.
Results Measurements of infarct volume were found to be highly accurate and reproducible. Twenty-one patients (mean age, 66.5 years; range, 28 to 90 years) with cortical middle cerebral artery territory infarcts in whom adequate data could be obtained were studied within 72 hours from onset (mean delay to MRI, 27.5 hours; range, 5 to 72 hours). The Scandinavian Stroke Scale was used to calculate a prognostic score, and clinical outcome was assessed at 3 months. Infarct volume was found to significantly predict outcome. Mean infarct volume in the independent patients was 35.7±29.7 cm3 compared with 88.3±71.3 cm3 in dependent patients and 166.5±65.9 cm3 in dead patients (F=10.52, P<.001). Patients with an initial infarct volume less than 80 cm3 were found to have a better outcome than those with larger infarct volumes. Secondary hemorrhage visible on MRI also predicted a poor outcome. In contrast, the Scandinavian Stroke Scale did not significantly predict outcome.
Conclusions The results demonstrate that measurement of the size of middle cerebral artery infarction with MRI is a useful tool in assessing prognosis and will have a valuable role in assessing new therapeutic agents.
Key Words: cerebral infarction • magnetic resonance imaging • middle cerebral artery • prognosis
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Introduction |
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TopAbstractIntroductionSubjects and MethodsResultsDiscussionReferences |
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Major advances in the treatment of acute stroke are likely to result from the application of experimental pharmacology in animal models to human stroke. Clinical trials of agents with dramatic benefit in animal models, such as N-methyl-D-aspartate antagonists, are being planned at present. Animal models are selected for reproducibility of infarct size. In contrast, the prognosis of human stroke is highly variable. One approach to the problem of patient variability in clinical trials is to recruit very large numbers of patients. An alternative that would allow the recruitment of smaller numbers into clinical trials is to accurately measure the size and severity of the ischemic insult to ensure that the treated and placebo groups are comparable. At the same time, an easily quantifiable and accurate measure of outcome is needed to assess the effectiveness of treatment. In acute stroke, accurate prognosis requires prediction of acute mortality, the chances of functional recovery in survivors, and the longer term risk of recurrence or death. Multivariate analysis has been advocated to identify and bring together those factors that make an independent contribution to the predictive outcome. Several models have been derived1 2 3 that combine variables into a regression formula. It has been shown that the more complex these models become, the less likely they are to be widely applicable4 ; moreover, these predictors bear only an indirect relation to the ischemic insult. Simple clinical variables have been shown to offer as much to clinicians as complex multivariate models.2 5 This reflects the heterogeneity of the disease and the variability in morbidity and mortality seen in subtypes of cerebral infarction.6 However, it is likely that the volume and site of infarction have a major influence on outcome. In human studies of stroke, CT scanning,7 8 single photon emission computed tomographic imaging,9 10 and magnetic resonance spectroscopy11 12 13 have not been found to be accurate and reliable predictors of stroke outcome in humans. Additional information obtained from CT has been shown to add little to predictions based on clinical data alone.14 MRI is superior to any of these techniques in imaging cerebral infarction, and modern computer software allows the areas of abnormality to be easily measured. Current trials of therapy are concentrating on the group with the worst outcome, ie, MCA territory infarcts. We therefore studied the association between the size of the infarction measured with MRI and clinical outcome in a group of patients with infarcts in a single vascular territory supplied by the MCA.
Infarct volume is used as the measure of effectiveness in pharmacological evaluation of drug treatments for stroke in animal models. The MCA occlusion model has been found to be the most reproducible method and is used widely to assess new treatments.15 The validity of stroke volume as a measure of outcome has been questioned by many researchers, since it gives no information about the clinical condition of the animal. The aim of this study was to establish whether the simple measurement of stroke volume can be used as an accurate predictor of clinical outcome in humans and also whether it is a relevant measure to use to assess the outcome of therapy in human and animal studies.
