THE WESTERN Journal of Medicine

Refer to: U Hoi Sang, Wilson CB; Surgical treatment of intracranial vascular malformations. West J Med 123:175-183, Sep 1975

Surgical Treatment of Intracranial Vascular Malformations HOI SANG U, MD, and CHARLES B. WILSON, MD, San Francisco

Arteriovenous malformations often pursue a progressive course, increasing in morbidity and mortality. Whenever possible they should be excised totally. The operating microscope, bipolar coagulation and high quality angiography have extended the generally accepted indications for surgical operation. Intraoperative adjuncts of contrast angiography and cardiac green have been helpful in accurately defining deep or complex lesions. CEREBRAL ARTERIOVENOUS MALFORMATIONS (AVM'S) were first described by Steinheil in 1895. Although classified as tumors (angiomas) by Cushing and Bailey' and Dandy,2'3 subsequent observations established their congenital and nonneoplastic nature.4-6 In the preangiography era, the study of AVM'S was confined to the operating table and to the postmortem examination. The introduction of angiography by Egas Moniz (1927) provided a means of studying their dynamic and anatomical characteristics. Clinical and

angiographic evaluation of patients harboring AVM'S has established their liability for expansion, repeated hemorrhage and seizures with associated morbidity and mortality. In 1948, Olivecrona7 predicted that conservative management would be ineffective in treating AVM'S, a projection that was subsequently confirmed by the disappointing long-term results reported by Moody and Poppen,8 Forster9 and Morello.'0 The nature of the AVM was well expressed by Potter," who anticipated the futility of carotid ligation, decompression and clipping of feeding arteries in long-term treatment. At best, these procedures provide temFrom the Department of Neurological Surgery, University of California, San Francisco. This work was supported in part by NINDS Training Grant

5593.

Submitted January 28, 1975. Reprint requests to: C. B. Wilson, MD, Department of Neurological Surgery, University of California, San Francisco, School of Medicine, San Francisco, CA 94143.

porary palliation because the AVM is- not eliminated. The treatment of choice is total excision, when possible, as dictated by the lesion's location and size. Our approach to the treatment of arteriovenous malformations reflects the current aggressive attitude expressed by many neurosurgeons. Advancements in angiography and surgical technology have broadened the indications for surgical treatment of these anomalies, and our purpose here is to present the results of treating 31 patients harboring AVM'S, many of which were considered unsuited for operation before the introduction of

surgical microscopy. Clinical Material This study comprises 31 patients treated by one surgeon (C.W.) on the Neurosurgical Service of the University of California Medical Center, San Francisco, during the period from 1968 to 1974 (Table 1). During the period covered by this study an equal number of patients did not meet our criteria for operation, the majority because of either large size or location of AVM'S, or both. In most instances these latter patients were referred by other neurosurgeons who had considered these malformations inoperable because of anticipated surgical morbidity and mortality. Because of reTHE WESTERN JOURNAL OF MEDICINE

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Figure 1.-(Case 7) Left, preoperative arteriovenous malformation (AVM) in the left parietal-occipital region. Right, postoperative excision of AVM.

ferral patterns our experience is heavily biased toward unfavorably situated lesions, and as a consequence the proportion of patients undergoing operation does not reflect the operability of AVM 's in an unselected sample. Twenty-nine cases were documented by angiography before operation. In two cases (6 and 20) the AVM presented as a mass, later identified at operation as hematoma secondary to an AVM. The surgical objective was excision or obliteration of the lesion, even when it was situated in crucial regions of the brain as in case 7 (Figure 1). This approach was modified for large malformations involving more than one third of a hemisphere (such as cases 2, 10 and 14). In one case (9), the patient was moribund from intracerebral hemorrhage, and surgical operation was undertaken as a palliative measure. In the patients in whom excision or obliteration of AVM'S was done, postoperative arteriograms made in 18 cases confirmed successful elimination of the AVM as shown in Figures 2 and 3. In the remaining seven patients treated similarly, no angiogram was made after operation, either because the patient refused or because of total elimination of the AVM at operation and the unjustified risk of angiography. Patients in the latter group have been followed for two months; seven months; two, three, four, five and six years and in none has there been an indication for postoperative angiography. Of the four patients treated with ligation of feeding arteries, two were studied postoperatively

