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Cerebral angiography and neuropsychological measurement: The twain may meet
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Cerebral Angiography and Neuropsychological Measurement: The Twain May Meet A n n e Dull Baird, Ph.D., R o u s h d y Boulos, M.D., Bharat Mehta, M.D., K e n n e t h M. A d a m s , P h . D . , M a r k W . Shatz, P h . D . , J a m e s I. A u s m a n , M . D . , P h . D . , F e r n a n d o G. D i a z , M . D . , P h . D . , a n d M a n u e l D u j o v n y , M . D . Departments of Psychiatry, Radiology, and Neurosurgery, Henry Ford Hospital, Detroit, Michigan
Baird AD, Boulos R, Mehta B, Adams KM, Shatz MW, Ausman JI, Diaz FG, Dujovny M. Cerebral angiography and neuropsychological measurement: the twain may meet. Surg Neurol 1985;23:641-50.
In a sample of 31 cerebral revascularization candidates, severity and dissemination of atherosclerosis on the cerebral angiogram were correlated with two of three global indicators of neurobehavioral impairment. Additionally, the angiographic rating was correlated with age and with an index of medical risk factors, but not with duration of the longest symptomatic episode. It seems likely that several variables, particularly collateral circulation, help to determine whether a given pattern of stenoses results in neuropsychological dysfunction and what type of behavioral deficit occurs. In many cases, the configuration of neuropsychological test scores may not directly mirror the pattern of cerebrovascular stenoses. KEYWORDS: Cerebral angiography; Cerebral arteriosclerosis; Cerebral ischemia; Cerebrovascular disorders; Cerebral revascularization; Psychological testing
Cerebral angiography and neuropsychological testing are at opposite ends of the spectrum of tools used in diagnostic evaluation of candidates for superficial temporal artery-middle cerebral artery bypass and other cerebral revascularization procedures. Four-vessel arteriography is the essential procedure for identifying the severity and loci of cerebrovascular occlusive disease, the primary indication for these microsurgical procedures. It is the sine q u a non for surgical planning. It is well known that neuroradiologic techniques yield the most reliable information about structural lesions in the cerebrovasculature as well as about the direction and patency of flow through the major cerebral vessels. However, inAddress reprint requests to: Anne Dull Baird, Ph.D., Henry Ford Hospital, Neuropsychology, K-11, 2799 West Grand Boulevard, Detroit, Michigan 48202.
© 198~ by Elsevier Science Publishing Co., Inc.
formation about the rate and quantity of the vascular supply to cerebral tissue is much less exact or direct. In contrast, neuropsychological testing is most useful in delineating the patient's behavioral functioning in meeting the demands of a range of standardized cognitive, perceptual, and motor tasks. The patient's life experiences, education, general health, and systemic and regional metabolic factors co-determine performance, in addition to neural infra- and macrostructures. Neuropsychological testing maps behavior in a detailed, even intricate way, but only indirectly reflects integrity of major neuroanatomic structures and neurovascular patency. Thus, neuropsychological testing and cerebral angiography are complementary procedures that together give much valuable information about structural and functional status in patients with stroke. In current work, the long-term goal is the development of predictive indices that will tell us which patients are most likely to show neurobehavioral improvement after neurosurgical anastomosis or endarterectomy for cerebral ischemia. Specifically, a sample of 80 cerebral revascularization candidates is being followed up for 18 months after operation. The hypothesis is that patients with a moderate level of behavioral impairment preoperatively are more likely to show improvement after operation. It is also likely that medical risk factors for cerebrovascular disease, dissemination of atherosclerosis, lateralization of symptoms and neurobehavioral impairment, and the type of neurosurgical intervention will affect postsurgical outcome. Studies of regional cerebral blood flow and nuclear magnetic resonance spectra will enhance this work by elucidating the role of metabolic factors in postoperative behavioral changes. As part of this work, it is necessary to gather detailed, consistently reported information from cerebral angiography. Such data permit quantitative as well as qualitative combination with other measures and aid in analysis of groups of patients as opposed to individual case 0090~'019/85/$3.30
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studies. Despite the great heterogeneity of cerebral revascularization candidates and the consequent risks of overgeneralization, group analyses are necessary if we are to extract reliable conclusions from accumulated experience in evaluating and treating patients with cerebral ischemia. From a neuropsychologist's point of view, correlations with angiographic data are necessary to establish firmly the strength and type of linkages between behavioral data and the structural pathology underlying cerebrovascular occlusive disease. Studies correlating psychological data with regional cerebral blood flow and clinical symptoms provide indispensible insights into hemodynamics and behavior [ 11], but cannot substitute for the structural data gleaned from angiography. This is an obvious distinction but one not always drawn, par-
ticularly in the psychological literature. Moreover, neither regional cerebral blood flow procedures nor angiography provides definitive information on metabolism - - a parameter of brain functioning likely to co-vary most directly with behavior. Psychological and neurological studies of structure-function relationships have drawn differing conclusions about their strength. Peerless et al [13] cite many references that show an association between multiple-vessel occlusions and dementia; they also list others that indicate that multiple-vessel disease is not always correlated with global behavior dysfunction. Kelly et al [9] found that presence of ulceration on angiography was not correlated with neurobehavioral impairment in candidates for carotid endarterectomy. Although mean scores are in the expected direction, Duke et al [5]
Angiogrophic Ratings of Cerebral Revosculorization Candidates Stenoses in Major Vessels Code:
0 or blank
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I
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I% to 2 9 . 9 9 %
2
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not enough information to rate, for example, artery not
stenosis
injected or not well-visualized instructions:
/
List codes in the order the arteries are listed:
/
Left common carotid artery, left external carotid artery, left internal carotid artery Right common carotid artery, right external carotid artery, right internal carotid artery Left anterior cerebral artery, left middle cerebral artery
i II.
Right anterior cerebral artery, right middle cerebral artery Left vertebral artery, right vertebral artery, basilar artery Left posterior cerebral artery, right posterior cerebral artery
Intracranial Radiographic Opacification Code:
0 or blank
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adequate radiographic opocificotion
I
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focal area of decreased radiographic opacification
2
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multifocal
or
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decrease
in
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opocification in the branches and small vessels 9
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not enough information to rate
Left cerebral hemisphere (List any focal area of decreased opocification) Right cerebral hemisphere (List any focal area of decreased opacification) Brainstem end cerebellor area (List any focal area of decreased opocification)
Figure 1. Cerebral angiogram rating sheet for cerebral revascularization candidates.