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Subjects and Methods |
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TopAbstractIntroductionSubjects and MethodsResultsDiscussionReferences |
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Twenty-three patients (mean age, 66.2 years; range, 28 to 90 years) with cortical MCA territory infarcts were studied within 72 hours of stroke onset (mean, 27.5 hours; range, 5 to 72 hours) over a period of 2 years. Patients with lacunar infarcts were excluded from the study. Patients who had a history of a previous stroke were excluded from the study, but silent infarcts found on the MRI scan did not result in removal from the study. Time from onset in those patients who suffered a stroke during the night was assumed to be when they were last known to be well. One patient was unable to lie still in the scanner, and the image quality was not sufficient to allow volume measurements. A second patient was admitted with pneumonia and underlying chronic lung disease, from which he died, and was excluded from the analysis. Twenty-one stroke patients (mean age, 66.5 years; range, 28 to 90 years) had infarct volume analysis.
MRI was carried out with a whole-body 1.5-T MRI system (Signa, General Electric) using a standard quadrature head coil. Contiguous 5-mm proton density (TR, 3500 milliseconds; TE, 19 milliseconds), T1-weighted (TR, 600 milliseconds; TE, 16 milliseconds), and T2-weighted (TR, 3500 milliseconds; TE, 95 milliseconds) scans were acquired with the fast spin-echo technique for diagnostic purposes. The presence of hemorrhage was determined with T1-weighted sequence, and if there was any doubt as to the presence of hemorrhage a CT scan was performed.
T2-weighted images were used to determine infarct volume with the volume estimator algorithm, a visual thresholding method, in the ANALYZE image software package,16 run on a Sun computer by operator 1 (D.E.S.). The volume estimator algorithm randomly superimposes markings over the entire image in a three-dimensional array of known size. The operator then selects those marks that he or she perceives to be within the infarct. Volumetric measurements made with this method on CT scans have been shown to correlate highly with measurements made by planimetry and postmortem weights.16 To validate our technique for volumetric measurements using MRI, measurements were performed on a pear and an apple, large and small cauliflower florets, and a tomato. The fruit and vegetables were imaged using contiguous 5-mm T2-weighted (TR, 3500 milliseconds; TE, 19 milliseconds) scans acquired with the fast spin-echo sequence. Volumes were calculated on three separate occasions by two independent operators. Operator 1 was experienced in MR; operator 2 had no experience in analyzing MR images but received a brief period of training before the beginning of the study. The mean volume of the fruit and vegetables was also determined using Archimedes' principle by weighing the weight of the water displaced three times. Interobserver and intraobserver variability were assessed by the two operators carrying out volume measurements on 15 arbitrarily selected patient images. Measurements were carried out on three separate occasions by each operator.
A prognostic score, which does not include imaging information, was
calculated for each patient at the time of the examination with the SSS
(Table 1
).17 Clinical
outcome was graded at 3 months by one observer using the method devised
for the International Stroke Trial.18 Patients were
divided into those that had died and those that had survived. Each
surviving patient was asked, "Do you need help from another person
to perform everyday activities?" and if they did not need help,
"Have you made a complete recovery from your stroke?" Patients
were therefore divided into three prognostic groups: dead, dependent,
and independent.
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Statistical analysis was carried out using a one-way ANOVA, correlation coefficients and regression lines, and Gabriel's test.
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Results |
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TopAbstractIntroductionSubjects and MethodsResultsDiscussionReferences |
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Accuracy of Volume Measurements
The mean volume measurements determined with the volume estimator method of the ANALYZE computer software correlated highly with the measurement made using Archimedes' principle (r=.99, P<.001). The slope of the regression line (1.16) deviated from the line of identity, and the intercept passed through -13.9 cm3, suggesting that Archimedes' principle underestimated the volume of the fruit and vegetables, presumably because of loss of water during the measurements.
Intraobserver and Interobserver Variability
The variability of the volume measurements did not deviate from
the mean measurement of stroke volume determined by the two
investigators (Fig 1). The difference of
the measurement from the mean was greatest at large volumes. There was
no correlation between the mean volume measurement and the measurement
determined by one operator. The mean intraobservational error was 7%
(range, 1% to 12%).
