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Multiple Intracerebral Arteriovenous Malformations: Report of Three Cases and Review of the Literature Michael Salcman, M.D., Herman
Scholtz, M.D., and Yuji Numaguchi,
M.D.
Divisions of Neurological Surgery and Neuroradiology, University of Maryland Hospital, Baltimore, Maryland
Salcman M, Scholtz H, Numaguchi Y. Multiple intracranial arteriovenous malformations: report of three cases and review of the literature. Surg Neurol 1992;38:121-8.
Multiple intracerebral arteriovenous malformations are thought to be exceedingly rare lesions and have usually been reported as single cases. During the past 2 years, we have treated three patients with multiple cerebral arteriovenous malformations, representing 3.2% of a consecutive series of 95 arteriovenous malformation patients seen since 1976. Details on 17 other cases are available in the literature and are summarized here. The incidence of multiple arteriovenous malformations in major series ranges from 0.3% to 3.2%; the average incidence is 1.9% based on 21 cases encountered in a total population of 1102 arteriovenous malformation patients. Patients with multiple arteriovenous malformations often have other vascular anomalies of the brain or soft tissues, but the clinical mode of presentation, age, sex, and anatomical distribution of the lesions are the same as those of patients with single arteriovenous malformations. The use of four-vessel angiography in combination with magnetic resonance imaging may result in a higher detection rate for such cases. KEY WORDS: Arteriovenous malformations; Arteriography; Vascular anomalies
Among the vascular anomalies found in the central nervous system, multiple intracerebral arteriovenous malformations (AVMs) are thought to be exceedingly rare lesions. Although the coincidence of AVM and arterial aneurysm is frequently discussed, multiplicity of AVMs is usually not even commented upon in the reports of most large clinical series or pathological studies. The relative incidence of multiple cavernous malformations and telangiectasias has been estimated to be 25%, but no similar estimate has been made for true AVMs of either the cerebral hemispheres or the posterior fossa [19]. Multiple cerebral AVMs have usually been reported as isolated cases, often in the context of a more Address reprint requests to."Michael Salcman, M.D., 7801 York Road, Suite 102, Towson, MD 21204. Received November 11, 1991; accepted February 10, 1992.
© I992 by Elsevier Science Publishing Co., Inc.
widespread dysembryonic condition [8,20]. We have recently had the opportunity to analyze three cases, treated at the University of Maryland during the last few years. N o n e of these patients suffered from vascular or other anomalies in tissues other than the cerebral hemispheres. In addition to reporting these cases, we have attempted to determine the incidence of cerebral AVM multiplicity based on our own series and the available information in the literature.
Case Reports
Case 1 M.R. is a 42-year-old, right-handed, white female who presented to our service with an intraventricular hemorrhage and depressed sensorium in N o v e m b e r 1988 (Figure 1). Magnetic resonance imaging (MRI) revealed the presence of two very large AVMs, one occupying the posterior two thirds of the left temporal lobe and the second located in the right parietal lobe (Figure 2). Arteriography demonstrated multiple anterior temporal artery feeders from the left middle cerebral artery (MCA) entering the first lesion mesially, as well as contributing vessels from the left posterior cerebral artery; drainage was into the left sylvian system and the left petrosal sinus (Figure 3 A - C ) . The right parietal AVM was fed by posterior branches of the right MCA and drained into the superior sagittal sinus (Figure 3 D). Because of the proximity of the left temporal lesion to the temporal horn and the atrium of the lateral ventricle, it was assumed that this lesion was responsible for the intraventricular hemorrhage. A large left temporal-occipital craniotomy was carried out, with a complete excision of the lesion, the posterior two thirds of the temporal lobe, and the temporal-occipital junction down to the tentorial incisura. The superior gyrus of the temporal lobe was microsurgically spared; a preoperative Wada test had indicated mixed cerebral dominance for language in this patient. Postoperatively, the patient quickly recovered from transient dysphasia. Three months later, a right parietal craniotomy with gross total resection of the second AVM was carried out. A cerebral angiogram postop0090-3019/92/$5,00
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Figure 1. Case l. C T scan demonstrates an intraventricular hemorrhage into the lateral ventricle. eratively demonstrated no evidence of residual AVM. The patient's recovery was uneventful.
Case 2
S.F. is a 49-year-old white female with multiple medical problems who first presented with an intracerebral hemorrhage at the age of 47 years. She underwent a craniotomy for clot removal at another institution and remained well until D e c e m b e r 1988 when a second hemorrhage and profound hemiparesis resulted in her admission to the University of Maryland (Figure 4) for an emergency craniotomy and evacuation of a right subdural and intracranial hematoma. Although the patient was alcoholic and hypertensive, the triangular shape of the clot with its apex pointing to the ventricle and its base subjacent to the old craniotomy flap made us suspicious of an underlying AVM. An arteriogram (Figure 5) revealed the presence of two medium-to-large right-hemisphere AVMs, one in the frontal lobe and one in the temporal lobe. Each appeared amenable to resection, but the patient suffered multiple episodes of gastrointestinal hemorrhage and could not be brought to surgery.
