Neuro radiology
Neuroradiology (•988) 30:201-210
© Springer-Verlag 1988
Encephalopathic cerebrovascular steal: dynamic CT of arteriovenous malformations J. R. Jinkins Neuroradiology Section, King Faisal Specialist Hospital and Research Center, Riyadh, Saudi Arabia
Summary. Arteriovenous malformations and the clinical symptoms they engender are due in large part to the cerebrovascular steal intimately associated with these lesions. Intravenous dynamic computed tomography was utilized in a series of 10 patients harboring cranial vascular malformations of varying size and location in an effort to further elucidate the pathophysiology and extent of the arteriovenous shunt in pre-hemorrhagic (8 subjects) and posthemorrhagic (2 subjects) clinical situations. Perfusion abnormalities were identified locally as well as distant from the nidus of the lesion, both intra- and extra-axially. The technique of dynamic computed tomography in this study group confirms past observations regarding the steal phenomenon and reveals aberrant perfusion states which were previously unknown.
Key words: Dynamic computed tomography - Cerebrovascular steal - Encephalopathy
The conventional radiologic methods utilized in the diagnosis of arteriovenous malformations (AVM) have been extensively described in the literature. The encephalopathy accompanying these malformations to include headache, seizure, progressive neurologic impairment and sudden generalized clinical deterioration are also well documented [1-7]. The cerebrovascular steal (CVS) largely directly or indirectly responsible for the progression of these manifestations is a difficult phenomenon to investigate, however, research in this area has been accomplished in the past using several different approaches, including direct surgical observations, blood gas analysis techniques, conventional angiography, radionuclide regional cerebral blood flow de-
terminations, single photon emission computed tomography, and stable Xenon enhanced computed tomography [1, 3, 5, 8-11]. The present study was undertaken to evaluate the potential of intravenous dynamic computed tomography (IVDCT) to characterize the aberrant cranio-cerebral perfusion patterns associated with the arteriovenous shunt (AVS) accompanying AVM's. It should be noted that the word "perfusion" can have a variety of meanings. In this paper it does not necessarilly imply capillary perfusion, but the passage of contract medium through whatever vessels are represented in the pixels imaged.
Subjects and methods A total of 10 normal and 10 AVM patients were studied with IVDCT utilizing a GE-9800 computed tomographic (CT) scanner (Table 1). A standard injection sequence was used: 4 cc Renografin-76/sec. injected through a 20 gauge antecubital venous catheter with a power injector for a total of 60 cc. The scan sequence was also standardized: one initial scan followed by an 8 second arm-to-head circulation time delay, 12 scans in rapid sequence without interscan delay, and 8 subsequent scans with a 30 second interscan delay (actual total time per scan equalled approximately 4.5 seconds). This extended the study through 5 minutes. The examination was performed at one level, with a 5 m m section thickness, through the center of the lesion as determined by a prior intravenous contrast static CT examination. Time-density dynamic perfusion curves (DPC) were constructed on each patient for the first 45-60 seconds and also for the entire 5 minute acquisition.
202 Table I. Summary of AVM patients Case No.
Age/Sex
1.
1-M
2.
22-M
3.
22-M
4.
23-M
5.
25-M
6.
36-F
7.
39-M
8.
42-M
9.
50-M
10.
54-M
Signs/Symptoms
enlarging head, delayed development, cardiac failure, papilledema sudden explosive headache, confusional state recurrent nonspecific headache, seizure, R-ptosis, bruit, papilledema recurrent non-specific headache, Rsided weakness, aphasia, homonymous hemianopsia recurrent L-transient hemiplegia, Lsided hemiparesthesia recurrent non-specific headache, bruit, L-quadranopsia sudden headache, depressed sensorium, R-hemiparesis, aphasia recurrent R-migrainous headache, grand real seizures recurrent grand mal seizure, intermittent L-sided weakness, L-homonymous hemianopsia, papilledema psychomotor epilepsy, intermittent L-sided weakness
AVM Location/ Character
Associated Findings
vein of Galen
focal mass effect, HC
L-frontal/focal
Arteriographic Supplying Vessels
Intra-Axial Steal
Extra-Axial Steal
Local
Distant
+
+
?