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Infarct Volume Results
Infarct volume data were log transformed to make the variance
uniform within the three outcome groups. The data were analyzed
by an ANOVA, and a multiple comparison procedure, Gabriel's test, was
then used to compare each pair of group means, thereby avoiding the
problem of multiple testing. The ANOVA showed that infarct volume
predicted outcome. The differences among the three prognostic
groups were highly significant: mean infarct volumes of the
independent, dependent, and dead groups were 35.7±29.7, 88.3±71.3,
and 166.5±65.9 cm3, respectively (F=10.52,
P<.001) (Fig 2). Patients
with an initial infarct volume less than 80 cm3 were found
to have a better outcome than those with larger infarct volumes. The
patient in the dependent group with a large volume of infarction was
particularly disabled and required full-time care in a nursing
home. The patient in the dead group with an initial infarct volume of
less than 80 cm3 died at 3 months from a probable cardiac
cause. The Gabriel's test showed that the mean infarct volume in each
clinical outcome group was significantly different from each other mean
at the P=.05 level. The mean infarct size of the independent
group mean was found to be different from that of the mean of the
dependent and the dead groups at the P=.01 level, but the
difference between the means in the dependent and dead groups was
not significant at this level.
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),
dependent (
), and dead (
). There is a close relationship
between infarct volume and clinical outcome so that the larger the
infarct, the worse the outcome. ANOVA shows that there is a significant
difference in the volume measurements among the three groups (F=10.5,
P=.001). Gabriel's test showed that the mean volumes in the
three groups were all significantly different.
Prognostic Score
The SSS score did not significantly predict clinical outcome. The
SSS did not have uniform variance, nor was it possible to transform it.
The rank equivalent method of one-way ANOVA, the Kruskal-Wallis
test, was used to analyze the data. There was no significant
difference in the mean SSS score among the three outcome groups
(
2=7.5, P=.1) (Fig 3).
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Clinical Findings
There was no significant difference in the age and hours from
onset that could have explained the difference among the three outcome
groups. Two patients were nonwhite and were in the independent outcome
group; the remainder were white. Two patients in the dependent group
and 1 patient in the group who died had no hemorrhage on the
initial scan but went on to develop petechial hemorrhage shown
on subsequent scans. All 4 patients with secondary hemorrhage
shown on their initial MRI scan died (Table 2). Seven of the 9 patients died in the
hospital, and the remaining 2 died at 6 weeks and 3 months. Four
patients died within the first week, 1 patient died after a
pulmonary embolus (confirmed at postmortem) at day 10, 1
patient died from pneumonia, and 1 patient who was unconscious died
from an unknown cause. The patient who died at 6 weeks had a small
infarct and had made a good recovery and had been discharged from
hospital. An MRI scan on the day before his death showed no evidence of
hemorrhage or recurrent infarction. Doppler examination had
revealed carotid artery disease. The patient who died with a large
infarct was being cared for in a nursing home. The patient who died of
a pulmonary embolus was the only patient to have a postmortem
examination.
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Discussion |
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TopAbstractIntroductionSubjects and MethodsResultsDiscussionReferences |
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This work shows that the volume of MCA infarction visible on MRI in patients within 72 hours of onset predicts outcome. The infarct volume was significantly different among the groups with three different outcomes: independent, dependent, and dead. The larger the infarct volume, the worse the outcome, and patients with an initial infarct volume of less than 80 cm3 had a better outcome than patients with larger infarct volumes. Although this is not a surprising result, it has not been demonstrated before. The findings also have the important implication that it is appropriate to use infarct volume as a surrogate end point in the assessment of therapeutic agents in the treatment of acute stroke. Furthermore, we have demonstrated that infarct size is a better prognostic indicator than the SSS score in patients with MCA infarcts.