Case 3
is a 28-year-old white female who presented with severe headache, neck stiffness, and seizures resulting L.L.
Figure 2. Case 1. Patient with two large AVMs. (A) T2-weighted axial M R I scan shows an A V M in the left temporal lobe. (B) T2-weighted axial MRI scan of the A V M in the posterior right parietal lobe.
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d
A Figure 3. Case I. (A) Left internal carotid angiogram, lateral projection. The temporal lobe A V M is fed by the left MCA. (B) The left vertebral injection demonstrates contributing vessels from the left posterior cerebral after), in the anteroposterior view. (C) Left internal carotid angiogram. /ateral projection. The venous drainage of the temporal lobe A V M is into the left ,lyh,ian system and left petrosal sinus. (D) Right internal carotid angiogram, lateral projection. The parietal lobe A V M is fed by posterior brancheJ of the M C A and drains into the superior sagittal sinus.
from a left temporal lobe hemorrhage in July 1987. H e r preoperative MRI (Figure 6) and arteriogram (Figure 7) indicated two relatively small AVMs in the left temporal lobe. A left temporal craniotomy was carried out, and a 1 × 1-cm capillary-like lesion was dissected out completely from the surrounding brain tissue. However, the
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Figure 4. Case 2. Axial CT demonstrates a right parietal subdural hematoma, intracranial and intraventricular blood, and deviation of the midline to the left.
Figure 5. Case 2. Right internal carotid angiogram, lateral projection. There are two AVMs, one in the frontal lobefed by the MCA and a second in the temporal lobefed by the posterior cerebralartery and posterior branches of the MCA.
Figure 6. Case 3. T l-weighted MR1 scan shows increased signal intensity in the left temporal lobe, suggesting hemorrhage mesial to the inner A VM.
large draining vessel seen on the angiogram was not identified. A postoperative arteriogram revealed the second A V M just medial to the other lesion (Figure 8), so a decision was made to explore the temporal lobe more posteriorly. T h e second A V M was found connected to the first by an interposed vein and was also completely resected. N o residual A V M was seen on the final postoperative angiogram.
Discussion T h e r e have been at least 20 cases of multiple cerebral AVMs reported in the literature; only two reports have described m o r e than a single patient in detail (Table 1). The earliest case appears to be a 35-year-old male with a basal ganglia lesion fed by the right M C A and anterior cerebral artery that bled on two occasions, who also had a smaller A V M in the caudate nucleus [10]. This case was reported in 1958 by H o o k and Johanson and is somewhat problematic due to the p o o r quality of the early angiograms and the close proximity of the two
Multiple Intracerebral AVM
lesions. Another early case was a 9-year-old boy, and it appears to be definitive because the right frontal AVM bled and the left occipital lesion was a presumed cause of headache [5]. This 1963 report is especially interesting because it also provided a review of other vascular anomalies encountered in a series of 97 patients with AVMs. T h e first report of the coexistence of a supratentorial A V M with a posterior fossa A V M is probably that of Tamaki et al in 1971 [20]. Current interest in the subject dates back to the series of four patients reported by Schlachter and colleagues in 1980 [16]. As several subsequent authors have pointed out, two or three of the four cases are questionable. Their second case had mirror lesions on the mesial surface of each parieto-occipital lobe, and it is possible that they were not really separate. The analysis of the third case was based on two lesions seen on computed tomographic (CT) scan in the left frontal and midbrain regions, without either published arteriograms or histology; the right frontal occult A V M was established histologically after evacuation of a C T - d o c u m e n t e d clot. It is possible that the other lesions in this case were cavernous malformations. Their fourth patient had a left tentorial A V M and a right parieto-occipital lesion that was described as cryptic, without even CT documentation. Nevertheless, the cases are included in Table 1 because of their historical importance. Voigt et al acknowledged that some communication might have existed between the two AVMs in their patient, since they shared a c o m m o n draining vein, and
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Figure 7. Case 3. (A) Left vertebral angiogram, anteroposterior view. Two small A VMs fed by the left posterior cerebral arter5 are visible medially and laterally. (B) Venous drainage of the lesion is to the petrosal sinus. No hematoma was visible by C T or at surger3, in the ttisue between these two lesions. Figure 8. Case 3. Postoperative left vertebral angiogram, Townes projection. Shows a small left posterior cerebral artery A V M medial to the other lesion, with venous drainage into the superior sagittal sinus.
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Table 1. Reported Cases of Multiple Intracranml Arteriovenous Malformations Source (year)
Case no.