-and in both, the residual malformation was smaller. Age at onset of symptoms ranged from 16 months to 58 years, and in one third (11 of 31) of patients initial symptoms developed in the third decade. The patients were distributed equally as to sex (16 and 15). Supratentorial AVM's predominated (25 of 31), with the greater number (15 of 25) occupying the right cerebral hemisphere. In almost one half (14 of 31) of patients, intracranial bleeding was the initial symptom, at an average age of 21 years, and the majority of these (9 of 14) presented with an intracerebral hematoma. In one fourth (7 of 31) of patients, the initial symptom was a seizure, occurring at an average age of 35 years and typically focal. Only three patients had headache (in the absence of recognized bleeding) as an initial symptom. Two patients described sensory phenomena and two had disturbance of speech as the initial symptom. Single instances of motor deficit, visual deficit and a bruit account for the remainder. Relationship of Symptomatic Hemorrhage and Epilepsy to Lesion Size The malformations divide into three groups: small (less than 2 cm in overall diameter), moderate (2 to 4 cm in overall diameter) and large (greater than 4 cm in overall diameter). The smaller lesions tended to present with hemorrhage, while the large ones were more often associated with convulsions (Table 2). THE WESTERN JOURNAL OF MEDICINE

179

INTRACRANIAL VASCULAR MALFORMATIONS

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Figure 2.-(Case 13) Left, preoperative arterlovenous malformation (AVM) in the right occipital pole (note arterial supply from the anterior circulation). Center, preoperative AVM showing supply from the posterior circulation. Right, postoperative excision of AVM.

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Figure 3.-(Case 18) Left, preoperative deep right parietal arteriovenous malformation (AVM) (lateral view). Center, preoperative deep right parietal AVM (anteroposterior view). Right, postoperative excision of AVM.

Diagnosis In all patients, angiographic studies were done, and in 29 patients, the diagnosis of arteriovenous malformation was established conclusively. The remaining two patients presented with intracerebral hematomas; the diagnosis was made at surgical operation and confirmed by pathological examination.

Surgical Technique Our goal was excision whenever possible, and the operating microscope was used in every case. Hypothermia-to approximately 31°C (87.8°F) -was used in four lesions, three of which were small or moderate in size, but located deep within the hemisphere. The fourth lesion was moderate in size and located in the dominant parasagittal TABLE

2.-Relationship

of Symptomatic Hemorrhage and Epilepsy to Lesion Size Small (17)

Hemorrhage ..... 8 (47%) Epilepsy ....... 2 (12%)

180

SEPTEMBER 1975

Moderate (7)

Large (7)

5 (71%) 1 (14%)

1 (14%) 4 (57%)

-

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parietal region. Exposure of deeply situated malformations necessarily promotes the development of postoperative cerebral edema, and in our opinion the lessened reactivity of hypothermic brain argues for the use of hypothermia in selected cases. Intraoperative arteriography and injection of cardiac green for identification of afferent vessels were used in three patients. Intraarterial injections were made through a catheter placed in the superficial temporal artery, directed into the external carotid artery and maintained with a constant infusion pump. For direct visualization of arteries contributing to the malformation, we injected a bolus of cardiac green (CardiogreenD, Guth Pharmaceuticals), 10 to 20 ml, and in each instance this method provided satisfactory color contrast for identification of arteries leading into the shunt. In two patients the lesion's small size and deep location dictated the use of arteriography for localization with the help of cortical markers. In the third patient, the lesion was large and superficial; arteriography and cardiac green were used

INTRACRANIAL VASCULAR MALFORMATIONS

for identifying afferent and efferent vessels in a feeder-clipping palliative procedure to ensure adequate reduction of the AVM. Hypotension was not used in any patient.