IPH
R-PCA, L-PCA, R-ACA, L-ACA, R-ECA, L-ECA L-ACA
-
-
-
midline-suprasellar/focal
focal mass effect
R-LSA, L-LSA, R-TPA, L-TPA
+
-
-
L-basal ganglia/focal
focal atrophy
L-MCA
+
-
-
R-parietal sensoft-motor area/focal
calcifications, focal atrophy,
R-ACA, R-MCA
+
-
-
R-occipital/diffuse
focal mass effect
R-PCA, R-MCA, R-ECA
+
+
+
L-parietal/focal
SAH
L-MCA, L-ACA
?
?
+
R-parieto-occipital/diffuse
focal mass effect
R-PCA, R-MCA
+
+
-
R-parieto-occipital/diffuse
diffuse mass effect, calvarial erosion
R-MCA, R-PCA, R-ACA, R-ECA, L-ECA
+
+
+
L-MCA
+
+
-
L-parietal/focal focal atrophy
(R = right, L = left, ACA = anterior cerebral artery, MCA = middle cerebral artery, PCA = posterior cerebral artery, LSA = lenticulostriate arteries, TPA=thalamoperforating arteries, ECA=external carotid artery, S A H = s u b a r a c h n o i d hemorrhage, IPH=intraparenchymal hemorrhage, HC = hydrocephalus, + = yes, - = no, ? = unknown)
Parameters evaluated in this study included the intracranial as well as the extracranial soft tissues. Intracranially, the lobar cortical and white matter regions and the interlobar watershed areas were measured and plotted together from one hemispheric region to the other. Extracranially, the soft tissues of the scalp, including muscular tissue but excluding large-bore vascular structures, were measured where possible in the frontal, parietal and occipital areas. The DPC's were then compared to similar measurements of the corresponding contralateral homologous area. This method is important in that
it provides an internal frame of reference by which to gauge perfusion characteristics. All of the perfusion curves illustrated in this study are plots of relative changes in CT numbers verses time. It should be stressed that the actual CT numbers are of no absolute significance. Rather, the shape, position, and amplitude of the curves acquired from regions of pathology, related to other relatively more normal areas of the same study should lead to observations of significant deviations from this "normal" internal control. Nevertheless, IVDCT control studies on 10 nor-
203
mal patients were included in this series in order to further place these observations in context. The same parameters were examined in this control group. An example of a normal control study centered at the thalamic level demonstrates the perfusion peak difference between ipsilateral cerebral lobes (Fig.la). Noted is an increasing DPC amplitude peak progressing from the frontal, through the occipital, to the parietal area (Fig. 1 a). The regional parietal lobe perfusion peak was normally consistantly above that of the other lobes, although, in practice, the frontal and occipital lobes were occasionally near equal. Comparison with a white matter region, such as the internal capsule, revealed a perfusion curve which was parallel although always below areas of gray matter. Generally, the white matter perfusion peak was approximately one-third to two-thirds that of predominately gray matter areas. Comparisons of the two hemispheres demonstrates that while the ipsilateral lobes manifest differing perfusion peaks, the contralateral homologous areas show perfusion curves which are congruous and nearly equal (Fig. lb). An inherent problem in this type of measurement system is the choice of pixel number, pixel group shape, and pixel location from which to obtain the data for construction of the DPC. Necessarily the decision required individual tailoring for each case and circumstance. No standardization was therefore possible in this regard. Obviously this will introduce varying degress of observer bias. In addition, partial volume averaging effects must be considered as a source of error, particularly in small region of interest measurements. All 10 AVM subjects underwent conventional film-screen angiography (CFSA) or arterial digital subtraction angiography (ADSA) as an integral part of their evaluation. No adverse reactions nor complications were encountered as a result of these procedures. None of the patients underwent surgical resection of the demonstrated AVM, and therefore no post-operative evalutations were possible in this study.