Age/sec
Locations Right basal ganglia Caudate nucleus Right frontal Left occipital Right basal ganglia Posterior fossa Right centroparietal Right mesial parietal both sides of falx Right parasagittal Right parietotemporal Right parietooccipital Left parietooccipital Right frontal Left frontal Midbrain Left tentorium Right parietooccipital Right frontal Left parietal Right posttemporal Right parietal Left parietal Left parietal Right parietal Left superior frontal gyrus Right sylvian fissure Left medial operculium Right frontal Right temporal Left parietooccipital Right frontal Right temporal Right temporoparietal Left temporoparietal Left insular Left basal ganglia Right occipital Dorsal pons Left temporal Right parietal Right frontal Right temporal Left temporal Left temporal
Hook & Johanson [10] (1958)
1
35/M
Frugoni et al [5] (1963)
2
9/M
Tamaki et al [20] (1971)
3
19/F
Voigt et al [21] (1973)
4
28/F
Schlachter et al [16] (1980)
5
27/M
Schlachter et al [16] (1980)
6
29/M
Schlachter et al [16] (1980)
7
45/M
Schlachter et al [16] (1980)
8
33/M
Hanieh et al [8] (1981)
9
31/F
Shigemori et al [17] (1982)
10
47/F
Stone e~:al [19] (1983)
11
24/M
Zellem & Buchheit [24] (1985)
12
36/F
Reddy et al [13] (1987)
13
16/F
Romero et al [15] (1988)
14
36/M
Fong & Chan [4] (1988)
15
9/F
Nakayama et al [11] (1989)
16
40/M
Nakayama et al [11] (1989)
17
37/F
Present report (1992)
18
42/F
Present report (1992)
19
49/F
Present report (1992)
20
28/F
Arteries
Presentation
MCA & ACA Choroidal pericallosal ? ? Lenticulostriates Vertebral artery MCA )
SAH twice
MCA MCA ICA ICA ~ ? ? Meningohypophyseal ) ~ ? ~
Bled
Angular/posttemporal MCA Angular MCA Callosomarginal & MCA Parietal MCA ? MCA & ACA MCA MCA MCA MCA MCA MCA MCA MCA PCA Pontine MCA/PCA MCA MCA MCA/PCA PCA PCA
Clot, headache Staggering gait, blindness, retardation Seizures
Bled Headache, staggering gait, dysphasia Bled Seizures Clot
Bled Tinnitus for 13 years, headache, transient dysphasia Seizure
? Bled Bled Bled Bled Bled Bled
Abbreviations: M, male; MCA, middle cerebral artery; ACA, anterior cerebral artery; SAH, subarachnoid hemorrhage; F, female; ICA, internal carotid artery; PCA, posterior cerebral artery.
one was right centroparietal in location, while the other was right mesial parietal on both sides of the falx [21]. The case reported by Hanieh et al had histologic confirmation but no arteriography [8]. In 1985, Zellem and Buchheit reported the first patient with three AVMs; many of her family members had suffered cerebrovascular accidents and she had a cousin with an intracranial AVM [24]. Yasargil has also encountered a patient with three separate cerebral AVMs and gives brief accounts o f 14 other cases in his recent textbook [23].
In general, patients with multiple AVMs are similar to those with single malformations. The reported patients range in age from 9 to 49 years, with a mean of 30.6 years. There have been nine males and 11 females reported, but a disproportionate number of the questionable cases have been male. The MCA has been the most frequently involved feeding vessel, its anterior and posterior branches often supplying separate lesions in the same hemisphere. The second AVM has been located in the opposite hemisphere or in the posterior fossa on 14
Multiple Intracerebral AVM
occasions; these cases are generally indisputable. The great majority of patients presented because of an intraparenchymal or subarachnoid hemorrhage; a few patients were investigated because of headache, seizures, or retardation. Several of the patients have unusual family histories or other associated anomalies. The patient reported by Reddy et al had three separate AVMs; her brother sought medical attention for headaches and was noted to have Rendu-Osler-Weber syndrome [13]. The positive family history in Zellem and Buchheit's case has already been noted [24]. Some of the patients have had vascular anomalies of the face, neck, and eye [20] or in the soft tissues of the hand [8]. A patient with two AVMs also had four aneurysms and ectasia o f both anterior cerebral arteries [21]. A basilar artery aneurysm has been reported in association with three hemispheric AVMs [ 17]. We report one patient with three connecting AVMs on the same side. Patients with multiple intracranial AVMs, therefore, are likely to demonstrate within themselves or through family members a general tendency toward vascular maldevelopment. This is also demonstrated by the unusual case of a child with multiple AVMs in both the brain and the spinal cord [9]. The incidence o f multiple cerebral AVMs is difficult to determine from the literature, since relatively few o f the authors who have reported individual cases have also indicated the size of their personal series of treated patients. Conversely, a number of authors who have reported an AVM series have remarked on the occurrence o f an unusual case of multiplicity without further documentation. The first clinicians to do so were probably Patterson and McKissock in 1956, who mention one patient in a series of 110 cases with a left frontal AVM and "possibly" a lesion in the other hemisphere [12]. Drake et al reported that one o f their 66 patients with posterior fossa AVMs also had a second lesion supratentorially [3]. In a series of 500 AVM patients, Yasargil reported that 15 were multiple [23], and in a review of the Phoenix experience, there was one case in 300 [14]. The child reported by Fong and Chan was one of a series of 39 cases observed in the pediatric age group, while the child reported by Frugoni et al is from a series of 97 AVMs in both children and adults [4,5]. We have personally treated three cases in a consecutive series of 95 surgical patients, for an incidence of 3.2%; this estimate is probably on the high side (Table 2), although the likelihood of discovering such cases may be increasing in the era of MRI scanning. Each of our surgical cases was treated in the last few years. Excluding the pediatric and posterior fossa series, 21 cases have been encountered in a total o f 1105 AVM patients, for a reported mean incidence of 1.9%.