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found no differences between candidates for carotid endarterectomy with large vessel atherosclerosis on angiography versus those patients with only small-vessel disease on angiography. In contrast, in their studies of candidates for carotid endarterectomy, H o r n e and Royle [7] stated that severity of atherosclerosis did relate to severity of psychological impairment; Jacobs et al [8] found that patients with at least 75% reduction in crosssectional lumen of the carotid arteries were more impaired than patients with only 2 5 % stenosis. For these studies, the objective was an angiographic measure that would provide detailed information on stenoses in the major cerebral vessels and reflect the distinctions and cutoffs most reliably and frequently made by neuroradiologists in studying candidates for extracranial-intracranial arterial anastomoses and other revascularization procedures. In examining the utility of this measure, the strategy was to look first at general relationships between atherosclerotic involvement and neuropsychological impairment. T h r e e neuropsychological measures thought to be sensitive to disturbances in higher cortical functioning were included. Measures of severity and dissemination of atherosclerosis and of intracranial opacification were devised to quantify information from cerebral angiography. Statistical analyses using these general radiographic and behavioral mea-
1. Description of.31 Cerebral Revascularization Candidates
Table
Age Mean Standard deviation Education (years) Mean Standard deviation G e n d e r (n) Male Female Race (n) Caucasian Black Subsequent surgery (n) Unilateral carotid endarterectomy Bilateral carotid endarterectomy Unilateral S T A - M C A bypass Bilateral S T A - M C A bypass Carotid endarterectomy and contralateral S T A - M C A bypass Vertebral-carotid transposition N o surgery Longest s y m p t o m prior to assessment (n) N o definite clinical s y m p t o m s Transient ischemic attack Reversible ischemic neurological deficit Stroke STA-MCA, superficial temporal artery-middle cerebral artery.
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Table 2. Summary Stenotic Rating and Related Variables." Descriptive Statistics Summary stenotic rating (n = 31 ) Median Range Medical index (n = 23) Median Range Wechsler Memory Quotient (n = 29) Mean Standard deviation Average impairment rating (n = 26) Mean Standard deviation Digit symbol scaled score (n = 29) Mean Standard deviation
9 2-26 10 4-20 99.7 15.6 1.64 0.69 6.5 2.6
sures suggest this angiographic scale may be useful in clinical studies of cerebral revascularization.
Method
Angiographic Ratings Figure 1 shows the rating system. These ratings were based on four-vessel studies that usually used a femoral injection, unless significant peripheral vascular disease made this site unfeasible. In this case, brachial injection of dye was performed. To rate the major vessels, a stenotic rating system was designed; to tap information on filling within the small intracranial vessels, a radiographic opacification rating system was devised.
60.6 11.5
Summary Stenotic Rating 12.0 3.8 17 14 24 7 10 2 7 1 2 1 8 1 16 5 9
This form is based partly on the index developed by Bloor et al [2]. However, there are two important differences. First, it was decided to avoid imposing a weighting system upon the ratings until sufficient data and experience allowed careful scaling. Secondly, explicit ratings of all the major vessels were deemed desirable for future study of laterality, caudality, and clinical syndromes associated with specific arteries. The current scale is the result of several earlier versions that Table 3. Spearman's p Correlations u,ith the Summary Stenotic Rating Average impairment rating Digit symbol scaled score Wechsler m e m o r y quotient Medical index Age S y m p t o m duration ~p < 0.05. ~'p < 0.001~ 'Not significant.
0.41Y -0.57 h -
0.02'
0.47 ~ 0.32 ~ 11.16'
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included more complicated finer-grained coding systems, which seemed unwieldy, unreliable, and potentially unsuitable for group analysis. Moreover, the more complex the coding system, the more likely some information would be missing for a given subject and complicate quantification o f data. In practice, the rater often writes in additional information o f note, such as evidence of ulceration. The cutoffs listed for the ratings are those ranges commonly used by neuroradiologists. Roughly, the rating o f I corresponds to minimal stenosis;
Figure 2. Patient 1 illustrates severe and widespread stenosis coexistent with marked behavioral impairment. This 57-year-old man suffered a stroke involving the left arm and leg approximately 14 weeks before angiography and neuropsychological testing. A t the time of the ictus, he also noted some dizziness. Testing showed bilateral moderate-to-severe tactile and motor deficits with mild-to-moderate decrements in intellectual functioning. This anteroposterior projection was taken after left common carotid artery injection. It shows 7 0 % - 8 0 % stenosis of the left internal carotid artery.
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the rating of 2 indicates mild-to-moderate narrowing, the rating of 3 is in the range where stenosis is thought to be hemodynamically significant [6,10]; a rating of 4 indicates complete occlusion. T o obtain the summary stenotic rating used in these analyses, the ratings for all 15 vessels were summed up. In cases in which more than one site of stenosis within a vessel was seen, the most severe stenosis was rated.
Intracranial Radiographic Opacification In part, this scale reflects the system for quantification of collateral flow developed by T h o m p s o n et al [18]. Our ratings are more general, however, and inferences as to adequacy and quantity of flow are not made: only radiographic opacification is rated. It was felt that more precise judgments, for example, about opacification of subsystems of circulation, might not be reliable. Again, the three ratings, for each hemisphere and the brainstem, were summed to obtain the index of radiographic opacification.
Figure 3. Patient I. This projection was obtained after right subclavian injection and illustrates severe atherosclerotic disease in the vertebrobasilar system.
Cerebral Angiography and Neuropsychology
Medical Index We composed a rough index of stroke-related medical risk factors based on information presented in Stroke Risk Handbook [17]. We decided against use of the stroke risk profile from the Handbook because this measure was developed for use in populations that had not yet suffered transient ischemic attack or stroke. The presence of the 11 factors was recorded, weighted, and summed. Weights were assigned according to the relative importance given the factor in the Stroke Risk Handbook. Three points were accredited for STT wave abnormality, cardiac block, or left ventricular hypertrophy; cardiac arrhythmia; or history of cardiac or peripheral vascular disease. The two-point indicators were a current cigarette smoking habit; elevated serum cholesterol; historical or laboratory evidence of diabetes; and abnormal hematocrit, hemoglobin, or coagulation studies. Cardiac enlargement, elevated serum uric acid, and elevated serum triglycerides were one-point indicators. From one to five points were assigned for elevated systolic blood pressure, depending on severity.
Neurobehavioral Measures The Wechsler Memory Quotient, the Wechsler Adult Intelligence Scale (WAIS) digit symbol scaled score, and
Figure 4. Patient 1. Obtained following right common carotid injection, this film reveals severe stenosis in the right internal carotid artery with possible ulceration.
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the average impairment rating were examined as general indicators of adaptive functioning. The average impairment rating is an index of general neuropsychological impairment similar to the rating presented by Russell et al [ 16]. The present average impairment rating is the arithmetic mean of ratings derived from scores on eight tests, the tokens test, the WAIS digit symbol subtest, the trail making test--part B, the sensory-perceptual impairment rating, the finger tapping test, the grip strength test, the static steadiness test, and the foot tapping test. Because the impairment rating is based on multiple mea-
Figure 5. Patient 2 shows minimal behaz'ior impairment correlated with ~,ery mild stenosis u,ithin the cerebro1~asculature. The most significant angiographic finding was a left subclavian steal. This 42-year-old woman had a 3 I/2-month history of transient numbness and u'eakness in the right side of the body. a vertiginous sensation, and "u'hite spots" in both visual fields. After left common carotid injection, reflux into the left l,ertebra/ and /eft subclavian arteries u'as noted.
