Surg Neurol 1984,21:267-71 267 Coexistence of Bilateral Aneurysms of the Internal Carotid Arteries and an Arteriovenous Malformation of the Left Frontal Lobe Rom~in Garza-Mercado, M.D., Ricardo A. Rangel, M.D., and Juan F. Garza-V~izquez, MD Divisions of Neurosurgery, and Neurology, Faculted de Medicina y Hospital Universitario "J. Eleuterio Gonz~lez," Universidad Aut6noma de Nuevo Le6n, Monterrey, Nuevo Le6n, Mdxico Garza-Mercado, R, Rangel RA, Garza-V~quez JF. Coexistence of bilateral aneurysms of the internal carotid arteries and an arteriovenous malformation of the left frontal lobe. Surg Neurol 1984;21:267-71. A 44-year-old right-handed man was hospitalized because of a subarachnoid hemorrhage. He was drowsy on admission and exhibited a left partial third nerve palsy, right hemiparesis, and selective motor aphasia. A large subcortical arteriovenous malformation involving the left frontal lobe was demonstrated by angiography. The malformation filled from either carotid system and from the vertebrobasilar system as well. In addition, there were two bilaterally symmetrical (mirror) aneurysms of each internal carotid artery. Computed axial tomography revealed a left intratemporal-intraventricular hematoma. Deterioration of the patient's clinical condition occurred a few days after admission. Improvement was obtained after removal of the hematoma at a left subtemporal craniectomy, at which time the ruptured aneurysm arising from the left internal carotid artery was clipped. Sixteen months later, the intact aneurysm of the right internal carotid artery was clipped, and the arteriovenous malformation was radically excised through a bifrontal (Pool) craniotomy with microsurgical technique and with the aid of intraoperative angiography. The patient remained with a fixed neurological deficit, as observed preoperatively. KEY WORDS: Aneurysm, Arteriovenous malformation; Intracerebral hematoma; Intraoperative angiography; Multiple aneurysms; Subarachnoid hemorrhage The simultaneous association o f intracranial aneurysms and arteriovenous malformation is a fairly rare clinical condition. In 1959, B o y d - W i l s o n [7] analyzed 17 such cases from the literature, three o f his own included, and Addre.~s reprints requests to." Romfi.n Garza-Mercado, M.D., Aleutianas 396, Col. V. Hermosa, Monterrey, N.L., M~xico. ~c~198,/I by Elsevier Science PublishingCo., Inc. in 1981, Hayashi et al [18] accounted for 74. Such coexistence is even rarer when the arteriovenous malformation occurs with symmetrically opposite aneurysms of internal carotid arteries in a mirrorlike fashion, as in the case to be presented. Credit is given in the literature [7] to Walsh and King [40] as the first to record in 1942 a case of coexisting aneurysm and arteriovenous malformation. Their patient, a 50-year-old black man, was hospitalized because of subarachnoid hemorrhage. H e had a 4-year history of intermittent right frontal headache, right third cranial nerve palsy, and right homonymous hemianopsia. The clinical diagnosis o f a right supraclinoid aneurysm was corrobrated at the operation, but the aneurysm was found thrombosed. T h e patient died a few days later, and at necropsy a ruptured arteriovenous malformation of the left occipital lobe was disclosed, with intraventricular and subarachnoid hemorrhages. The aneurysm of the right internal carotid artery was unruptured and filled with a thrombus, and a symmetrical, although smaller, aneurysm was also found on the opposite internal carotid artery. Walsh [39] describes this patient as case 377 in his Clinical NeuroOphthalmology. The incidence of coexisting aneurysm and arteriovenous malformation has been recorded from 2.7% [31] and 3% [30] to 9 . 3 % [19]. In 490 patients with arteriovenous malformation, Perret and Nishioka [32] found 3 .7 cases of coexisting aneurysm (7.55%). O f the 34 of their patients studied in detail, there were six with two aneurysms, two with three, one with six, and another one with "multiple small aneurysms." In reviewing a series of 112 aneurysms found in 74 patients, Hayashi et al [18] noted 2 8 % to have multiple aneurysms. In reporting a personal series of 30 large (namely, larger than 2 cm [30]) arteriovenous malformations, 20 of which were submitted to microsurgical treatment, one of the authors ( R . G - M . ) found two patients with associated intracranial aneurysms (6.6%) [13]. One of these two patients had one aneurysm, the case hereby presented had two. 0090~ ~019/84/S ~.00 268 Surg Neurol 1984;21:267-71 Case Report A 44-year-old right-handed man was