Mortality (Two Cases, 6.4 Percent) One death early in the series resulted from uncontrolled intraoperative intraventricular bleeding that led to irreversible cardiac arrest. Removal of the AVM in this patient had been abandoned by another surgeon, and the patient was referred to us after recurrent bleeding. The second death resulted from immediate postoperative complications. In this patient there was massive intracerebral hemorrhage secondary to restoration of blood flow to a chronically ischemic cerebral hemisphere. Both deaths followed attempts to excise massive malformations.

Postoperative Condition (After Excision or Obliteration) The majority of disabilities (about three quarters) were reversed by excision of the AVM, and about one fourth of the patients improved. New disabilities appeared in four cases. In the first case, a patient in whom there was a moderatesized left medial occipital AVM, the operation included clipping of the posterior cerebral artery resulting in a right homonymous hemianopia, which subsequently showed pronounced improvement. In the second case a moderate-sized parasagittal left parietal AVM was excised, causing mild weakness in the patient's right leg. Two months after operation the weakness has resolved and the patient now walks without a limp. In the third patient, there was a moderate-sized left parietal lesion at the trigone, and postoperatively a transient right hemiparesis and dysphasia developed, with progressive improvement over two years. Grand mal seizures were also experienced, twice in two years; these are now under control. The fourth case (Figure 4) was that of a patient with a left cerebellar tonsillar lesion in whom unexplained positional vertigo developed four weeks postoperatively despite intact neurological status for the first two weeks after operation. This has now cleared completely. Of the patients who had intracranial hemorrhage (14 cases), five patients have been followed from two to seven months, and the rest for one to six years; in none of these has bleeding recurred. In one patient, a single grand mal seizure occurred.

Of the patients presenting initially with epilepsy (six cases), followed from seven months to six years in four cases, none had recurrence of seizures. Two patients, in both of whom progressive neurological deterioration and repeated bleeding developed before surgery, were operative deaths.

Postligation of Feeding Vessels Feeding vessels were ligated in four cases. After five years of followup, patient 2 has not shown significant improvement. Patient 9 was moribund and in coma before operation. Now at two years of age, he is retarded and severely incapacitated. Patient 10, three years postoperatively, has been asymptomatic and is working full time. Patient 14 was quadriparetic and mute before operation; she has improved sufficiently to resume preparing meals and keeping house. Mentation is intact and the patient has regained normal speech. Postoperative Angiographic Evaluation * Postexcision and obliteration group (25 cases). In 18 patients (72 percent), findings on postoperative angiographic evaluation showed complete obliteration of the AVM. Seven patients were not studied, and at this time none has had clinical symptoms requiring evaluation. * Postligation of feeding vessels group (4 cases). In the two cases studied, AVM size decreased. Two cases were not studied following operation. Follow-up Status (Table 3)

*Twenty-nine patients have been followed for periods ranging from two months to six years (ten patients were followed for up to one year, nine patients for one to two years, two patients for two to three years, two patients for three to four years, one patient for between four and five years, and five patients for five to six years). Table 3 compares preoperative to postoperative capacity. Before operation, 60 percent of patients were moderately to severely incapacitated, while only 29 percent were minimally, or not at all, incapacitated. Although the number of patients in the minimally incapacitated group did not increase postoperatively, the number of patients with full capacity increased; accordingly the number of patients with moderate to severe incapacity decreased. THE WESTERN JOURNAL OF MEDICINE

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INTRACRANIAL VASCULAR MALFORMATIONS

Figure 4.-(Case 31) Left, preoperative left cerebellar tonsillar arteriovenous malformation (AVM) (lateral view). Center, preoperative left cerebellar tonsillar AVM (Towns view). Right, postoperative excision of AVM.