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sures in different behavioral domains, it is perceived to be a reliable, sensitive measure of overall neurobehavioral status. Although the WAIS digit symbol subtest and the Wechsler M e m o r y Scale initially were developed as measures o f more specific areas of functioning, research has suggested strongly that both measures in fact are general indicators of cerebral dysfunction [ 12,15]. In particular, the digit symbol subtest score has been shown to be sensitive to cerebral lesions, regardless of locus.
Subjects O f 39 angiograms rated, in eight patients one or more vessels could not be rated because of poor visualization. Thus, the present sample consists of 31 candidates for cerebral revascularization, who underwent angiography and partial or full neuropsychological testing. Consistent with the selection criteria usually employed for cerebral revascularization, most o f these patients are very mildly to moderately impaired on neuropsychological tests and present with transient ischemic attacks or mild strokes, rather than with severe fixed deficits, as shown in Tables 1 and 2. Figure 6. Patient 2. A further illustration of left subclavian steal, as well as minimal narrowing of the left external carotid and left internal carotid arteries. Left common carotid injection.
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After giving written consent on standard institutional forms for invasive procedures, all patients underwent cerebral angiography as part of a diagnostic work-up for symptoms suggestive of cerebrovascular disease. Subjects signed consent forms for neuropsychological follow-up as part of a research protocol last approved by the institutional human rights committee on February 23, 1984.
Results
Summary Stenotic Rating and Neurobehavioral Measures The average summary stenotic rating was 10.9, with a mode of 7, and a median of 9. T h e r e is some positive Figure7. Patient3. This case exemplifies incongruence between the stenotic ratings and neuropsychological test performance. Eight years before assessment this 74-year-old woman had a stroke involving the right side of her body and her speech. Shortly thereafter, she lost the vision in her right eye and began to experience transient episodes of dizziness and some change in consciousness. Despite bilateral carotid occlusions and severe atherosclerosis in the left subclavian and vertebral arteries, only mild tactile, motor, and cognitive deficits were noted on testing. This aortic arch study shows left common carotid artery occlusion, right internal carotid artery occlusion, and severe atherosclerosis in the left subclavian.
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are diverse in terms of severity and type of symptomatology and behavioral impairment, this lack of variability underlines the fact that radiographic opacification cannot be equated with adequate blood flow, blood volume, or metabolic functioning. Patient Studies
The correlations between neurobehavioral impairment and the summary stenotic rating are modest, and there is substantial variation in the strength of this relationship from patient to patient. T o emphasize this variability, four patients were selected from this sample: Patients 1 and 2 illustrate a high positive relationship between neurobehavioral impairment and severity and dissemination of atherosclerosis; patients 3 and 4 show a negative correlation between angiographic involvement and deficits on neuropsychological tests, that is, in the direction op-
Figure 9. Patient 3. Both anterior cerebral and middle cerebral arteries fill via the posterior communicating arteries after right brachial injection.
Figure 8. Patient 3. Right brachial injection reveals bilateral internal carotid artery occlusion.
skewing on the scores. Because equality of intervals between rating points cannot be assumed, the angiographic ratings were treated as ordinal-level data. Spearman's p correlation coefficients between the summary stenotic rating and the three neurobehavioral measures were significant for two out of three neuropsychological test scores. Significant correlations also were obtained between the summary stenotic rating and the patient's age, and score on a weighted index of medical risk factors. The correlation between the duration of the patient's longest symptomatic episode and the summary stenotic rating was not significant. The correlation coefficients appear in Table 3. Radiographic Opacification
For 29 of 30 patients rated, radiographic opacification was judged to be adequate for both cerebral hemispheres and the brainstem region. Thus, variability was insufficient for statistical analysis. In that these patients
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posite to prediction. Angiographic results are pictured in Figures 2 - 1 1 ; the stenotic ratings and a subset of the neuropsychological data appear in Table 4.
Discussion The results of these analyses suggest that these angiographic ratings relate to several of the dimensions thought to be important in cerebrovascular occlusive disease-Figure 10. Patient 4. Whereas neuropsychological assessment revealed a moderate level of behavioral impairment, the stenotic ratings showed only mild stenosis of the left common carotid and about 4 0 % narrowing of the left internal carotid artery with possible ulceration. Five months before presentation, this 62-year-old, college-educated man experienced sudden onset of dysphasia and paralysis of the right arm and continued to note residual difficulties in speech, memory, and coordination. This picture was taken after left common carotid artery injection.
Baird et al
neurobehavioral status, age, and medical risk factors in stroke. Moreover, most four-vessel studies appear to yield information sufficient for these ratings: this practical advantage eases the way to more reliable, generalizable group studies, compared with case studies that use no formal angiographic rating system. Further analyses are necessary to determine whether these ratings also reflect laterality of symptoms and lateralization on neuropsychological tests, as well as caudality of symptoms. An earlier study [1] used angiographic reports and site o f surgery to decide whether the carotid or vertebrobasilar arterial system was primarily involved by atherosclerosis. N o differences between the pattern of neuropsychological findings in the anterior and posterior groups were found. Thus, it would not be surprising to find that neurobehavioral data relate globally to cerebral angiographic findings but may not Figure I I. Patient 4. Further illustration of a probable ulcerated placque in the left internal carotid artery and the left carotid bulb as seen on left common carotid injection.