admitted to the Hospital Universitario on July 8, 1978. Two hours earlier he had been awakened from his sleep in the middle of the night by an intense headache of sudden onset. Although he could get up, only mumbling of unintelligible expressions were heard by the relatives, and a right-sided weakness was obvious. H e lapsed into a short period of unconsciousness before his admission to the hospital. The past history was significant only in that partial seizures involving the right side had occurred intermittently since age 11 years, when a diagnosis of meningitis (subarachnoid hemorrhage?) had been made. There was no history o f hypertension, renal dysfunction, or tobacco consumption. On examination, the patient was drowsy. H e responded to mild painful stimuli by flexion of the left extremities. His blood pressure was 140/70 mmHg, pulse 74 beats per minute, temperature 36.5°C, respiratory rate 17 breaths per minute. H e was unable to speak. T h e r e was a paresis of the lower right side of his face, and a partial left third nerve palsy. The left pupil was slightly dilated but reacted to light. The optic fundi were normal. T h e r e was a spastic hemiparesis of the right side, with increased deep-tendon reflexes and a right Babinski sign. Moderate stiffness o f the neck was noticed. N o lumbar puncture was performed then. Admitted to the neurology division, the patient improved by the next day, and he was well enough to attend simple commands. It was now evident that he had a motor aphasia. Laboratory data and x-ray studies of the skull and chest were normal. Angiograms of the bilateral carotid and right vertebral arteries (via a femoral artery) were made under local analgesia on the fifth day after admission. A large subcortical arteriovenous malformation containing a bilobulated varicose dilatation was seen to occupy most of the left frontal lobe. It was fed predominantly from the left anterior cerebral artery, with a few branches from the left middle cerebral artery. However, the malformation opacified equally well when the right carotid artery was injected, through a dilated anterior communicating artery, and it received an important contribution from the vertebrobasilar system also via branches of the left posterior cerebral artery. After two seconds, the malformation drained into both the superior longitudinal sinus and the deep venous system. The left middle cerebral artery was displaced upwards and medially. In addition, bilaterally symmetrical opposite aneurysms were observed on each internal carotid artery, at the level of the posterior communicating artery (Figure 1). Computed axial tomography performed on the seventh day of admission revealed an intratemporal-intraventricular hematoma on the left side (Figure Garza-Mercado et al 1). A neurosurgery consultation was then requested because of worsening of the patient's clinical condition. The patient was drowsier than before the computed tomography scan, and the third nerve palsy was now complete. The patient was promptly taken to the operating room. On the evening of July 15, 1978, an emergency left subtemporal craniectomy was performed under general endotracheal anesthesia. The dura mater was tense and not pulsating, and it was blue in color. After aspiration of 60 mL o f old liquified blood through a ventricular needle, pulsation of the dura mater was observed. A large intratemporal clot was removed through a 3-cm horizontal cortical incision in the second temporal gyrus after incising the dura mater. The hematoma, composed of dark-colored clots of different densities, was easily aspirated. The hematoma had broken into the ipsilateral temporal ventricular horn, and extended into the mesial portion of the temporal lobe. Although some abnormal vessels from the malformation were visualized, it seemed that the clot did not extend into the frontal lobe. Gentle retraction of the now-collapsed brain allowed exposure of the aneurysm arising from the left internal carotid artery, and occlusion of its neck with a curved Mayfield clip. It was obvious that the bleeding had occurred from rupture of the aneurysm and not from the arteriovenous malformation. It was felt unwise to attack the malformation at this time, so the wound was closed, leaving the dura mater open. The patient regained consciousness by the next day. H e improved enough to understand simple commands, but a selective motor aphasia persisted. The hemiparesis of the right side and the complete left third nerve palsy remained unabated when he was discharged from the hospital on September 3, 