MRI has been shown to be more sensitive than CT in patients with acute
stroke studied within 24 hours of onset. In one study, patients with
all subtypes of stroke, including primary intracerebral
hemorrhage, were included; 82% of infarcts were seen on MRI
compared with only 58% seen with CT.19 Follow-up
imaging revealed infarcts visible in 95% of patients with MRI compared
with 82% on CT scanning. Although T2-weighted scans show
evidence of acute infarct within 3 to 4 hours of onset in animal
models,20 studies in humans have concluded that MRI is not
reliable in detecting ischemic stroke before 8
hours.21 In our study, only one patient was scanned before
8 hours from onset; MRI showed a well-delineated lesion on
T2-weighted scans within 5 hours of onset (Fig 4), and this allowed accurate measurement
of infarct volume. We have shown that volume measurements of fruits and
vegetables, imaged using contiguous 5-mm T2-weighted
MRI, correlate well over a wide range with volumes determined by
Archimedes' principle. Estimates are reliable for both small objects
and objects with complex borders. This confirms that the
ANALYZE image software is particularly valuable in
measuring the volume of cerebral infarction in stroke where the border
may be irregular and follow the lines of a sulcus.
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The SSS was inspired by the work of Oxbury et al,22 who found that the best predictors of clinical outcome were level of consciousness, severity of hemiplegia, and presence of gaze palsy or gaze deviation. The SSS was selected for our study because it is a simple and straightforward prognostic indicator of clinical outcome that may be performed when patients are acutely unwell and does not include items that are difficult for physicians to assess in the acute stages of stroke, such as mental confusion, visual field defects, sensory disturbances, and urinary incontinence. It is possible that a more sophisticated score such as the Guy's Hospital prognostic score23 may have been more accurate in predicting the outcome, but such scores are more complex.
The independent group collectively was found to have more risk factors
than the dependent and dead groups, but there was no close association
of one particular risk factor with a good or bad outcome (Table 3). In other studies, diabetic stroke
patients have been shown to have a worse long-term outcome than
nondiabetic stroke patients.24 No other risk factors have
been shown to correlate with long-term outcome.7
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The observation that all patients who developed secondary hemorrhage visible on MRI died is in keeping with the previous finding that large infarct size and the presence of mass effect are useful predictors of hemorrhagic transformation.25 Death within the first week of an acute stroke is usually a direct result of the brain lesion, and the final common mechanism of early death is overwhelming brain stem compression. Deaths from 2 to 4 weeks after stroke onset are due to complications, particularly pneumonia (35%) and cardiac complications (21%).26 Hemorrhagic transformation is said to occur in 74% of all cardioembolic strokes and 30% of all ischemic strokes, as determined with CT.27 In our study, 32% had evidence of hemorrhagic transformation within 72 hours of stroke onset determined by MRI.
The nature of the pathology that is seen on T2-weighted MRI images needs to be considered. Cerebral edema is characterized by an alteration in the distribution of water within the tissue, and the pathogenesis is regarded as consisting of two broad but indistinct phases. The initial phase ("cytotoxic edema") is characterized by an increase in intracellular water arising from membrane pump failure and consequent breakdown of cell volume regulation. If this pathology is allowed to evolve uninterrupted, eventual impairment of the blood-brain barrier ensues, resulting in leakage of plasma proteins and an accumulation of water in the extracellular space. This phase is termed "vasogenic edema"; it normally occurs several hours after the insult and is characterized by an overall increase in brain water. Cytotoxic edema occurs within minutes of the insult, and reversing these changes can lead to recovery of cell function, unlike vasogenic edema. Regions of high signal intensity on T2-weighted images have been shown to correlate with pathological changes associated with regions of tissue damage defined by postmortem changes corresponding to "vasogenic edema."28 The detection of ischemic tissue in the stage of cytotoxic edema has been demonstrated by a recently developed imaging technique known as diffusion-weighted imaging. This technique is believed to detect a reduction in the movement of water between intracellular and extracellular space,29 which occurs as a result of shrinkage of the interstitial space that is known to occur during ischemia.30 The region of ischemia seen on diffusion-weighted images is larger and seen earlier than changes on T2-weighted images20 and has been shown to be reversed by N-methyl-D-aspartate antagonists.31 Although diffusion-weighted imaging may prove to be useful in the future, hardware and technical requirements are high; at the moment, it remains a research tool that is not generally available. T2-weighted imaging is available on all MR scanners, and we believe it will prove to be an important tool in the diagnosis and management of patients with acute stroke. Our results demonstrate that the imaging of infarct size with the method we have described in patients with MCA territory infarction will have a valuable role in assessing the value of new therapeutic agents.