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Table 4. Angiographic and Neuropsychological Data for Four Patients Case 1 Stenotic ratings Left c o m m o n carotid artery Left external carotid artery Left internal carotid artery Right c o m m o n carotid artery Right external carotid artery Right internal carotid artery Left anterior cerebral artery Left middle cerebral artery Right anterior cerebral artery Right middle cerebral artery Left vertebral artery Right vertebral artery Basilar artery Left posterior cerebral artery Right posterior cerebral artery Opacification ratings Left cerebral hemisphere Right cerebral hemisphere Brainstem and cerebellar area Neuropsychological data Average impairment rating T o k e n test score Digit symbol scaled score Trails B seconds Sensory-perceptual exam Grip strength dominant hand (kg) b N o n d o m i n a n t hand Finger taps/second dominant hand N o n d o m i n a n t hand Static steadiness D o m i n a n t hand time ~ D o m i n a n t hand count N o n d o m i n a n t hand time N o n d o m i n a n t hand count Foot taps/second dominant foot N o n d o m i n a n t foot Wechsler M e m o r y Quotient
Case 2
Case 3
Case 4
1
0
4
2
2 3
1 l
4 4
0 2
l 1
0 0
2 ~
0 0
3 0
0 0
4 0
0 0
1
0
0
0
0 0 4 3 3 0 0
0 0 0 0 0 0 0
0 0 3 l 0 0 0
0 0 0 0 0 0 0
0 0 0
0 0 0
0 0 0
0 0 0
2.71 31(1) a 4(3) 186(4) (3) 27(2) 23(2) 1.9(4) 2.8(3) 58.06(2) 33(0) 54.85(2) 50(0) d -93
1.13 36(0) 10(1) 106(2) (0) 30(1) 29(1) 3.9(3) 3.8(3)
1.38 34(1) 5(2) 186(4) (0) 27(1) 26( 1 ) 5.4(0) 4.5(0)
26.94(1) 142(1) 26.60(1) 156(l ) 3.1(1) 2.9(1) 119
22.86(1 ) 136(1) 26.20(1) 130(1) 2.7(1) 2.2(2) 116
2.38 18(3) 6(2) 186(4) (3) 45(1) 44(1) 3.2(3) 3.4(3) 18.03(1) 61(1) 15.27(1) 64(0) 2.7(1) 2.3(2) 78
~The parenthesized scores are impairment ratings. An impairment rating of 0 indicates high normal performance; l suggests normal performance; 2 represents mild impairment; 3, moderate impairment; and 4, severe impairment. briand and foot preference were determined by verbal questioning. 'Time and count are measures of cumulative seconds of contact and number of contacts with the rim of a hole in a metal plate. In the static steadiness test, the subject is asked to keep a stylus inserted in a hole without touching the edge of the hole. '~Not administered because of poor balance.
relate on a point-by-point basis. This hypothesis is consistent with evidence that symptoms do not occur significantly more frequently in patients with stenosis when they are compared with age-matched subjects without stenosis [4]. This speculation also is compatible with reports of steal phenomena in which a stenosis in the vertebrobasilar system may produce symptoms usually associated with the carotid arterial system [19]. In this sample, age, medical risk factors, and neuropsychological impairment all correlated with dissemination and severity of atherosclerosis. Separate analyses revealed that age and medical risk factors, as well as symptom duration, also were correlated with behavioral
impairment. Thus, the relationship between the stenotic rating and neuropsychological impairment cannot be assumed to be independent of these other correlations. As a larger sample is accumulated, multiple regression analyses may be used to ascertain these interconnections. In this sample, variation in radiographic opacification did not relate to variation in neurobehavioral impairment. The absence of a relationship may have been due to the lack of variability in radiographic opacification: Only one angiogram was rated as showing inadequate intracranial opacification. Moreover, as illustrated by the four selected patients, the relationship between the stenotic and the behavioral indices is far from consistent
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across patients. Likely, this variability is not due entirely to random error but rather reflects other variables that systematically moderate the relationship between stenosis and behavioral dysfunction. Several variables deserve consideration as moderators. First, collateral circulation, general cardiovascular condition, and locus of stenosis [4,6] are believed to be important in determining severity of ischemia. Hence, these factors may influence severity of neuropsychological impairment. Secondly, stenosis at some sites may be more likely to produce marked impairment on neuropsychological tests. For example, even though stenosis was very limited in severity and dissemination in patient 4, who was moderately impaired, the principal site of involvement was the internal carotid artery feeding the cerebral hemisphere dominant for speech. Research in regional cerebral blood flow has yielded results and hypotheses that parallel those in the present report. In one study, comparisons between percent hemispheric differences in blood flow and judgments of laterality of neuropsychological findings showed strong agreement [3]. In another study, ratings of regionality of asymmetries in cerebral blood flow did not correspond with the site of stenosis on the angiogram [14]. However, there was a relationship between the overall presence or absence of abnormalities in regional cerebral blood flow and on angiography. Measurements such as regional cerebral blood flow may be more directly related to function, and hence to neuropsychological measures than are the stenotic ratings, which pertain mostly to static or slowly changing obstructions in the cerebrovasculature. The stenotic rating system presented herein seems to provide a useful way of quantifying and comparing neuroradiologic results across groups of cerebral revascularization candidates. Global indicators of neurobehavioral impairment relate to severity and dissemination of atherosclerosis in the cerebrovasculature, even though many of these stenoses probably do not produce clinical symptoms. Additional work is likely to clarify this relationship. In particular, possible intervening variables, such as regional differences in rate and volume of blood flow, metabolic function, and patterns of collateral circulation, require further study. The long-term goal is to learn how severity and dissemination of atherosclerosis moderate neuropsychological changes after cerebral revascularization. We wish to express appreciation to Ms. Gall Bruno for secretarial assistance in obtaining angiographic data, to Ms. Cathleen McDonald for her careful work in testing these patients and in organizing the data, and to Dr. Gregory G. Brown for critical comments and continuing collaboration. Research on candidates for cerebral revascularization is supported by NS17116-01.
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References 1. Baird AD, Adams KM, Shatz MW, Brown GG, Diaz F, Ausman JI. Can neuropsychological tests detect the sites of cerebrovascular stenoses and occlusions? Neurosurgery 1984;14:416-23. 2. Bloor B, Asli R, Nugent R, Majzoub H. Relationship of cerebrovascular reactivity to degree of extracranial vascular occlusion. Circulation 1966;33(suppl 2):28-34. 3. Brown GG, EwingJR, Weiss SM, Robertson WM, Welch KMA. Neuropsychological correlates of regional cerebral blood flow in candidates for extracranial to intracranial bypass. J Cereb Blood Flow Metab 1983;3(suppl L):$594-5. 4. DeLand FH. Cerebral radionuclide angiography. Philadelphia: WB Saunders Co, 1976:210. 5. Duke RB, Bloor BM, Nugent GR, Majzoub HS. Changes in performance on WAIS, trail making test and finger tapping test associated with carotid artery surgery. Percept Mot Skills 1968;26:399-404. 6. Einsiedel-Lechtape H, Kleihues P. Pathology of cerebral vascular insufficiency. In: Newton TH, Ports DG, eds. Radiology of the skull and brain. Vol 3. St Louis: CV Mosby, 1977:3173-96. 7. Home DJ, Royle JP. Cognitive changes after carotid endarterectomy. Med J Aust 1974;1:316-7. 8. Jacobs LA, Ganji S, Shirley JG, Morrell RM, Brinkman SD. Cognitive improvement after extracranial reconstruction for the low flow-endangered brain. Surgery 1983;93:683-7. 9. Kelly MP, Garron DC, Javid H. Carotid artery disease, carotid endarterectomy, and behavior. Arch Neurol 1980;37:743-8. 10. Kilgore BB, Fields W. Arterial occlusive disease. Section I1. Arterial occlusive disease in adults. In: Newton TH, Potts DG, eds. Radiology of the skull and brain. Vol 2, book 4. St Louis: CV Mosby, 1974:2310-43. 11. Kohlmeyer K. Studies of rCBF on neuropsychological disorders caused by acute cerebrovascular accidents in the major hemisphere. In: Langfitt TW, McHenry LC, Reivich M, Wollman H, eds. Cerebral circulation and metabolism. New York: SpringerVerlag, 1975:269-71. 12. Lezak MD. Neuropsychological assessment. New York: Oxford University Press, 1976:2 L4 13. Peerless SJ, Chater NL, Ferguson GF. Multiple-vessel occlusions in cerebrovascular disease--a further followup of the effects of microvascular bypass on the quality of life and the incidence of stroke. In: Schmiedek P, ed. Microsurgery for stroke. New York: Springer-Verlag, 1977:251-9. 14. Robertson WM, Welch KMA, EwingJR, Weiss S. Correlation of cerebral angiographic lesions with regional cerebral blood flow (abst). Presentation to the ninth international joint conference on stroke and cerebral circulation of the American Heart Association, Tampa, Florida, February 16-18, 1984. Stroke 1984;15:186. 15. Russell EW. The pathology and clinical examination of memory. In: Filskov SB, Boll TJ, eds. Handbook of clinical neuropsychology. New York: John Wiley and Sons, 1981:287-8. 16. Russell EW, Neuringer C, Goldstein G. Assessment of brain damage: a neuropsychological key approach. New York: Wiley-Interscience, 1970:1-161. 17. Stroke risk handbook: estimating risk of stroke in daily practice. New York: American Heart Association, 1974. 18. Thompson JR, Rouhe graphic cerebral blood candidates. In: Fein J, tomoses for cerebral 1978:145-57.