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Table 2. Incidence of Multiple Intracranial Arteriovenous
Malformations in Reported Series Source (year)
No. of cases
No. (c~) multiple
Patterson & McKissock [12] I1956) Frugoni et al [5] (1963) Yasargil [23] (1988) Rigamonti et al [14] (1987) Present report t1992) Total
1 I0
1 (0.9~ /
97
1 (1.0c)~)
500 300
15 (3.0g{) 1 (0.39¢)
95 1102
3 (3.29~) 21 (1.9,~/;)
The question naturally arises as to whether each of the AVMs in a multiply afflicted patient should be resected or otherwise subjected to treatment. Recent publications support the concept that AVMs represent a 1% to 3% annual risk of hemorrhage [1,2,6,7,22], whether previously ruptured or not. In a patient with more than one lesion, these probabilities are additive. The child reported by Fong and Chan first bled from the rightsided lesion at age 9 years and then bled again from the left-sided lesion at age 16 years [4]. Several of the other cases in Table 1 bled on more than one occasion, including our third patient. A decision to operate, therefore, should be based on (1) the patient's age, since this determines the remaining lifetime exposure to risk; (2) the patient's condition, as this affects the quality of life to be expected after treatment; and (3) the likely risk of resection as estimated by the grading scheme of Spetzler and Martin [18]. In every instance, the AVM that has most recently hemorrhaged or the one that is most symptomatic should be resected first if at all possible. Since the quality of life is often determined by the response to the first operation, all other things being equal, the largest and most difficult lesion should be attacked at the first procedure. In some cases, residual AVM as well as smaller multiple lesions might be treated with stereotactic radiosurgery. Since the morbidity and mortality of surgery (as well as the risk of hemorrhage and death) are also additive in multiple AVM patients, it is suggested that these lesions be treated in cerebrovascular centers.
References 1. Brown RD Jr, Wiebers DO, Forbes G, O'Fallon WM, Piepgras DG, Marsh WR, Maciunas RJ. The natural history of unruptured intracranial arteriovenous malformations. J Neurosurg 1988;68:352-7. 2. Crawford PM, West CR, Chadwick DW, Shaw MDM. Arteriovenous malformations of the brain: natural history in unoperated patients. J Neurol Neurosurg Psychiatry 1986;49:1-10. 3. Drake CG, Friedman AR, Peerless SJ. Posterior fossa arteriovenous malformations. J Neurosurg 1986;64:1-10.
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4. Fong D, Chan S-T. Arteriovenous malformation in children. Childs Nerv Syst 1988;4:199-203. 5. Frugoni P, Mingrino S, Giannusso V. Association of cerebral vascular malformations: coexistence of arteriovenous angioma and persistent carotid-basilar anastomosis (primitive trigeminal artery). Neurochirurgia (Stuttg) 1963;6:74-81. 6. Fults D, Kelly DLJr. Natural history of arteriovenous malformations of the brain: a clinical study. Neurosurgery 1984; 15:658-62. 7. GrafCJ, Perret GE, TornerJC. Bleeding from cerebral arteriovenous malformations as part of their natural history. J Neurosurg 1983;58:331-7. 8. Hanieh A, Blumberg PC, Carney PG. Multiple cerebral arteriovenous malformations associated with soft tissue vascular malformations. Case report. J Neurosurg 1981;54:670-2. 9. Hoffman JH, Mohr G, Kusunoki T. Multiple arteriovenous malformations of spinal cord and brain in a child. Case report. Childs Brain 1976;2:317-24. 10. Hook O, Johanson C. Intracranial arteriovenous aneurysm: a follow-up study with particular attention to their growth. Arch Neurol Psychiatry 1958;80:39-54. 11. Nakayama Y, Tanaka A, Yoshinaga S, Tomonaga M, Maehara F, Ohkawa M. Multiple intracerebral arteriovenous malformations: report of two cases. Neurosurgery 1989;25:281-6. 12. Patterson JH, McKissock W. A clinical survey of intracranial angiomas with special reference to their mode of progression and surgical treatment: a report of 110 cases. Brain 1956;79:233-66. 13. Reddy K, West M, McClarty B. Multiple intracerebral arteriovenous malformations. A case report and literature review. Surg Neurol 1987;27:495-9.
