0148-396 X/86/1801-0029$02.00/0 NEUROSURGERY Copyright © 1986 by the Congress of Neurological Surgeons Vol. 18, No. 1, 1986 Printed in U.S.A. Intracranial Arteriovenous Malformations Associated with Aneurysms Hunt Batjer, M.D., Richard A. Suss, M.D., and Duke Samson, M.D. Division of Neurosurgery, Department of Surgery (HB, DS), and Division of Neuroradiology (RAS), University of Texas Health Science Center, Dallas, Texas The presence of intracranial aneurysm in association with arteriovenous malformation has been well documented. Aneurysms have been described in typical proximal sites along the feeding system to the arteriovenous malformation, in abnormal distal locations along feeding vessels, and in sites remote and apparently hemodynamically unrelated to the arteriovenous malformation. Little attention has been focused on the most appropriate medical and surgical care of patients harboring these lesions. Since 1977, 22 patients with this combination of lesions have been evaluated at our institution. Nine patients (41%) presented after intracranial hemorrhage. The remaining 13 patients were investigated because of seizures in 5 patients (23%), headaches in 4 patients (18%), and progressive ischemia in 4 patients (18%). Among the patients suffering intracranial hemorrhage, 78% had bled from an aneurysm, with 22% having hemorrhaged from their arteriovenous malformation. All 7 of the patients who suffered aneurysmal hemorrhage bled from atypical distal aneurysms on major feeding vessels. Our experience and that of others has led us to believe that the safest approach to patients with this combination of lesions is to treat the aneurysm before microsurgical resection of the | associated arteriovenous malformation. Hemodynamic changes associated with the abrupt elimination of an arteriove- nous malformation may place associated aneurysms at immediate risk. (Neurosurgery 18:29-35, 1986) Key words: Aneurysm, Arteriovenous malformation, Subarachnoid hemorrhage Walsh and King in 1942 reported the first example of a patient harboring an aneurysm and an arteriovenous malfor- mation (AVM) (19). After their publication, numerous case reports and small series began to appear in the literature (2, 3, 5: 17). That this combination of lesions was particularly hazardous both with and without surgical therapy was em- phasized by Perret and Nishioka in 1966 in the Cooperative Aneurysm Study (13). In their report, 9 of 18 conservatively managed patients and 6 of 16 surgically managed patients died. Gamache et al. in 1981 reviewed 42 medically managed patients from the literature. They found that 38% died, 7% had significant neurological difficulties, and only 14% were doing well (6). Several published series have suggested that between 2.7% (12) and 9.3% (9) of patients with AVMs have associated aneurysms. Most recent series using current diagnostic meas- ures imply that the incidence of this combination is probably higher than the expected natural occurrence of aneurysms in the general population. These reports have described aneu- rysms in typical proximal sites along the feeding system to the AVM, in abnormal distal locations along feeding vessels, and in sites remote and apparently hemodynamically unre- lated to the AVM. The apparent clustering of aneurysms along feeding vessels has provoked considerable discussion about the mechanism of formation of aneurysms in general. Most publications have dealt with the descriptive aspects of this patient population: significantly less attention has been paid to the most appropriate medical and surgical manage- ment of these patients. Since 1977, 22 patients with this combination of intracra- nial vascular lesions have been evaluated and treated at The University of Texas Health Science Center at Dallas. This group comprises 14% of our total operative AVM series during this time. The present retrospective review was under- taken to examine this population carefully in terms of symp- toms, the anatomical relationship of aneurysms to AVMs, and therapeutic morbidity and mortality. CLINICAL MATERIAL Twenty-two patients with an intracranial AVM and at least one arterial aneurysm have been evaluated and treated by us since 1977. Most of these patients were referred to our insti- tution by neurologists and neurosurgeons for the considera- tion of surgical therapy. The remaining patients presented to Parkland Memorial Hospital from the Dallas area after the development of neurological symptoms. The referral nature of our patient population may in part explain the heavy predominance of aneurysms in our AVM patients. Fifty-nine per cent of our patients were male, and 41% were female. The patients ranged in age from 11 to 55 years. Nine patients (41%) presented after intracranial hemorrhage (Table 3). There were 7 cases of subarachnoid hemorrhage (SAH), 1 case of intraparenchymal hemorrhage, and | case of isolated intraventricular bleeding. The remaining 13 pa- tients were investigated because of seizures in 5 patients (23%), headaches in 4 patients (18%), and progressive ische- mia in 4 patients (18%). Nineteen of the 22 patients under- went surgical procedures; operation was directed toward the aneurysm alone in 8 cases, toward the AVM in 3 cases, and at both lesions in 8 patients. ILLUSTRATIVE CASE REPORTS Case 6 This 47-year-old, right-handed man developed double vi- sion insidiously