SA, Austin GM, Simmons CR. Angioflow patterns in STA-MCA anastomosis Reichman OH, eds. Microvascular anasischemia. New York: Springer-Verlag,
19. Toole JF. Management of transient ischemic attacks. In: Scheinberg P, ed. Cerebrovascular diseases. New York: Raven Press, 1976:23-30.
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Cerebral Angiography and Neuropsychological Measurement: The Twain May Meet A n n e Dull Baird, Ph.D., R o u s h d y Boulos, M.D., Bharat Mehta, M.D., K e n n e t h M. A d a m s , P h . D . , M a r k W . Shatz, P h . D . , J a m e s I. A u s m a n , M . D . , P h . D . , F e r n a n d o G. D i a z , M . D . , P h . D . , a n d M a n u e l D u j o v n y , M . D . Departments of Psychiatry, Radiology, and Neurosurgery, Henry Ford Hospital, Detroit, Michigan
Baird AD, Boulos R, Mehta B, Adams KM, Shatz MW, Ausman JI, Diaz FG, Dujovny M. Cerebral angiography and neuropsychological measurement: the twain may meet. Surg Neurol 1985;23:641-50.
In a sample of 31 cerebral revascularization candidates, severity and dissemination of atherosclerosis on the cerebral angiogram were correlated with two of three global indicators of neurobehavioral impairment. Additionally, the angiographic rating was correlated with age and with an index of medical risk factors, but not with duration of the longest symptomatic episode. It seems likely that several variables, particularly collateral circulation, help to determine whether a given pattern of stenoses results in neuropsychological dysfunction and what type of behavioral deficit occurs. In many cases, the configuration of neuropsychological test scores may not directly mirror the pattern of cerebrovascular stenoses. KEYWORDS: Cerebral angiography; Cerebral arteriosclerosis; Cerebral ischemia; Cerebrovascular disorders; Cerebral revascularization; Psychological testing
Cerebral angiography and neuropsychological testing are at opposite ends of the spectrum of tools used in diagnostic evaluation of candidates for superficial temporal artery-middle cerebral artery bypass and other cerebral revascularization procedures. Four-vessel arteriography is the essential procedure for identifying the severity and loci of cerebrovascular occlusive disease, the primary indication for these microsurgical procedures. It is the sine q u a non for surgical planning. It is well known that neuroradiologic techniques yield the most reliable information about structural lesions in the cerebrovasculature as well as about the direction and patency of flow through the major cerebral vessels. However, inAddress reprint requests to: Anne Dull Baird, Ph.D., Henry Ford Hospital, Neuropsychology, K-11, 2799 West Grand Boulevard, Detroit, Michigan 48202.
© 198~ by Elsevier Science Publishing Co., Inc.
formation about the rate and quantity of the vascular supply to cerebral tissue is much less exact or direct. In contrast, neuropsychological testing is most useful in delineating the patient's behavioral functioning in meeting the demands of a range of standardized cognitive, perceptual, and motor tasks. The patient's life experiences, education, general health, and systemic and regional metabolic factors co-determine performance, in addition to neural infra- and macrostructures. Neuropsychological testing maps behavior in a detailed, even intricate way, but only indirectly reflects integrity of major neuroanatomic structures and neurovascular patency. Thus, neuropsychological testing and cerebral angiography are complementary procedures that together give much valuable information about structural and functional status in patients with stroke. In current work, the long-term goal is the development of predictive indices that will tell us which patients are most likely to show neurobehavioral improvement after neurosurgical anastomosis or endarterectomy for cerebral ischemia. Specifically, a sample of 80 cerebral revascularization candidates is being followed up for 18 months after operation. The hypothesis is that patients with a moderate level of behavioral impairment preoperatively are more likely to show improvement after operation. It is also likely that medical risk factors for cerebrovascular disease, dissemination of atherosclerosis, lateralization of symptoms and neurobehavioral impairment, and the type of neurosurgical intervention will affect postsurgical outcome. Studies of regional cerebral blood flow and nuclear magnetic resonance spectra will enhance this work by elucidating the role of metabolic factors in postoperative behavioral changes. As part of this work, it is necessary to gather detailed, consistently reported information from cerebral angiography. Such data permit quantitative as well as qualitative combination with other measures and aid in analysis of groups of patients as opposed to individual case 0090~'019/85/$3.30
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studies. Despite the great heterogeneity of cerebral revascularization candidates and the consequent risks of overgeneralization, group analyses are necessary if we are to extract reliable conclusions from accumulated experience in evaluating and treating patients with cerebral ischemia. From a neuropsychologist's point of view, correlations with angiographic data are necessary to establish firmly the strength and type of linkages between behavioral data and the structural pathology underlying cerebrovascular occlusive disease. Studies correlating psychological data with regional cerebral blood flow and clinical symptoms provide indispensible insights into hemodynamics and behavior [ 11], but cannot substitute for the structural data gleaned from angiography. This is an obvious distinction but one not always drawn, par-
ticularly in the psychological literature. Moreover, neither regional cerebral blood flow procedures nor angiography provides definitive information on metabolism - - a parameter of brain functioning likely to co-vary most directly with behavior. Psychological and neurological studies of structure-function relationships have drawn differing conclusions about their strength. Peerless et al [13] cite many references that show an association between multiple-vessel occlusions and dementia; they also list others that indicate that multiple-vessel disease is not always correlated with global behavior dysfunction. Kelly et al [9] found that presence of ulceration on angiography was not correlated with neurobehavioral impairment in candidates for carotid endarterectomy. Although mean scores are in the expected direction, Duke et al [5]
Angiogrophic Ratings of Cerebral Revosculorization Candidates Stenoses in Major Vessels Code:
0 or blank
=
0%
I
=
I% to 2 9 . 9 9 %
2
=
3 0 % to 4 9 . 9 9 %
3
=
50% to 99.99%
b,
=
100%
9
=
not enough information to rate, for example, artery not
stenosis
injected or not well-visualized instructions:
/
List codes in the order the arteries are listed:
/
Left common carotid artery, left external carotid artery, left internal carotid artery Right common carotid artery, right external carotid artery, right internal carotid artery Left anterior cerebral artery, left middle cerebral artery
i II.