TABLE 3.-Working Capacity Before and After Surgical Operation Preoperativ e

Status

Postoperative

Full capacity ...... .. 1 Incapacitation Light .... 8 ..... Moderate ..... ... 9 Severe .... .... 10 Coma .... ..... 1 TOTALS .......

..

29

17 7 3 2 0 29

Full capacity: asymptomatic, no deficit, fully employed. Incapacitation Light: No symptoms to minimal symptoms, minimal deficit, fully employed. Moderate: Mentally alert and independent, full self care, moderateiy symptomatic, has moderate motor or sensory deficit (for example, paresis), unemployed or partially employed. Severe: Mentally confused, severe subjective complaints, severe motor or sensory deficit (for example, plegias), requiring care.

Discussion In the present series, the majority of patients became symptomatic in the 20 to 40 year age group, a finding similar to that of Morello'0 and Paterson.'2 The distribution between male and female is equal in our group, although other authors have reported an increased incidence in males.7"0'2 Presenting symptoms and their relative frequencies are also similar to those noted by Paterson.'2 Forster,9 Henderson'3 and Morello'0 report hemorrhage as the more frequent presenting symptom, in as many as 75 percent of cases; although McKenzie'4 and Olivecrona7 reported the greater prevalence of seizures. Smaller malformations bleed more frequently while the larger ones are more prone to manifest themselves by seizures, either focal or general.10"12"15 The natural history of AVM'S iS one of symptomatic recurrence with progressive disability especially in those that bleed.9"2-'4"16"17 Our patients 15 and 30 illustrate the point. Olivecrona stated, "In the end, probably most, if not all, patients 182

SEPTEMBER 1975 * 123 * 3

die of hemorrhage or are completely incapacitated. Mental deterioration is a common feature in cases of an inveterate lesion."7 According to the Cooperative Study,'2 the mortality from the initial hemorrhage is about 10 percent, the risk of a second hemorrhage is 20 percent with a mortality of 13 percent for the second hemorrhage and about 20 percent for subsequent hemorrhage. Potter" presented a plausible pathophysiological mechanism for recurrent bleeding and Waltimo'8 provided evidence that these malformations, when small, tend to enlarge. Presented with such an unfavorable natural history, there is no strong argument for conservative treatment. Surgical treatment has taken the form of decompression, exploration, ligation of internal carotid artery and ligation of feeding vessels-as well as total excision or obliteration. Our experience with ligation of feeding vessels is limited and inconclusive. The results of surgical procedures other than total excision have been disappointing,7-9" 9-2' and most surgeons regard total excision as the treatment of choice.7,9'10'16'19'2' Traditionally indications for surgical operation have been: (1) repeated subarachnoid hemorrhage, (2) intracerebral hematoma and (3) progressive intractable neurological disability. To these indications we have added (1) malformation causing seizure without prior bleeding, if favorably situated for excision with minimal risk of producing a major functional deficit, (2) small malformation associated with prior minor bleeding and situated in an important functional region and (3) some malformations previously considered inoperable because of depth or size or both. These inclusions evolved as a direct consequence of three factors: (1) improved angiographic delineation of afferent and efferent ves-

INTRACRANIAL VASCULAR MALFORMATIONS

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Figure 5.-(Case 12) Left, preoperative arteriovenous malformation (AVM) in the right occipital lobe (anteroposterior view). Center, preoperative AVM in the right occipital lobe (lateral view). Right, postoperative (first operation) showing the residual anteriorly placed segment of the AVM.