over several weeks, followed by a SAH. He was admitted to our institution in Hunt-Hess Grade | status. His initial computed tomographic (CT) scan revealed a small amount of localized blood in his left ambient cistern. Angiog- raphy demonstrated a distal superior cerebellar aneurysm located on a major arterial feeder to a left cerebellar hemi- sphere AVM (Fig. 1). At operation on the following day, his superior cerebellar aneurysm was encased in fresh clot. This 30 BATJER et al. Neurosurgery, Vol. 18, No. 1 Fic. 1. Case 6. A 47-year-old man with a new left 4th nerve palsy and SAH. Anteroposterior (A) and lateral (B) vertebral arteriograms demonstrate a ruptured distal left superior cerebellar artery aneurysm and a left cerebellar hemisphere AVM fed by the left superior cerebellar artery. aneurysm was clipped, sparing the 4th nerve, which was stretched over its fundus. One month later, the patient was readmitted for the clipping of an incidental right middle cerebral artery aneurysm and the subsequent removal of his small AVM. He remains neurologically intact. Case 3 This 45-year-old, right-handed man was transferred to our hospital 2.5 weeks after a SAH from which he had completely recovered. A CT scan showed relatively diffuse subarachnoid blood, perhaps most apparent in the interhemispheric fissure. Angiography revealed a large AVM involving the left mesial occipital lobe, the left pulvinar and splenium, which were fed by the left anterior cerebral artery, and the left posterior cerebral artery (Fig. 2). Also present were a large, basilar P-1 aneurysm on the right, a left P-1-P-2 junction aneurysm, a small intracavernous carotid aneurysm, an anterior commu- nicating artery aneurysm, and a distal left pericallosal artery aneurysm. At operation, the large basilar aneurysm and then the smaller P-1-P-2 junction aneurysm were clipped. Next, the small and unruptured anterior communicating artery aneurysm was clipped. As the source of hemorrhage had not yet been found, the dissection through the gyrus rectus was continued following the left A-2 branch. Fresh hemorrhage was noted in the subarachnoid space and in the brain paren- chyma immediately surrounding the patient’s pericallosal aneurysm. This aneurysm was clipped and evacuated. The patient made a slow but steady recovery from his craniotomy and is now back to his premorbid state of health. We have elected to defer resection of his large and asymptomatic AVM. Case 15 This 17-year-old, right-handed boy sustained a sudden ictus and was admitted to the hospital in a bilaterally decerebrate condition with a dilated and fixed left pupil. A CT scan revealed a large parietal hemorrhage with significant subarach- noid blood (Fig. 3). Immediate arteriography revealed a small parietal AVM fed predominantly by the contralateral anterior cerebral artery. There was an irregular fusiform aneurysm on the anterior cerebral artery in immediate proximity to the malformation and hematoma. Emergency operation for evac- uation of the hematoma and clipping of the ruptured aneu- rysm was performed, but the patient’s neurological deficit did not improve. He ultimately died a neurological death 2 weeks postoperatively. Case 8 This 22-year-old, right-handed woman presented with SAH during pregnancy. Arteriography demonstrated a right frontal AVM with feeding from the right pericallosal artery (Fig. 4). Two proximal carotid wall aneurysms were noted. It was presumed, probably incorrectly, that the patient had bled from her AVM, and she was managed as a high risk preg- nancy. After the completion of her pregnancy, she underwent the resection of her AVM and the clipping of her two proximal carotid wall aneurysms. Unfortunately, 2 weeks postopera- tively she sustained a second SAH. She subsequently under- went the clipping of her previously unrecognized distal ante- rior cerebral artery aneurysms and ultimately made a full neurological recovery. January 1986 ANEURYSM/AVM 31 Fic. 2. Case 3. A 45-year-old man with diffuse SAH. P-|-P-2 junction aneurysms involved with the feeding sys A and B, preoperative arteriograms demonstrate pericallosal, carotid wall, basilar, and em to a deep thalamic mesial occipital AVM. C and D, postoperative arteriograms show clipping of the ruptured anterior cerebral aneurysm and other asymptomatic intradural aneurysms. RESULTS Five of the 19 operative patients have died, for an operative mortality rate of 26%. One of these patients (Case 10) under- went the clipping of his aneurysms and multiple feeders to his AVM as the initial stage of a planned two-stage resection. He tolerated the procedure well, but died suddenly 1 week later of pulmonary embolism. A second patient (Case 15) was left comatose after a dev- astating subarachnoid and intraparenchymal hemorrhage. His operation was directed at the removal of his life-threatening clot and the clipping of his aneurysm. He unfortunately did not improve after operation and ultimately died of uncon- trolled intracranial hypertension. Two patients (Cases | and 11) died as a result of massive intraoperative hemorrhage. Patient | harbored a large (5-cm), right, prerolandic malformation that had been treated by staged ligation of middle cerebral and anterior cerebral feeders and by clipping of her incidental distal middle cerebral aneu- rysm. One week later, she returned to the operating room for definitive resection. Late