Right anterior cerebral artery, right middle cerebral artery Left vertebral artery, right vertebral artery, basilar artery Left posterior cerebral artery, right posterior cerebral artery
Intracranial Radiographic Opacification Code:
0 or blank
=
adequate radiographic opocificotion
I
=
focal area of decreased radiographic opacification
2
=
multifocal
or
diffuse
decrease
in
radiographic
opocification in the branches and small vessels 9
=
not enough information to rate
Left cerebral hemisphere (List any focal area of decreased opocification) Right cerebral hemisphere (List any focal area of decreased opacification) Brainstem end cerebellor area (List any focal area of decreased opocification)
Figure 1. Cerebral angiogram rating sheet for cerebral revascularization candidates.
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found no differences between candidates for carotid endarterectomy with large vessel atherosclerosis on angiography versus those patients with only small-vessel disease on angiography. In contrast, in their studies of candidates for carotid endarterectomy, H o r n e and Royle [7] stated that severity of atherosclerosis did relate to severity of psychological impairment; Jacobs et al [8] found that patients with at least 75% reduction in crosssectional lumen of the carotid arteries were more impaired than patients with only 2 5 % stenosis. For these studies, the objective was an angiographic measure that would provide detailed information on stenoses in the major cerebral vessels and reflect the distinctions and cutoffs most reliably and frequently made by neuroradiologists in studying candidates for extracranial-intracranial arterial anastomoses and other revascularization procedures. In examining the utility of this measure, the strategy was to look first at general relationships between atherosclerotic involvement and neuropsychological impairment. T h r e e neuropsychological measures thought to be sensitive to disturbances in higher cortical functioning were included. Measures of severity and dissemination of atherosclerosis and of intracranial opacification were devised to quantify information from cerebral angiography. Statistical analyses using these general radiographic and behavioral mea-
1. Description of.31 Cerebral Revascularization Candidates
Table
Age Mean Standard deviation Education (years) Mean Standard deviation G e n d e r (n) Male Female Race (n) Caucasian Black Subsequent surgery (n) Unilateral carotid endarterectomy Bilateral carotid endarterectomy Unilateral S T A - M C A bypass Bilateral S T A - M C A bypass Carotid endarterectomy and contralateral S T A - M C A bypass Vertebral-carotid transposition N o surgery Longest s y m p t o m prior to assessment (n) N o definite clinical s y m p t o m s Transient ischemic attack Reversible ischemic neurological deficit Stroke STA-MCA, superficial temporal artery-middle cerebral artery.
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Table 2. Summary Stenotic Rating and Related Variables." Descriptive Statistics Summary stenotic rating (n = 31 ) Median Range Medical index (n = 23) Median Range Wechsler Memory Quotient (n = 29) Mean Standard deviation Average impairment rating (n = 26) Mean Standard deviation Digit symbol scaled score (n = 29) Mean Standard deviation
9 2-26 10 4-20 99.7 15.6 1.64 0.69 6.5 2.6
sures suggest this angiographic scale may be useful in clinical studies of cerebral revascularization.
Method
Angiographic Ratings Figure 1 shows the rating system. These ratings were based on four-vessel studies that usually used a femoral injection, unless significant peripheral vascular disease made this site unfeasible. In this case, brachial injection of dye was performed. To rate the major vessels, a stenotic rating system was designed; to tap information on filling within the small intracranial vessels, a radiographic opacification rating system was devised.
60.6 11.5
Summary Stenotic Rating 12.0 3.8 17 14 24 7 10 2 7 1 2 1 8 1 16 5 9
This form is based partly on the index developed by Bloor et al [2]. However, there are two important differences. First, it was decided to avoid imposing a weighting system upon the ratings until sufficient data and experience allowed careful scaling. Secondly, explicit ratings of all the major vessels were deemed desirable for future study of laterality, caudality, and clinical syndromes associated with specific arteries. The current scale is the result of several earlier versions that Table 3. Spearman's p Correlations u,ith the Summary Stenotic Rating Average impairment rating Digit symbol scaled score Wechsler m e m o r y quotient Medical index Age S y m p t o m duration ~p < 0.05. ~'p < 0.001~ 'Not significant.
0.41Y -0.57 h -
0.02'
0.47 ~ 0.32 ~ 11.16'
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included more complicated finer-grained coding systems, which seemed unwieldy, unreliable, and potentially unsuitable for group analysis. Moreover, the more complex the coding system, the more likely some information would be missing for a given subject and complicate quantification o f data. In practice, the rater often writes in additional information o f note, such as evidence of ulceration. The cutoffs listed for the ratings are those ranges commonly used by neuroradiologists. Roughly, the rating o f I corresponds to minimal stenosis;
Figure 2. Patient 1 illustrates severe and widespread stenosis coexistent with marked behavioral impairment. This 57-year-old man suffered a stroke involving the left arm and leg approximately 14 weeks before angiography and neuropsychological testing. A t the time of the ictus, he also noted some dizziness. Testing showed bilateral moderate-to-severe tactile and motor deficits with mild-to-moderate decrements in intellectual functioning. This anteroposterior projection was taken after left common carotid artery injection. It shows 7 0 % - 8 0 % stenosis of the left internal carotid artery.
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the rating of 2 indicates mild-to-moderate narrowing, the rating of 3 is in the range where stenosis is thought to be hemodynamically significant [6,10]; a rating of 4 indicates complete occlusion. T o obtain the summary stenotic rating used in these analyses, the ratings for all 15 vessels were summed up. In cases in which more than one site of stenosis within a vessel was seen, the most severe stenosis was rated.
Intracranial Radiographic Opacification In part, this scale reflects the system for quantification of collateral flow developed by T h o m p s o n et al [18]. Our ratings are more general, however, and inferences as to adequacy and quantity of flow are not made: only radiographic opacification is rated. It was felt that more precise judgments, for example, about opacification of subsystems of circulation, might not be reliable. Again, the three ratings, for each hemisphere and the brainstem, were summed to obtain the index of radiographic opacification.
Figure 3. Patient I. This projection was obtained after right subclavian injection and illustrates severe atherosclerotic disease in the vertebrobasilar system.