sels, (2) bipolar coagulation and (3) the operating microscope. Others, particularly Kunc,19 have reached similar conclusions. Improved illumination and magnification afforded by the operating microscope allow more precise excision and protection of adjacent normal brain. Intraoperative angiography and repeated injections of cardiac green for direct visual verification of critical afferent and efferent vessels have been used selectively. These techniques are especially helpful in accurately localizing small deep malformations, and for extensive malformations where the meshwork of vessels can be con-

fusing. The surgical mortality rate and postoperative follow-up status in the present series compare favorably with other series as reported by Kunc,'9 Morello,'0 Paterson and McKissock,12 Forster9 and Moody.8 Patients presenting with hemorrhage have been free of recurrence after total excision or obliteration. Contrary to the experience of others," 2'8-'0 we excised six lesions in patients who presented with seizures and, in follow-up, seizures have not recurred. However, the period of observation is short, and anticonvulsant medication has been continued in all cases. One patient who presented with intracerebral hemorrhage developed grand mal seizures that are now controlled by medical management. Postoperative angiographic study is important, particularly in cases where total excision of the lesion is in doubt. In all patients, postoperative angiograms have confirmed total excision. One patient (illustrated in Figure 5) was shown to have residual malformation and a second pro-

cedure was carried out with angiographicallyconfirmed total removal. Smacher and coworkers16 reported their unfavorable experience with incompletely removed malformations underlining the indication for postoperative angiography. REFERENCES 1. Cushing H, Bailey P: Tumors Arising From the Blood Vessels of the Brain. Springfield, Ill., Charles C Thomas, 1928 2. Dandy WE: Arteriovenous aneurysm of the brain. Arch Surg

17:190, 1928 3. Dandy WE: The Brain-A Classical Reprint. New York, Hoeber Medical Division, Harper and Row, 1969 4. Kaplan HA, Aronson SM, Browder EJ, et al: Vascular malformation of the brain-An anatomical study. J Neurosurg 18: 630-635, 1961 5. Hamby WB: The pathology of supratentorial angioma. J Neurosurg 15:65-75, 1958 6. McCormick WF: The pathology of vascular ("arteriovenous") malformation. J Neurosurg 24:807-816, 1966 7. Olivecrona H, Riives J: Arteriovenous malformation of the brain. Arch Neurol Psychiatry 59:567-602, 1948 8. Moody RA, Poppen JL: Arteriovenous malformation. J Neurosurg 32:503-511, 1970 9. Forster DMC, Steiner L, Hakanson S, et al: Arteriovenous malformation of the brain. J Neurosurg 37:562-570, 1972 10. Morello G, Borghi GP: Cerebral angiomas. Acta Neurochir 28:135-155, 1973 11. Potter JM: Angiomatous malformation of the brain. Ann Royal College of Surg 16:227-243, 1955 12. Paterson JH, McKissock W: A clinical survey of intracranial angiomas with special reference to their mode of progression and surgical treatment. Brain 79:233-265, 1956 13. Henderson WR, Gomez R: Natural history of cerebral angiomas. Br Med J 4:571-574, 1967 14. MacKenzie I: The clinical presentation of cerebral angioma. Brain 76:184-214, 1953 15. Waltimo 0: The relationship of size, density, and localization of intracranial arteriovenous malformation to the type of initial symptom. J Neurol Sci 19:13-19, 1973 16. Smacher AL, Allcock JM, Drake CG: Cerebral angiomas: The sequelae of surgical treatment. J Neurosurg 37:571-575, 1972 17. Perret G, Nishioka H: Arteriovenous malformation-An analysis of 545 cases of craniocerebral arteriovenous malformation and fistulas reported to the cooperative study. J Neurosurg 25:467-490, 1966 18. Waltimo 0: The change in size of intracranial arteriovenous malformation. J Neurol Sci 19:21-27, 1973 19. Kunc Z: Surgery of arteriovenous malformation in the speech and motor-sensory regions. J Neurosurg 40:293-303, 1974 20. Norlen G: Arteriovenous aneurysms of the brain. J Neurosurg 6:475-494, 1949 21. Pool JL: Treatment of arteriovenous malformation of the cerebral hemisphere. J Neurosurg 19:136-141, 1962

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