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14. Rigamonti D, Spetzler RF, Johnson PC, Drayer BP, Carter LP, Uede T. Cerebral vascular malformations. BNI Quarterly 1987;3(3):18-28. 15. Romero FJ, Ibarra B, Rovira M. Double intracranial arteriovenous malformation in the same patient. Neuroradiology 1988;30: 87-90. 16. Schlachter LB, Fleischer AS, Faria MA, Tindall GT. Multifocal intracranial arteriovenous malformations. Neurosurgery 1980; 7:440-4. 17. Shigemori H, Hara K, Shirahama M. Multiple vascular malformations of the brain associated with a cerebral aneurysm. Neurol Med Chir (Tokyo) 1982;22:383-8. 18. Spetzler RF, Martin NA. A proposed grading system ofarteriovenous malformations. J Neurosurg 1986;65:476-83. 19. Stone JL, Crowell RM, Lisner BM, Naseem M, Oldershaw JB. Bilateral parietal arteriovenous malformations: report of a case. Neurosurgery 1983;13:587-92. 20. Tamaki N, Fujita K, Yamashita H. Multiple arteriovenous malformations involving the scalp, dura, retina, cerebrum, and posterior fossa. Case report. J Neurosurg 1971;34:95-8. 21. Voigt K, Beck U, Reinshagen G. A complex cerebral vascular malformation studied by angiography: multiple aneurysms, angiomas, and arterial ectasia. Neuroradiology 1973;5:117-23. 22. Wilkins RH. Natural history of intracranial vascular malformations: a review. Neurosurgery 1985;16:421-30. 23. Yasargil MG. Microneurosurgery, vol 1. Stuttgart: Thiem Medical 1988:165, 24. Zellem RT, Buchheit WA. Multiple intracranial arteriovenous malformations. Case report. Neurosurgery 1985;17:88-93.
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Multiple Intracerebral Arteriovenous Malformations: Report of Three Cases and Review of the Literature Michael Salcman, M.D., Herman
Scholtz, M.D., and Yuji Numaguchi,
M.D.
Divisions of Neurological Surgery and Neuroradiology, University of Maryland Hospital, Baltimore, Maryland
Salcman M, Scholtz H, Numaguchi Y. Multiple intracranial arteriovenous malformations: report of three cases and review of the literature. Surg Neurol 1992;38:121-8.
Multiple intracerebral arteriovenous malformations are thought to be exceedingly rare lesions and have usually been reported as single cases. During the past 2 years, we have treated three patients with multiple cerebral arteriovenous malformations, representing 3.2% of a consecutive series of 95 arteriovenous malformation patients seen since 1976. Details on 17 other cases are available in the literature and are summarized here. The incidence of multiple arteriovenous malformations in major series ranges from 0.3% to 3.2%; the average incidence is 1.9% based on 21 cases encountered in a total population of 1102 arteriovenous malformation patients. Patients with multiple arteriovenous malformations often have other vascular anomalies of the brain or soft tissues, but the clinical mode of presentation, age, sex, and anatomical distribution of the lesions are the same as those of patients with single arteriovenous malformations. The use of four-vessel angiography in combination with magnetic resonance imaging may result in a higher detection rate for such cases. KEY WORDS: Arteriovenous malformations; Arteriography; Vascular anomalies
Among the vascular anomalies found in the central nervous system, multiple intracerebral arteriovenous malformations (AVMs) are thought to be exceedingly rare lesions. Although the coincidence of AVM and arterial aneurysm is frequently discussed, multiplicity of AVMs is usually not even commented upon in the reports of most large clinical series or pathological studies. The relative incidence of multiple cavernous malformations and telangiectasias has been estimated to be 25%, but no similar estimate has been made for true AVMs of either the cerebral hemispheres or the posterior fossa [19]. Multiple cerebral AVMs have usually been reported as isolated cases, often in the context of a more Address reprint requests to."Michael Salcman, M.D., 7801 York Road, Suite 102, Towson, MD 21204. Received November 11, 1991; accepted February 10, 1992.
© I992 by Elsevier Science Publishing Co., Inc.
widespread dysembryonic condition [8,20]. We have recently had the opportunity to analyze three cases, treated at the University of Maryland during the last few years. N o n e of these patients suffered from vascular or other anomalies in tissues other than the cerebral hemispheres. In addition to reporting these cases, we have attempted to determine the incidence of cerebral AVM multiplicity based on our own series and the available information in the literature.