Results
Local intra-axial steal
Depending upon the size of the shunt and its proximity to the dural venous sinuses, the IVDCT demonstrated near simultaneous peak opacification of the cerebral arteries, the nidus of the AVM, and the venous system (case nos.l,3-10). Over large areas
Fig. l a , b. Normal Control. a DPC's centered at thalamic level contrasting relative differences in perfusion curves and peaks for ipsilateral cerebral lobes as compared to the contralateral internal capsule, b DPC's in same subject comparing relative similarities in perfusion curves and peaks for contralateral, homologous cerebral structures (see text for further explanation)
surrounding the nidus of the AVM, obvious hyperperfusion was seen as compared to the contralateral region (case nos. 1, 4-6, 8-10). If, however, measurements were collected from smaller areas, while at the same time selecting out the large-bore arteries from the region of interest, the perfusion was at once seen to be below that of the same point in the opposite hemisphere (Fig.2d; case nos.3-6, 8-10). The local vascularity also illustrated different characteristics based upon whether the cortex or white matter adjacent to the AVM was measured. Acquisitions in regions of white matter adjacent to the AVM revealed moderate hypoperfusion, while the perfusion calculations of the contiguous gray matter
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Fig. 2a-fi Case No.6. a Routine post-contrast examination demonstrating the serpentine vascular structures largely confined to the medial right occipital lobe. b Towne's view of left vertebral ADSA revealing the right posterior cerebral supply to the AVM but without obvious abnormal!ty within the left posterior cerebral distribution, e Right external carotid ADSA showing the right middle meningeal (straight arrows) and right occipital arterial contribution to the right occipital AVM. No such parasitization was seen from subsequent left external carotid injection, d DPC selectively measuring the brain parenchyma between the largebore arterial structures revealing the hypoperfused right parietal lobe (X) as compared to the left (Y) compatible with local intraaxial steal, e DPC comparing the hyperperfused left occipital lobe not obviously angiographically involved with the vascular malformation (5) as compared to the relative normal perfusion of the distant left frontal lobe (6) indicating intra-axial interhemispheric steal. f DPC's with areas of interest centered over posterior parietal scalp not including within the boundary the enlarged, right occipital artery seen in Fig. 2c. The comparison of the DPC's reveals relative hypoperfusion of the right scalp (R) as compared to the same region on the left (L) compatible with distal extra-axial steal from the vascular territory supplied by the parasitized right external carotid artery
205
Fig. 3a-d. Case No. 5. a Initial four frames from dynamic sequences demonstrating the areas of calcification in the cortex on the first frame on the upper left (arrOws), and the subsequent early opacification of multiple large-bore arteries supplying the nidus of the AVM. b DPC illustrating the hyperperfused cortex on the right (D) as compared to the cortex on the left (S) indicative of parallel, non-nutritive high-flow intra-axial steal, e DPC centered over white matter regions indicating the hypoperfusion on the right (R) as compared to the left (L) indicating a local low-flow intra-axial steal, d Coronal section through nidus of superficial cortical lesion demonstrating assodated atrophy due to the cerebral vascular steal as revealed by the enlarged overlying subarachnoid space (arrow)
were commonly markedly elevated (Fig. 3b, c; case nos.4-6, 8-10). Distant intra-axial steal
Small AVM's may exert no radiologically detectable effect upon hemispheric perfusion. However, larger AVM's with larger AVS's begin to steal blood flow
from distant sources. In hemispheres with large lesions, the flow through the watershed region was seen to become elevated (Fig.4b; case nos.1, 6, 8-10). Also, in one case, the frontal lobe far removed from the occipital nidus adjacent lobe itself was hyperperfused indicating transterritorial steal (Fig. 5; case no. 8). In no case was a direct correlation to this seen at angiography. Distant lobar
Fig. 4a, b. Case No.9. a Frame from dynamic sequence at approximately 20 seconds illustrating the diffuse bihemispheric collection of serpiginous vascular structures being most prominent in the right occipital region. The enlarged occipital scalp arteries which contribute to the AVM are also identified (arrows). b DPC's of fronto-parietal junctions demonstrating the high-flow watershed steal in the right hemisphere (W) as compared to the left (J) Fig. 5. Case No. 8. DPC's of frontal regions demonstrating moderate hyperperfusion of the right frontal lobe (5) as compared with the left (6) indicating a minor high-flow intra-axial transterritorial steal by the right parieto-occipital AVM Fig. 6a, b. Case No.7. a DPC's centered over parieto-occipital watersheds demonstrating the hypoperfusion on the left (7) as compared to the right (8) one week following subarachnoid hemorrhage emanating from the left parietal AVM. b DPC's acquired over the extracranial soft tissues illustrating the hypoperfused left temporalis muscle (L) as compared to the right (R). No evidence of left external carotid supply to the AVM could be identified at angiography which indicates a proximal carotid bifurcation extraaxial steal
207
hyperfusion was not only seen ipsilaterally, but a single subject revealed similar involvement of the opposite hemisphere (Fig. 2 e; case no. 6). No case of distant ipsilateral or contralateral hypoperfusion was observed in the present series in any of the patients with uncomplicated AVM's (not having acute/ subacute hemorrhage).