1978, after postoperative angiography of the bilateral carotid and right vertebral arteries. The aneurysm on the left internal carotid artery was excluded from the circulation, but the malformation, and the aneurysm on the right internal carotid artery had the same characteristics as before. The patient was hospitalized again from N o v e m b e r 28, 1978, through January 24, 1979, for treatment of recurrent bouts of pyelonephritis. The neurological signs remained fixed. Gelfoam embolization of the malformation via the femoral artery was unsuccessful. The patient was admitted to the hospital for the third time on October 25, 1979, for further neurosurgical treatment. There had been no recurrent bleeding episodes, the seizures had been under therapeutic control, and the neurological defciency remained stationary. The patient was cheerful, and understood simple commands in spite of his selective aphasia. The laboratory data were normal. Repeat angiography of the bilateral carotid and right vertebral arteries showed both the arteriovenous Combined Aneurysms and AUM Surg Neurol 1984;21:267-71 269 Figure 1. Bilatera/ carotid arteriograms. lateral tlieu's. The arteriorenous mal/brmation of the le/t frontal lobe is seen to have opacified equally well from the right ¢left) and the /eft (rightj carotid systems. The bilaterally opposite saccular aneu~.sms o[ the internal carotid arteries are clearly shown (arrows). malformation and the aneurysm on the right internal carotid artery unchanged. On N o v e m b e r 13, 1979, 16 months from the initial treatment, a bifrontal (Pool) craniotomy was performed under general endotracheal anesthesia. Exposure of the optic nerve and the internal carotid artery was accomplished bilaterally after ligature and section of both the superior and the inferior longitudinal sinuses, and retraction of the frontal lobes. Under microscopy the neck of the intact aneurysm of the right internal carotid artery was occluded with a straight Mayfield clip. The anterior communicating artery and the left anterior cerebral artery were grossly enlarged. They had an estimated threefold increase in diameter as compared with the right anterior cerebral artery. T e m p o r a r y occlusion of the left pericallosal artery with a Mayfield clip did not seem to significantly reduce the vascularity of the malformation, as seen in a single intraoperative angiogram of the left carotid artery. The malformation was then radically excised. A repeat intraoperative single angiogram of the left carotid artery showed absence of the malformation, with preservation of the parent vessels, as displayed also on the postoperative cerebral panangiography. The patient was discharged on D e c e m b e r 1, 1979 with no increase in his preoperative neurological deficit. However, he died at home on June 21, 1980, of bronchopneumonia. Discussion The coexistence of intracranial aneurysms and arteriovenous malformations has been reported by several authors [1,3,4,7-9,11,13,14,18,19,22,23,31,37]. The three basic theories are reviewed by some of them [7, Figure 2. Computed axial tomography. An intratemporal-intraventricular hematoma is observed on the/eft side. Postcontrast (Conr, teriovenous malformations. An analysis of 545 cases of intracerebral arteriovenous malformations and fistulae reported to the Cooperative Study. J Neurosurg 1966:25:467-90. 33. Reigh EE, Lemmen LJ. Cerebral aneurysms with other intracranial pathology. J Neurosurg 1960:17:469-':6. 34. Salazar JL. Surgical treatment of asymptomatic and incidental intracranial aneurysms. J Neurosurg 1980;53:2{)- 1. 35. Samson DS, Hodosh RM, Clark WK. Surgical management of unruptured asymptomatic aneurysms. J Neurosurg 1977 ;46:731-4. 36. Shenkin HA, Jenkins F, Kim K. Arteriovenous anomaly of the brain associated with cerebral aneurysms. (-ase report. J Neurosurg 1971;34:225-8. 37. Suzuki J, Onuma T. Intracranial aneurysms associated with arteriovenous malformations. J Neurosurg 19v9;50:7t2-6. 38. Vlahovitch B, Frerebeau PH, Ouaknine G, Billet M, Gross C. Angiography during operation on cerebrovascular malformations. In: DeJong RN, Sugar O, eds. Year book of neurology anti neurosurgery. Chicago: Year Book Medical Publishers, 1971:401-2. 39. Walsh FB. Clinical Neuro-Ophthalmology. 2nd ed. Baltimore: The Williams and Wilkins Company, 1957:831. 40. Walsh FB, King AB. Ocular signs of intracranial saccular aneurysms. Arch Ophthal (Chicago) 1942;27:1-~3. 41. Wirth FP, Laws ER, Jr., Piepgras D, Scott RM. Surgical treatment of incidental intracranial aneurysms. Ncurosurgery 1983:12:507-11.