This work is preliminary in that it has been conducted with a small number of patients; further work needs to be carried out in patients with MCA infarcts. Studies are also needed to establish whether the observation that stroke volume is important in predicting clinical outcome in MCA infarction holds for other subtypes of cerebral infarcts.
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Selected Abbreviations and Acronyms |
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Acknowledgments |
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This project was funded by the Stroke Association, England. We thank Dr Franklyn Howe and Martin Graves for their unending help in the MRI unit. We thank Dr Christine Heron for the reporting of patients' scans and Dr J.M. Bland for his help with the statistical analysis. Many thanks go to Dr David Winterbourne for his help in constructing the figures. We thank Ryan Waters for his help and diligence while in the department.
Received June 23, 1995; revision received August 24, 1995; accepted August 24, 1995.
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V. N. Thijs, M. G. Lansberg, C. Beaulieu, M. P. Marks, M. E. Moseley, and G. W. Albers Is Early Ischemic Lesion Volume on Diffusion-Weighted Imaging an Independent Predictor of Stroke Outcome? : A Multivariable Analysis Stroke, November 1, 2000; 31(11): 2597 - 2602. [Abstract] [Full Text] [PDF]
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C. Oppenheim, Y. Samson, R. Manai, T. Lalam, X. Vandamme, S. Crozier, A. Srour, P. Cornu, D. Dormont, G. Rancurel, et al. Prediction of Malignant Middle Cerebral Artery Infarction by Diffusion-Weighted Imaging Stroke, September 1, 2000; 31(9): 2175 - 2181. [Abstract] [Full Text] [PDF]
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R. Pineiro, S. T. Pendlebury, S. Smith, D. Flitney, A. M. Blamire, P. Styles, and P. M. Matthews Relating MRI Changes to Motor Deficit After Ischemic Stroke by Segmentation of Functional Motor Pathways Stroke, March 1, 2000; 31(3): 672 - 679. [Abstract] [Full Text] [PDF]
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G. W. Albers Expanding the Window for Thrombolytic Therapy in Acute Stroke : The Potential Role of Acute MRI for Patient Selection Stroke, October 1, 1999; 30(10): 2230 - 2237. [Abstract] [Full Text] [PDF]
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 V Ganesan, V Ng, W K Chong, F J Kirkham, and A Connelly Lesion volume, lesion location, and outcome after middle cerebral artery territory stroke Arch. Dis. Child., October 1, 1999; 81(4): 295 - 300. [Abstract] [Full Text]
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A. C. Pereira, D. E. Saunders, V. L. Doyle, J. M. Bland, F. A. Howe, J. R. Griffiths, and M. M. Brown Measurement of Initial N-Acetyl Aspartate Concentration by Magnetic Resonance Spectroscopy and Initial Infarct Volume by MRI Predicts Outcome in Patients With Middle Cerebral Artery Territory Infarction Stroke, August 1, 1999; 30(8): 1577 - 1582. [Abstract] [Full Text] [PDF]
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K.J. van Everdingen, J. van der Grond, L.J. Kappelle, L.M.P. Ramos, and W.P.T.M. Mali Diffusion-Weighted Magnetic Resonance Imaging in Acute Stroke Stroke, September 1, 1998; 29(9): 1783 - 1790. [Abstract] [Full Text] [PDF]
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