Extra-axial steal Extra-axial steal was indirectly observed on CT in two cases in the form of enlarged superficial temporal or occipital arteries (Fig.4a; case nos.6, 9). Correlations were seen angiographically in the enlargement of the scalp arteries which fed the AVM by passing trans-osseously and trans-durally (Fig.2c). Obviously, meningeal vessels as demonstrated, on arteriogram also contribute to the steal via trans-dural anastomoses, however the discrimination of prominent meningeal vessels from enlarged pial vessels on the surface of the cerebrum is not possible on IVDCT. The net result of this external carotid artery steal is a consonant reduction of the relative perfusion measurements of the primary tissues (scalp, calvarium, meninges) (Fig.2f; case nos. 6, 9). One subject showed an extra-axial steal on DPC calculations which was not evident angiographically in the form of parisitized extra-axial vasculature. Lesions of moderate size, but without evidence of direct external carotid supply on angiography, may still therefore demonstrate depressed perfusion of the extra-axial structures (Fig. 6b; case no.7).
Cranial hypertension Three cases in the study group presented with papilledema, indicating cranial hypertension, as part of the clinical picture (case nos. 1, 3, 9). Only one of these three also manifested associated hydrocephalus (case no. 1). IVDCT was not found to be sufficently sensitive to determine the presence or absence of perfusion abnormalities connected with this pathologic state.
Hemorrhage The one subject studied (case no. 2) who revealed a sub-acute intraparenchymal hemorrhage (10 days), demonstrated isoperfusion of the surrounding cerebral tissue, and therefore no significant evidence of steal phenomenon on DPC. The post-hemorrhagic nidus, however, was confined to a very small tangle of vessels draining into a solitary cortical vein. It was not determined whether its small size was due
to a primary appearance or to a partial hemorrhagic obliteration. A single patient, (case no.7), presented with a sub-acute subarachnoid hemorrhage (one week). The examination of the left temporo-parietal AVM illustrated depression of the perfusion pattern in the watershed areas between the occipital and frontal lobes as compared to the opposite hemispheres which was a reversal of the usual pattern associated with uncomplicated AVS (Fig.6a). The IVDCT coincided with the patient's depressed sensorium, progressive right hemiparesis, and aphasia and correlated with severe vascular spasm seen on an arteriography immediately following the CT study.