in the dissection, after her lateral ventricle had been entered and the major thalamostriate draining vein had been dissected but not sacrificed, the brain became tense and numerous previously coagulated vessels in the gyral bank surrounding her malformation suddenly began to bleed. Her AVM was quickly removed without abatement of the hemorrhage. Her carotid artery was ultimately sacri- ficed intracranially after hypotension failed to improve the situation. Carotid ligation allowed control of this catastrophic bleeding, but the patient developed severe neurological deficit postoperatively and died 6 days later. We suspect that the resection of this large, high flow malformation may have resulted in normal perfusion pressure breakthrough. Patient 11 had suffered SAH from a distal right superior 32 BATJER et al. Bow cerebellar artery aneurysm on a feeding vessel to a 3-cm cerebellar hemispheric AVM. After recovery from her SAH and the subtemporal clipping of her aneurysm, she underwent an elective suboccipital craniectomy. Because of the broad representation of her malformation on the superior surface of the cerebellar hemisphere, we planned to operate with her in the sitting position. During the initial stages of the dissection, uncorrectable major air embolism was encountered. We quickly rolled her into the prone position and redraped. Neurosurgery, Vol. 18, No. 1 Fic. 3. Case 15. A 17-year-old boy who presented bilaterally decerebrate after a sudden ictus, 4, the CT scan reveals a large parietal hemorrhage with intraventricular and subarachnoid blood. B and C, preoperative angiograms demonstrate the rup- tured anterior cerebral aneurysm with its associated AVM. During this episode, she never became hypotensive, but her pulmonary pressures were altered significantly. Although the cerebellum was slightly more full than it had been while she was in the sitting position, we unfortunately decided to pro- ceed with the removal of her malformation. Relatively early in the resection of her malformation, a small tuft of vessels was amputated from the vascular mass. The resultant bleeding very shortly became uncontrollable. Despite attempts to ex- tirpate her lesion quickly, massive hemorrhage from within January 1986 Fic. 4. Case 8. A 22-year-old woman with SAH. A, the preoperative early phase arteriogram shows proximal carotid and distal anterior cerebral aneurysms. B, later phase arteriogram reveals a mesial frontal AVM. the 4th ventricle developed, and she quickly became hypoten- sive and suffered cardiac arrest. We suspect that the hemo- dynamic alterations produced by her air emboli contributed to the escalation of a technical error that should have been relatively easy to correct. In retrospect, the procedure should have been terminated at the onset of serious air embolism. The final patient (Case 5) never awakened after the resec- tion ofa large vermian AVM. Postoperative CT scans revealed that he had sustained brain stem hemorrhage during his Operative procedure. One patient (Case 20) developed a new expressive aphasia after his AVM resection; fortunately, the aphasia is improving. The remaining 13 patients in the operative series (69%) have had good outcomes, with a return to their premorbid occu- pations. A striking 50% of our 22 patients harbored multiple aneu- rysms. A total of 44 aneurysms were detected, with 82% of the aneurysms being located in hemodynamic association with the malformation (see Tables | and 2). Fifty per cent of these aneurysms were located proximally along the feeding system of the AVM. If one considers the pericallosal origin a distal site for aneurysmal development, 32% of all aneurysms were located in atypical distal points along major feeding vessels. The remaining 18% of the aneurysms were found in sites remote from the patients’ AVMs. All nine patients who suffered intracranial hemorrhage underwent surgical procedures (Table 3). Two patients in that group died (22%), one of whom was comatose at the time of operation. At present, six of these nine patients (67%) have returned to their previous occupations. The source of hem- orrhage in the nine patients who had bled was determined by surgical findings correlated with CT scan and angiographic evidence. Seven of the nine patients (78%) had bled from an aneurysm, with the remaining two patients (22%) having bled from their AVM. All seven patients who had suffered aneu- rysmal SAH had bled from aneurysms located in atypical distal sites on major feeding vessels. None of the aneurysms at sites remote from the AVM ever bled, to the best of our ET ANEURYSM/AVM 33 TABLE | Summary of Clinical Data No. Patients 22 Aneurysms 44 Patients with single aneurysms 1 Patients with multiple aneurysms Il - TABLE 2 Location of Aneurysms No. Aneurysms Anterior —_ Posterior Total circulation circulation Proximal on the feeding 17 § 22 (50%) vessel Distal on the feeding 10 4 14 (32%) vessel Remote from the AVM 5 3 8 (18%) TABLE 3 Outcome in Patients with Hemorrhage Case Location of Hemorrhage Result? 1 SAH Died 3 SAH Good 6 SAH Good 7 SAH Good 8 SAH Good 15 SAH, intraparenchymal Died 16 Intraventricular Good 20 Intraparenchymal New aphasia (resolving) 22 SAH Good “Good, return to previous occupation. 