Cerebral Angiography and Neuropsychology
Medical Index We composed a rough index of stroke-related medical risk factors based on information presented in Stroke Risk Handbook [17]. We decided against use of the stroke risk profile from the Handbook because this measure was developed for use in populations that had not yet suffered transient ischemic attack or stroke. The presence of the 11 factors was recorded, weighted, and summed. Weights were assigned according to the relative importance given the factor in the Stroke Risk Handbook. Three points were accredited for STT wave abnormality, cardiac block, or left ventricular hypertrophy; cardiac arrhythmia; or history of cardiac or peripheral vascular disease. The two-point indicators were a current cigarette smoking habit; elevated serum cholesterol; historical or laboratory evidence of diabetes; and abnormal hematocrit, hemoglobin, or coagulation studies. Cardiac enlargement, elevated serum uric acid, and elevated serum triglycerides were one-point indicators. From one to five points were assigned for elevated systolic blood pressure, depending on severity.
Neurobehavioral Measures The Wechsler Memory Quotient, the Wechsler Adult Intelligence Scale (WAIS) digit symbol scaled score, and
Figure 4. Patient 1. Obtained following right common carotid injection, this film reveals severe stenosis in the right internal carotid artery with possible ulceration.
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the average impairment rating were examined as general indicators of adaptive functioning. The average impairment rating is an index of general neuropsychological impairment similar to the rating presented by Russell et al [ 16]. The present average impairment rating is the arithmetic mean of ratings derived from scores on eight tests, the tokens test, the WAIS digit symbol subtest, the trail making test--part B, the sensory-perceptual impairment rating, the finger tapping test, the grip strength test, the static steadiness test, and the foot tapping test. Because the impairment rating is based on multiple mea-
Figure 5. Patient 2 shows minimal behaz'ior impairment correlated with ~,ery mild stenosis u,ithin the cerebro1~asculature. The most significant angiographic finding was a left subclavian steal. This 42-year-old woman had a 3 I/2-month history of transient numbness and u'eakness in the right side of the body. a vertiginous sensation, and "u'hite spots" in both visual fields. After left common carotid injection, reflux into the left l,ertebra/ and /eft subclavian arteries u'as noted.
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sures in different behavioral domains, it is perceived to be a reliable, sensitive measure of overall neurobehavioral status. Although the WAIS digit symbol subtest and the Wechsler M e m o r y Scale initially were developed as measures o f more specific areas of functioning, research has suggested strongly that both measures in fact are general indicators of cerebral dysfunction [ 12,15]. In particular, the digit symbol subtest score has been shown to be sensitive to cerebral lesions, regardless of locus.
Subjects O f 39 angiograms rated, in eight patients one or more vessels could not be rated because of poor visualization. Thus, the present sample consists of 31 candidates for cerebral revascularization, who underwent angiography and partial or full neuropsychological testing. Consistent with the selection criteria usually employed for cerebral revascularization, most o f these patients are very mildly to moderately impaired on neuropsychological tests and present with transient ischemic attacks or mild strokes, rather than with severe fixed deficits, as shown in Tables 1 and 2. Figure 6. Patient 2. A further illustration of left subclavian steal, as well as minimal narrowing of the left external carotid and left internal carotid arteries. Left common carotid injection.
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After giving written consent on standard institutional forms for invasive procedures, all patients underwent cerebral angiography as part of a diagnostic work-up for symptoms suggestive of cerebrovascular disease. Subjects signed consent forms for neuropsychological follow-up as part of a research protocol last approved by the institutional human rights committee on February 23, 1984.
Results
Summary Stenotic Rating and Neurobehavioral Measures The average summary stenotic rating was 10.9, with a mode of 7, and a median of 9. T h e r e is some positive Figure7. Patient3. This case exemplifies incongruence between the stenotic ratings and neuropsychological test performance. Eight years before assessment this 74-year-old woman had a stroke involving the right side of her body and her speech. Shortly thereafter, she lost the vision in her right eye and began to experience transient episodes of dizziness and some change in consciousness. Despite bilateral carotid occlusions and severe atherosclerosis in the left subclavian and vertebral arteries, only mild tactile, motor, and cognitive deficits were noted on testing. This aortic arch study shows left common carotid artery occlusion, right internal carotid artery occlusion, and severe atherosclerosis in the left subclavian.
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are diverse in terms of severity and type of symptomatology and behavioral impairment, this lack of variability underlines the fact that radiographic opacification cannot be equated with adequate blood flow, blood volume, or metabolic functioning. Patient Studies
The correlations between neurobehavioral impairment and the summary stenotic rating are modest, and there is substantial variation in the strength of this relationship from patient to patient. T o emphasize this variability, four patients were selected from this sample: Patients 1 and 2 illustrate a high positive relationship between neurobehavioral impairment and severity and dissemination of atherosclerosis; patients 3 and 4 show a negative correlation between angiographic involvement and deficits on neuropsychological tests, that is, in the direction op-
Figure 9. Patient 3. Both anterior cerebral and middle cerebral arteries fill via the posterior communicating arteries after right brachial injection.
Figure 8. Patient 3. Right brachial injection reveals bilateral internal carotid artery occlusion.
skewing on the scores. Because equality of intervals between rating points cannot be assumed, the angiographic ratings were treated as ordinal-level data. Spearman's p correlation coefficients between the summary stenotic rating and the three neurobehavioral measures were significant for two out of three neuropsychological test scores. Significant correlations also were obtained between the summary stenotic rating and the patient's age, and score on a weighted index of medical risk factors. The correlation between the duration of the patient's longest symptomatic episode and the summary stenotic rating was not significant. The correlation coefficients appear in Table 3. Radiographic Opacification
For 29 of 30 patients rated, radiographic opacification was judged to be adequate for both cerebral hemispheres and the brainstem region. Thus, variability was insufficient for statistical analysis. In that these patients
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posite to prediction. Angiographic results are pictured in Figures 2 - 1 1 ; the stenotic ratings and a subset of the neuropsychological data appear in Table 4.
Discussion The results of these analyses suggest that these angiographic ratings relate to several of the dimensions thought to be important in cerebrovascular occlusive disease-Figure 10. Patient 4. Whereas neuropsychological assessment revealed a moderate level of behavioral impairment, the stenotic ratings showed only mild stenosis of the left common carotid and about 4 0 % narrowing of the left internal carotid artery with possible ulceration. Five months before presentation, this 62-year-old, college-educated man experienced sudden onset of dysphasia and paralysis of the right arm and continued to note residual difficulties in speech, memory, and coordination. This picture was taken after left common carotid artery injection.