Discussion
The problems associated with the revelation and understanding of the phenomenon of CVS are based upon sound anatomical and physiological principles. As the AVM does not engender a separate new circulation, the complex collateral available to the cerebrum must explain the local and distant perfusion observations both intra- and extraaxially [12]. Steal parisitization is possible from any arterial radicle within or removed from the primarily involved vascular territory to include vessels supplying the cerebrum, meninges, calvarium or extracranial soft tissues. Local intra-axial steal was manifested in the present study by both hyper- and hypoperfused regions within the lobes of the cerebrum intimately involved with the vascular malformation. Hyperperfused areas indicate the presence of an AVS but reveal nothing of the associated CVS. The physiological steal of blood occurs at the capillary/cellular level, and therefore only gross observations of regional perfusion abnormalities were possible using the IVDCT method. This hyperperfusion represents non-nutrient blood coursing through the volume of tissue en-route to the AVM, but quite possibly not adequately supplying the cerebral substance it passes through. Such elevated perfusion was noted in measurements selectively including predominately cortex. This observation is due to the fact that the vessels feeding an AVM course for the most part over and through the gray matter. The explanation for this would seem to be that the vessels of the gray matter are profusely anastamotic and therefore liable to parasitization from adjacent vessels which are more directly involved with the nidus of the AVM. Measurements of the adjacent white matter areas, on the other hand, demonstrated a depression
208
of the DPC's. This is understood by perceiving the nature of the vascular supply to white matter which is represented largely by non-anastamotic, long endvessels and therefore subject to hypoperfusion when involved in a steal state [13]. It becomes apparent that the distant intra-axial steal of blood from one vascular territory to another cannot be possible without direct arterial-arterial communications. This type of "series" connection is found in the watershed areas where prominent interterritorial anastomoses are known to occur. However, an anatomic pathway for the stolen blood must be enlisted once the blood crosses into the adopted territory. Possibly collaterals through the richly anastomotic, highly vascularized gray matter in parallel to the major vessels may contribute the routes of this steal [14-16]. Whether this supposed "parallel cortical collateral steal" contributes to the flow through the AVS, and/or is collateral to replace blood being stolen from the adjacent territories, is not dear. In certain cases, to provide re-routing of blood, frank vascular flow reversal may occur in major arteries, although this was not observed in the present series [3]. It is well known that AVM's are capable of parisitization of blood supply from extra-axial sources [3, 5, 12, 15, 17]. The enlarged external carotid arteries supplying an intra-axial malformation are demonstrating extra-axial blood flow largely in transit to the AVM, and therefore non-nutritive. Decreased perfusion of the regional extracranial soft tissues support this contention [4]. Even without evidence of macroscopic steal from the external carotid system on conventional angiography, perfusion of the extra-axial tissues may be depressed. This is likely to be due to a proximal sump-steal at the level of the carotid bifurcation, with blood simply selectively flowing out of the internal carotid artery because of the decreased peripheral cerebrovascular resistance secondary to the AVS. In fact, the recurrent headaches associated with AVM's may be related to this steal phenomenon. These headaches are seen to be either non-specific or migrainous in character. The former could be due to ischemia of structures served by the external carotid artery which is involved in the steal process. Anoxia of pain sensitive areas in the dura, calvarium or scalp may be responsible for this clinical symptomatology. Migraine headaches are even less clearly defined in their nature and etiology. Nevertheless, their supposed vascular basis would find simple correlation in the vascular components of the AVM. Aside from the sudden, explosive headache accompanying catastrophic hemorrhage, small, otherwise clinically silent hemorrhages may
also account for some of the potential of AVM to cause cephalgia. Developmentally in the pathogenesis of the AVM's, a primary defect in embryogenesis of the capillary bed occurs which results in a direct AVS [2, 6, 12]. With progressive maturation of the vascular system, the "sump effect" and elevated arterial blood velocity causes a decreased perfusion of regional terminal arterioles secondary to a reduction in available perfusion pressure: the blood follows the path of least resistance through the fistula [12]. In response to this, effective autoregulation elevates the perfusion of these peripheral terminal arterioles, but only to a finite level [18]. With progressive enlargement of the AVM, the AVS presumably may concommitantly increase in size and therefore also increase the flow through the shunt. Growing in parallel to this enlargement is the parisitized collateral intra- and extra-axial steal. At a certain point, the reduced terminal capillary/arteriolar perfusion pressure can no longer perfuse the peripheral neural vascular bed in the face of cerebral venous hypertension also engendered by the AVS [6]. The arteriole and venule intravascular