Case Reports
Case 1 M.R. is a 42-year-old, right-handed, white female who presented to our service with an intraventricular hemorrhage and depressed sensorium in N o v e m b e r 1988 (Figure 1). Magnetic resonance imaging (MRI) revealed the presence of two very large AVMs, one occupying the posterior two thirds of the left temporal lobe and the second located in the right parietal lobe (Figure 2). Arteriography demonstrated multiple anterior temporal artery feeders from the left middle cerebral artery (MCA) entering the first lesion mesially, as well as contributing vessels from the left posterior cerebral artery; drainage was into the left sylvian system and the left petrosal sinus (Figure 3 A - C ) . The right parietal AVM was fed by posterior branches of the right MCA and drained into the superior sagittal sinus (Figure 3 D). Because of the proximity of the left temporal lesion to the temporal horn and the atrium of the lateral ventricle, it was assumed that this lesion was responsible for the intraventricular hemorrhage. A large left temporal-occipital craniotomy was carried out, with a complete excision of the lesion, the posterior two thirds of the temporal lobe, and the temporal-occipital junction down to the tentorial incisura. The superior gyrus of the temporal lobe was microsurgically spared; a preoperative Wada test had indicated mixed cerebral dominance for language in this patient. Postoperatively, the patient quickly recovered from transient dysphasia. Three months later, a right parietal craniotomy with gross total resection of the second AVM was carried out. A cerebral angiogram postop0090-3019/92/$5,00
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Figure 1. Case l. C T scan demonstrates an intraventricular hemorrhage into the lateral ventricle. eratively demonstrated no evidence of residual AVM. The patient's recovery was uneventful.
Case 2
S.F. is a 49-year-old white female with multiple medical problems who first presented with an intracerebral hemorrhage at the age of 47 years. She underwent a craniotomy for clot removal at another institution and remained well until D e c e m b e r 1988 when a second hemorrhage and profound hemiparesis resulted in her admission to the University of Maryland (Figure 4) for an emergency craniotomy and evacuation of a right subdural and intracranial hematoma. Although the patient was alcoholic and hypertensive, the triangular shape of the clot with its apex pointing to the ventricle and its base subjacent to the old craniotomy flap made us suspicious of an underlying AVM. An arteriogram (Figure 5) revealed the presence of two medium-to-large right-hemisphere AVMs, one in the frontal lobe and one in the temporal lobe. Each appeared amenable to resection, but the patient suffered multiple episodes of gastrointestinal hemorrhage and could not be brought to surgery.
Case 3
is a 28-year-old white female who presented with severe headache, neck stiffness, and seizures resulting L.L.
Figure 2. Case 1. Patient with two large AVMs. (A) T2-weighted axial M R I scan shows an A V M in the left temporal lobe. (B) T2-weighted axial MRI scan of the A V M in the posterior right parietal lobe.
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d
A Figure 3. Case I. (A) Left internal carotid angiogram, lateral projection. The temporal lobe A V M is fed by the left MCA. (B) The left vertebral injection demonstrates contributing vessels from the left posterior cerebral after), in the anteroposterior view. (C) Left internal carotid angiogram. /ateral projection. The venous drainage of the temporal lobe A V M is into the left ,lyh,ian system and left petrosal sinus. (D) Right internal carotid angiogram, lateral projection. The parietal lobe A V M is fed by posterior brancheJ of the M C A and drains into the superior sagittal sinus.
from a left temporal lobe hemorrhage in July 1987. H e r preoperative MRI (Figure 6) and arteriogram (Figure 7) indicated two relatively small AVMs in the left temporal lobe. A left temporal craniotomy was carried out, and a 1 × 1-cm capillary-like lesion was dissected out completely from the surrounding brain tissue. However, the
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Figure 4. Case 2. Axial CT demonstrates a right parietal subdural hematoma, intracranial and intraventricular blood, and deviation of the midline to the left.
Figure 5. Case 2. Right internal carotid angiogram, lateral projection. There are two AVMs, one in the frontal lobefed by the MCA and a second in the temporal lobefed by the posterior cerebralartery and posterior branches of the MCA.
Figure 6. Case 3. T l-weighted MR1 scan shows increased signal intensity in the left temporal lobe, suggesting hemorrhage mesial to the inner A VM.
large draining vessel seen on the angiogram was not identified. A postoperative arteriogram revealed the second A V M just medial to the other lesion (Figure 8), so a decision was made to explore the temporal lobe more posteriorly. T h e second A V M was found connected to the first by an interposed vein and was also completely resected. N o residual A V M was seen on the final postoperative angiogram.