34 BATJER et al. knowledge. Looked at another way, 68% of our patients presented with symptoms referrable to their AVMs and 32% presented with symptoms from associated aneurysms. DISCUSSION There has been considerable variability in the literature regarding the exact location of aneurysms associated with AVMs. Cronqvist and Troupp reported a series in which 69% of the aneurysms were located on the main arterial feeders of the malformations (5). Suzuki and Onuma noted a 44% incidence of aneurysms located on major feeders (18). In the Cooperative Study report by Perret and Nishioka, only 37% of the aneurysms were on major feeders, with 42% of the aneurysms in sites remote from the malformation (13). Several theories have been advanced to explain the apparent association between aneurysms and AVMs. Paterson and McKissock thought that the increased blood flow through the arterial feeders of the AVM contributed to the development of aneurysms (12). Anderson and Blackwood wrote that both lesions were simply part of a constellation of multiple vascular anomalies in the same patient (1). Boyd-Wilson thought that the association of these lesions was probably coincidental (4). There is considerable circumstantial evidence to support the theory of Paterson and McKissock. The hemodynamic effect of an AVM is reflected primarily in decreased intravas- cular resistance in its feeding vessels (15) and the attendant marked increase in arterial flow (4). Somach and Shenkin reviewed six patients who had undergone carotid artery liga- tion for the treatment of intracranial aneurysm (16). Repeat arteriography 3 to 10 years postoperatively revealed that two of these patients had developed aneurysms on the contralat- eral internal carotid artery. The authors concluded that in- creased flow in a cerebral artery predisposes to the develop- ment of an aneurysm. Conversely, Hayashi et al. (8), Shenkin et al. (14), and Koulouris and Rizzoli (11) all described significant decreases in the size of previously documented aneurysms on feeding vessels to AVMs after surgical obliter- ation of the AVM. Whether the arteriographic changes are due to intraluminal thrombosis or to intimal thickening is unclear, as is the long term fate of these aneurysms that have apparently diminished in size. Nevertheless, these important cases do lend credence to the relationship between increased flow and the development or growth of intracranial aneu- rysms. As a result of these latter studies, some authors have concluded that this phenomenon offers a possible alternative to the radical surgical treatment of both intracranial lesions in that excision of the AVM in some cases may result in the eventual obliteration of the associated aneurysm. Our personal philosophy regarding the surgical approach to these patients is colored by our experience (Case 8) and that of Drake (personal communication, May 1984) and Kassell (10), each of whom has described individual cases of the operative resection ofan AVM followed during the immediate postoperative period by disastrous SAH from an aneurysm on a feeding vessel. In spite of the few reported instances of this complication, such occurrences suggest that the sudden increase in vascular resistance associated with the abrupt resection of an AVM puts aneurysms in its feeding system at immediate risk of distension and possibly subsequent rupture. This risk is present even if the aneurysm has not previously bled. A similar but perhaps less persuasive argument can be made regarding the risk for aneurysm rupture remote from the AVM. After elimination of the sump effect with resection of Neurosurgery, Vol. 18, No. 1 the AVM, the vessels on which these aneurysms are located may be subjected to increased flow, with a resultant height- ened risk of future aneurysmal rupture. These concerns have led us to modify our surgical approach to patients with combined lesions. In almost all patients presenting with SAH from whatever source, seizures, or is- chemic neurological deficits, the intracranial aneurysm is treated first. Data from the Cooperative Study suggest that rebleeding from AVMs is not common during the first several posthemorrhage weeks (13). In fact, Graf et al. found that the risk of rebleeding is only 6% over the Ist year (7). Exceptions to this general rule are cases of large intraparenchymal clots from AVMs or patients with unrelated remote aneurysms. Obliterating the aneurysms and then microsurgically resecting the AVM is the safest approach to symptomatic lesions of this type. In our series, aneurysms on the feeding vessels to AVMs bled commonly, and aneurysms remote from the AVMs did not bleed. This experience causes us to wonder whether the natural history of aneurysms on feeding vessels is more malignant than that of uncomplicated unruptured aneurysms. For this reason, we most frequently recommend elective obliteration of aneurysms associated with AVMs in asymptomatic patients even if subsequent resection of the malformation is not contemplated. ACKNOWLEDGMENTS The authors extend special thanks to the physicians who referred these difficult patients to us and for the secretarial support of Ms. Jolene Jackson and Mrs. Vicki Rankin. Received for publication, March 12, 1985; accepted, August 24, 1985. Reprint requests: Hunt Batjer, M.D., Department of Surgery, Division of Neurosurgery, The University of Texas Health Science Center at Dallas, 5323 Harry Hines Boulevard, Dallas, Texas 75235. REFERENCES 1. 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