pressures are in balance as the perfusion pressure falls below the threshold for autoregulatory compensation. Even prior to this, cerebrovascular autoregulation may have failed, effecting a passive circulation, thereby complicating an already labile situation. Thus, the critical steal threshold is reached when, theoretically, circulatory arrest occurs. At this stage hypoxia, hypercarbia, and generalized metabolic neural toxicity take place [3, 8, 23, 24]. Besides the atrophy noted on CT and at autopsy, clinical manifestations of this pathologic progression include seizure and focal neurologic dysfunction to include paralysis and specific neurologic deficits. These noxious changes are further aggravated by the continuous atrophic potential of locally elevated tissue pressure and increased pulsations accompanying the AVM. In fact, these effects upon the supporting neural tissues may conceivably compound the process. Atrophy of the surrounding brain is accompanied by an increasingly negative adjacent tissue pressure which could potentially lead to secondary further enlargement of the nidus of the AVM. Linked with the reduced metabolic blood flow requirement of the atrophic change, the involved brain submits in an escalating fashion resulting in an overall phenomenon of encephalopathic vascular steal. The combination of progressive primary and collateral vascular supply enlargement as well as further dilation of the arterialized venous component eventually leads to a shunt flow level which ex-
209
cedes its capacity. Presumably it is at this "critical flow threshold" at which hemorrhage occurs. Many factors are active in the phenomenon of hemorrhage in AVM. From one subject to another, it is not the size of the nidus nor the size of the AVS which is of primary importance. This critical flow threshold can occur in any lesion of any size [2]. Each AVM therefore has its own unique hemorrhagic tendency closely related to an intrinsic vasculopathy [25]. The natural history of AVM's indicates that the hemorrhage which accompanies these lesions may be intracerebral, extracerebral, or a combination. The acute symptomatology, other than the previously discussed headaches, will relate to the compartment in which the bleeding occurs and to the size of the bleed. Assuming herniation has not occured, isolated parenchymal hemorrhage results in clinical manifestations largely due to local mass effects and adjacent tissue injury. In addition, hemorrhage induces compressive effects upon the AVM as well as the surrounding supportive cerebral parenchyma, which in combination with partial hemorrhagic obliteration of the nidus, may lead to a reduction in the AVS and the accompanying CVS. Thus the DPC calculations in such cases may indicate iso- or even hypoperfusion. With extravasated subarachnoid blood, the implications are somewhat different, as local and distant spasm causes differing degrees of depressed cerebral perfusion and attendant ischemia. As a further complication, these effects of parenchymal and subarachnoid hemorrhage occur in the face of a vascular system which is presumably already much altered by such variables as long-term elevations in blood flow and autoregulatory capability, frank tissue damage from chronic ischemic and toxic metabolic changes, and past bleeds. Thus, these superimposed acute hemorrhagic incidents may possibly be all the more profound in their final clinicopathologic expression. As a final consideration, increased intracranial pressure must be implicated in certain cases in the generation of the general encephalopathic picture. This abnormal cranial pressure gradient can be produced by at least three possible mechanisms: 1) simple volume/mass effect [26]; 2) cerebrospinal fluid pathway obstruction with attendant hydrocephalus; and 3) chronic cerebral venous hypertension with associated increased cerebral blood volume accompanying the AVS [6]. These factors potentially may operate singly or in combination to produce neurologic deterioration. Regardless of these speculations, the events leading to neural degeneration are the key to the
Table 2. Factors in the encephalopathic syndrome associated with AVM. Developmental capillary bed malformation Mechanical neural displacement CSF pathway obstruction Pulsatile/mass pressure effects Local intra-axial vascular steal Distant intra-axial vascular steal Extra-axial vascular steal Peripheral autoregulation arrest/insufficiency Chronic cerebral venous hypertension Spontaneous malformation thrombosis Intrinsic hemorrhagic vasculopathy Hemorrhagic sequellae
understanding of progressive neurologic dysfunction allied with CVS. Tissue hypoperfusion due to steal is present in all regions manifesting aberrant flow of any degree. By measurements, some areas are "high-flow" and some "low-flow", but all reflect the underlying primary steal. Only a certain amount of cerebrovascular compensation is possible by means of autoregulation, and thereafter the result is cellular ischemia, toxicity and irreversible neuronal injury. This pathologic process is further potentiated by the effects of intracranial hemorrhage closely linked with AVM's. Many steal phenomena are below the threshold of obvious radiologic detection, however, the technique of IVDCT allows a great deal of insight into occult perfusion abnormalities intimately and distantly associated with AVS's which are partially responsible for the encephalopathy accompanying this developmental vascular anomaly (Table 2). Acknowledgement: I wish to thank C.K.Jinkins for the manuscript research and preparation.
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