Discussion T h e r e have been at least 20 cases of multiple cerebral AVMs reported in the literature; only two reports have described m o r e than a single patient in detail (Table 1). The earliest case appears to be a 35-year-old male with a basal ganglia lesion fed by the right M C A and anterior cerebral artery that bled on two occasions, who also had a smaller A V M in the caudate nucleus [10]. This case was reported in 1958 by H o o k and Johanson and is somewhat problematic due to the p o o r quality of the early angiograms and the close proximity of the two
Multiple Intracerebral AVM
lesions. Another early case was a 9-year-old boy, and it appears to be definitive because the right frontal AVM bled and the left occipital lesion was a presumed cause of headache [5]. This 1963 report is especially interesting because it also provided a review of other vascular anomalies encountered in a series of 97 patients with AVMs. T h e first report of the coexistence of a supratentorial A V M with a posterior fossa A V M is probably that of Tamaki et al in 1971 [20]. Current interest in the subject dates back to the series of four patients reported by Schlachter and colleagues in 1980 [16]. As several subsequent authors have pointed out, two or three of the four cases are questionable. Their second case had mirror lesions on the mesial surface of each parieto-occipital lobe, and it is possible that they were not really separate. The analysis of the third case was based on two lesions seen on computed tomographic (CT) scan in the left frontal and midbrain regions, without either published arteriograms or histology; the right frontal occult A V M was established histologically after evacuation of a C T - d o c u m e n t e d clot. It is possible that the other lesions in this case were cavernous malformations. Their fourth patient had a left tentorial A V M and a right parieto-occipital lesion that was described as cryptic, without even CT documentation. Nevertheless, the cases are included in Table 1 because of their historical importance. Voigt et al acknowledged that some communication might have existed between the two AVMs in their patient, since they shared a c o m m o n draining vein, and
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Figure 7. Case 3. (A) Left vertebral angiogram, anteroposterior view. Two small A VMs fed by the left posterior cerebral arter5 are visible medially and laterally. (B) Venous drainage of the lesion is to the petrosal sinus. No hematoma was visible by C T or at surger3, in the ttisue between these two lesions. Figure 8. Case 3. Postoperative left vertebral angiogram, Townes projection. Shows a small left posterior cerebral artery A V M medial to the other lesion, with venous drainage into the superior sagittal sinus.
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Table 1. Reported Cases of Multiple Intracranml Arteriovenous Malformations Source (year)
Case no.
Age/sec
Locations Right basal ganglia Caudate nucleus Right frontal Left occipital Right basal ganglia Posterior fossa Right centroparietal Right mesial parietal both sides of falx Right parasagittal Right parietotemporal Right parietooccipital Left parietooccipital Right frontal Left frontal Midbrain Left tentorium Right parietooccipital Right frontal Left parietal Right posttemporal Right parietal Left parietal Left parietal Right parietal Left superior frontal gyrus Right sylvian fissure Left medial operculium Right frontal Right temporal Left parietooccipital Right frontal Right temporal Right temporoparietal Left temporoparietal Left insular Left basal ganglia Right occipital Dorsal pons Left temporal Right parietal Right frontal Right temporal Left temporal Left temporal
Hook & Johanson [10] (1958)
1
35/M
Frugoni et al [5] (1963)
2
9/M
Tamaki et al [20] (1971)
3
19/F
Voigt et al [21] (1973)
4
28/F
Schlachter et al [16] (1980)
5
27/M
Schlachter et al [16] (1980)
6
29/M
Schlachter et al [16] (1980)
7
45/M
Schlachter et al [16] (1980)
8
33/M
Hanieh et al [8] (1981)
9
31/F
Shigemori et al [17] (1982)
10
47/F
Stone e~:al [19] (1983)
11
24/M
Zellem & Buchheit [24] (1985)
12
36/F
Reddy et al [13] (1987)
13
16/F
Romero et al [15] (1988)
14
36/M
Fong & Chan [4] (1988)
15
9/F
Nakayama et al [11] (1989)
16
40/M
Nakayama et al [11] (1989)
17
37/F
Present report (1992)
18
42/F
Present report (1992)
19
49/F
Present report (1992)
20
28/F
Arteries
Presentation
MCA & ACA Choroidal pericallosal ? ? Lenticulostriates Vertebral artery MCA )
SAH twice
MCA MCA ICA ICA ~ ? ? Meningohypophyseal ) ~ ? ~
Bled
Angular/posttemporal MCA Angular MCA Callosomarginal & MCA Parietal MCA ? MCA & ACA MCA MCA MCA MCA MCA MCA MCA MCA PCA Pontine MCA/PCA MCA MCA MCA/PCA PCA PCA
Clot, headache Staggering gait, blindness, retardation Seizures
Bled Headache, staggering gait, dysphasia Bled Seizures Clot
Bled Tinnitus for 13 years, headache, transient dysphasia Seizure
? Bled Bled Bled Bled Bled Bled
Abbreviations: M, male; MCA, middle cerebral artery; ACA, anterior cerebral artery; SAH, subarachnoid hemorrhage; F, female; ICA, internal carotid artery; PCA, posterior cerebral artery.
one was right centroparietal in location, while the other was right mesial parietal on both sides of the falx [21]. The case reported by Hanieh et al had histologic confirmation but no arteriography [8]. In 1985, Zellem and Buchheit reported the first patient with three AVMs; many of her family members had suffered cerebrovascular accidents and she had a cousin with an intracranial AVM [24]. Yasargil has also encountered a patient with three separate cerebral AVMs and gives brief accounts o f 14 other cases in his recent textbook [23].