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neurobehavioral status, age, and medical risk factors in stroke. Moreover, most four-vessel studies appear to yield information sufficient for these ratings: this practical advantage eases the way to more reliable, generalizable group studies, compared with case studies that use no formal angiographic rating system. Further analyses are necessary to determine whether these ratings also reflect laterality of symptoms and lateralization on neuropsychological tests, as well as caudality of symptoms. An earlier study [1] used angiographic reports and site o f surgery to decide whether the carotid or vertebrobasilar arterial system was primarily involved by atherosclerosis. N o differences between the pattern of neuropsychological findings in the anterior and posterior groups were found. Thus, it would not be surprising to find that neurobehavioral data relate globally to cerebral angiographic findings but may not Figure I I. Patient 4. Further illustration of a probable ulcerated placque in the left internal carotid artery and the left carotid bulb as seen on left common carotid injection.
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Table 4. Angiographic and Neuropsychological Data for Four Patients Case 1 Stenotic ratings Left c o m m o n carotid artery Left external carotid artery Left internal carotid artery Right c o m m o n carotid artery Right external carotid artery Right internal carotid artery Left anterior cerebral artery Left middle cerebral artery Right anterior cerebral artery Right middle cerebral artery Left vertebral artery Right vertebral artery Basilar artery Left posterior cerebral artery Right posterior cerebral artery Opacification ratings Left cerebral hemisphere Right cerebral hemisphere Brainstem and cerebellar area Neuropsychological data Average impairment rating T o k e n test score Digit symbol scaled score Trails B seconds Sensory-perceptual exam Grip strength dominant hand (kg) b N o n d o m i n a n t hand Finger taps/second dominant hand N o n d o m i n a n t hand Static steadiness D o m i n a n t hand time ~ D o m i n a n t hand count N o n d o m i n a n t hand time N o n d o m i n a n t hand count Foot taps/second dominant foot N o n d o m i n a n t foot Wechsler M e m o r y Quotient
Case 2
Case 3
Case 4
1
0
4
2
2 3
1 l
4 4
0 2
l 1
0 0
2 ~
0 0
3 0
0 0
4 0
0 0
1
0
0
0
0 0 4 3 3 0 0
0 0 0 0 0 0 0
0 0 3 l 0 0 0
0 0 0 0 0 0 0
0 0 0
0 0 0
0 0 0
0 0 0
2.71 31(1) a 4(3) 186(4) (3) 27(2) 23(2) 1.9(4) 2.8(3) 58.06(2) 33(0) 54.85(2) 50(0) d -93
1.13 36(0) 10(1) 106(2) (0) 30(1) 29(1) 3.9(3) 3.8(3)
1.38 34(1) 5(2) 186(4) (0) 27(1) 26( 1 ) 5.4(0) 4.5(0)
26.94(1) 142(1) 26.60(1) 156(l ) 3.1(1) 2.9(1) 119
22.86(1 ) 136(1) 26.20(1) 130(1) 2.7(1) 2.2(2) 116
2.38 18(3) 6(2) 186(4) (3) 45(1) 44(1) 3.2(3) 3.4(3) 18.03(1) 61(1) 15.27(1) 64(0) 2.7(1) 2.3(2) 78
~The parenthesized scores are impairment ratings. An impairment rating of 0 indicates high normal performance; l suggests normal performance; 2 represents mild impairment; 3, moderate impairment; and 4, severe impairment. briand and foot preference were determined by verbal questioning. 'Time and count are measures of cumulative seconds of contact and number of contacts with the rim of a hole in a metal plate. In the static steadiness test, the subject is asked to keep a stylus inserted in a hole without touching the edge of the hole. '~Not administered because of poor balance.
relate on a point-by-point basis. This hypothesis is consistent with evidence that symptoms do not occur significantly more frequently in patients with stenosis when they are compared with age-matched subjects without stenosis [4]. This speculation also is compatible with reports of steal phenomena in which a stenosis in the vertebrobasilar system may produce symptoms usually associated with the carotid arterial system [19]. In this sample, age, medical risk factors, and neuropsychological impairment all correlated with dissemination and severity of atherosclerosis. Separate analyses revealed that age and medical risk factors, as well as symptom duration, also were correlated with behavioral
impairment. Thus, the relationship between the stenotic rating and neuropsychological impairment cannot be assumed to be independent of these other correlations. As a larger sample is accumulated, multiple regression analyses may be used to ascertain these interconnections. In this sample, variation in radiographic opacification did not relate to variation in neurobehavioral impairment. The absence of a relationship may have been due to the lack of variability in radiographic opacification: Only one angiogram was rated as showing inadequate intracranial opacification. Moreover, as illustrated by the four selected patients, the relationship between the stenotic and the behavioral indices is far from consistent
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across patients. Likely, this variability is not due entirely to random error but rather reflects other variables that systematically moderate the relationship between stenosis and behavioral dysfunction. Several variables deserve consideration as moderators. First, collateral circulation, general cardiovascular condition, and locus of stenosis [4,6] are believed to be important in determining severity of ischemia. Hence, these factors may influence severity of neuropsychological impairment. Secondly, stenosis at some sites may be more likely to produce marked impairment on neuropsychological tests. For example, even though stenosis was very limited in severity and dissemination in patient 4, who was moderately impaired, the principal site of involvement was the internal carotid artery feeding the cerebral hemisphere dominant for speech. Research in regional cerebral blood flow has yielded results and hypotheses that parallel those in the present report. In one study, comparisons between percent hemispheric differences in blood flow and judgments of laterality of neuropsychological findings showed strong agreement [3]. In another study, ratings of regionality of asymmetries in cerebral blood flow did not correspond with the site of stenosis on the angiogram [14]. However, there was a relationship between the overall presence or absence of abnormalities in regional cerebral blood flow and on angiography. Measurements such as regional cerebral blood flow may be more directly related to function, and hence to neuropsychological measures than are the stenotic ratings, which pertain mostly to static or slowly changing obstructions in the cerebrovasculature. The stenotic rating system presented herein seems to provide a useful way of quantifying and comparing neuroradiologic results across groups of cerebral revascularization candidates. Global indicators of neurobehavioral impairment relate to severity and dissemination of atherosclerosis in the cerebrovasculature, even though many of these stenoses probably do not produce clinical symptoms. Additional work is likely to clarify this relationship. In particular, possible intervening variables, such as regional differences in rate and volume of blood flow, metabolic function, and patterns of collateral circulation, require further study. The long-term goal is to learn how severity and dissemination of atherosclerosis moderate neuropsychological changes after cerebral revascularization. We wish to express appreciation to Ms. Gall Bruno for secretarial assistance in obtaining angiographic data, to Ms. Cathleen McDonald for her careful work in testing these patients and in organizing the data, and to Dr. Gregory G. Brown for critical comments and continuing collaboration. Research on candidates for cerebral revascularization is supported by NS17116-01.
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SA, Austin GM, Simmons CR. Angioflow patterns in STA-MCA anastomosis Reichman OH, eds. Microvascular anasischemia. New York: Springer-Verlag,
19. Toole JF. Management of transient ischemic attacks. In: Scheinberg P, ed. Cerebrovascular diseases. New York: Raven Press, 1976:23-30.