In general, patients with multiple AVMs are similar to those with single malformations. The reported patients range in age from 9 to 49 years, with a mean of 30.6 years. There have been nine males and 11 females reported, but a disproportionate number of the questionable cases have been male. The MCA has been the most frequently involved feeding vessel, its anterior and posterior branches often supplying separate lesions in the same hemisphere. The second AVM has been located in the opposite hemisphere or in the posterior fossa on 14
Multiple Intracerebral AVM
occasions; these cases are generally indisputable. The great majority of patients presented because of an intraparenchymal or subarachnoid hemorrhage; a few patients were investigated because of headache, seizures, or retardation. Several of the patients have unusual family histories or other associated anomalies. The patient reported by Reddy et al had three separate AVMs; her brother sought medical attention for headaches and was noted to have Rendu-Osler-Weber syndrome [13]. The positive family history in Zellem and Buchheit's case has already been noted [24]. Some of the patients have had vascular anomalies of the face, neck, and eye [20] or in the soft tissues of the hand [8]. A patient with two AVMs also had four aneurysms and ectasia o f both anterior cerebral arteries [21]. A basilar artery aneurysm has been reported in association with three hemispheric AVMs [ 17]. We report one patient with three connecting AVMs on the same side. Patients with multiple intracranial AVMs, therefore, are likely to demonstrate within themselves or through family members a general tendency toward vascular maldevelopment. This is also demonstrated by the unusual case of a child with multiple AVMs in both the brain and the spinal cord [9]. The incidence o f multiple cerebral AVMs is difficult to determine from the literature, since relatively few o f the authors who have reported individual cases have also indicated the size of their personal series of treated patients. Conversely, a number of authors who have reported an AVM series have remarked on the occurrence o f an unusual case of multiplicity without further documentation. The first clinicians to do so were probably Patterson and McKissock in 1956, who mention one patient in a series of 110 cases with a left frontal AVM and "possibly" a lesion in the other hemisphere [12]. Drake et al reported that one o f their 66 patients with posterior fossa AVMs also had a second lesion supratentorially [3]. In a series of 500 AVM patients, Yasargil reported that 15 were multiple [23], and in a review of the Phoenix experience, there was one case in 300 [14]. The child reported by Fong and Chan was one of a series of 39 cases observed in the pediatric age group, while the child reported by Frugoni et al is from a series of 97 AVMs in both children and adults [4,5]. We have personally treated three cases in a consecutive series of 95 surgical patients, for an incidence of 3.2%; this estimate is probably on the high side (Table 2), although the likelihood of discovering such cases may be increasing in the era of MRI scanning. Each of our surgical cases was treated in the last few years. Excluding the pediatric and posterior fossa series, 21 cases have been encountered in a total o f 1105 AVM patients, for a reported mean incidence of 1.9%.
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Table 2. Incidence of Multiple Intracranial Arteriovenous
Malformations in Reported Series Source (year)
No. of cases
No. (c~) multiple
Patterson & McKissock [12] I1956) Frugoni et al [5] (1963) Yasargil [23] (1988) Rigamonti et al [14] (1987) Present report t1992) Total
1 I0
1 (0.9~ /
97
1 (1.0c)~)
500 300
15 (3.0g{) 1 (0.39¢)
95 1102
3 (3.29~) 21 (1.9,~/;)
The question naturally arises as to whether each of the AVMs in a multiply afflicted patient should be resected or otherwise subjected to treatment. Recent publications support the concept that AVMs represent a 1% to 3% annual risk of hemorrhage [1,2,6,7,22], whether previously ruptured or not. In a patient with more than one lesion, these probabilities are additive. The child reported by Fong and Chan first bled from the rightsided lesion at age 9 years and then bled again from the left-sided lesion at age 16 years [4]. Several of the other cases in Table 1 bled on more than one occasion, including our third patient. A decision to operate, therefore, should be based on (1) the patient's age, since this determines the remaining lifetime exposure to risk; (2) the patient's condition, as this affects the quality of life to be expected after treatment; and (3) the likely risk of resection as estimated by the grading scheme of Spetzler and Martin [18]. In every instance, the AVM that has most recently hemorrhaged or the one that is most symptomatic should be resected first if at all possible. Since the quality of life is often determined by the response to the first operation, all other things being equal, the largest and most difficult lesion should be attacked at the first procedure. In some cases, residual AVM as well as smaller multiple lesions might be treated with stereotactic radiosurgery. Since the morbidity and mortality of surgery (as well as the risk of hemorrhage and death) are also additive in multiple AVM patients, it is suggested that these lesions be treated in cerebrovascular centers.
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