Surg Neurol 1987;27:323-30 323 The Perivenous Technique of Resection of Arteriovenous Malformations from Vital Areas of the Brain Otakar R. Hubschmann, M.D., and Abbott J. Krieger, M.D. Section of Neurological Surgery, University of Medicine and Dentistry, New Jersey Medical School, Newark, and the Veterans Administration Medical Center, East Orange, New Jersey Hubschmann OR, Krieger AJ. The perivenous technique of resection of arteriovenous malformations from vital areas of the brain. Surg Neurol 1987;27:323-30. A total of 17 patients with arteriovenous malformations (AVMs) in sensitive areas of the brain were operated on and the AVMs were completely resected using perivenous techniques. No patient suffered a new neurological deficit following surgery. The perivenous surgical technique is most suitable for small AVMs in sensitive cortex. It differs from the standard approach in that it places emphasis on perivenous microsurgical dissection, identification of the nidus before major arterial feeders, and early ligation of selected venous channels. Three different types of venous drainage--single, multiple, and dual--were identified. Each different type of venous drainage requires a different surgical approach for the best results. KEY WORDS: Arteriovenous malformation; Perivenous resection; Transvenous technique; Microsurgery; Subarachnoid hemorrhage; Intracranial hemorrhage T h e recent introduction o f magnetic resonance imaging (MRI) and increasingly m o r e sensitive computed tomography (CT) scanning devices, together with digital subtraction angiography, have led to the discovery of many arteriovenous malformations (AVMs) on routine work-up prior to their rupture. As a result, the question of surgical resection is often raised in patients who were previously considered inoperable. Due to better technical skills, radiographic delineation, and m o d e r n anesthesia, the resection o f "silent" or "polar" AVMs is becoming a routine procedure. H o w e v e r , the resection of A V M s from sensitive areas such as m o t o r cortex, speech area, or deep white matter abutting on essential neural structures still presents formidable technical difficulties [ 1 , 3 - 5 , 8 , 9 , 1 8 - 2 0 ] , as resection of any brain tissue surrounding an A V M in sensitive areas during the course Address reprint requests to: Otakar R. Hubschmann, M.D., 100 Bergen Street, M.S.B. Room H-592, Newark, NJ 07103. © 1987 by Elsevier Science PublishingCo., Inc. of surgery, or occlusion of blood supply to normal brain surrounding the malformation, will lead to a permanent neurological deficit. A basic principle of surgery for AVMs has been the early occlusion of its arterial supply. T h e venous drainage has always been scrupulously protected, as an inadvertent injury to the system necessitating its early ligation would lead to a catastrophe. While this principle can be met readily in large AVMs, particularly in polar or less eloquent areas, where the search for arteries feeding the AVM early during the resection is better tolerated, a similar search in a sensitive area will expose the brain to excessive and perhaps intolerable trauma. With the evolution of microsurgical techniques we have become increasingly aggressive and have been able to resect AVMs in eloquent areas by dissecting around veins draining the AVMs leading to the nidus. T h e occlusion of major arterial supply (MAS) has been left until an opportune time, and no effort has been made to search for the MAS early, unless it was readily accessible. However, to take full advantage of this technique one must recognize the specific types of venous drainage and tailor a specific technique to the type of venous drainage pattern. This report, with illustrative case presentations, describes the salient points o f this technique. Materials and Methods A total of 17 patients were operated on with AVMs in the following areas: m o t o r area (8), speech area (8), and close vicinity of the internal capsule (1). All patients were followed by a neurologist both preoperatively and postoperatively. Postoperative angiograms demonstrating a total resection of the AVMs were p e r f o r m e d on 15 patients and reviewed by a neuroradiologist. T w o patients refused a postoperative angiogram. T h e resection in these patients was judged to be complete by the operating surgeon. Age, sex, location of the AVM, and postoperative results at 6 months are summarized in Table 1. The following is the classification of the main venous draining patterns o f different AVMs with a de0090-3019/87/$3.50 324 Surg Neurol 1987;27:323-30 Hubschmann and Krieger Table 1. Patient Data Patient No. Age (years) Sex Preoperative signs and symptoms I 46 F TIA, speech arrest, SAH 2 42 M 3 12 M SAH, transient expressive aphasia Intracerebral hematoma, aphasia, complete flaccid right hemiplegia and coma 4 32 M 5 28 F 6 56 M 7 56 8 Location Left angular middle temporal gyrus Left middle frontal gyrus Left middle frontal gyrus TIA, SAH 4/5 right upper extremity paresis Intracerebral hematoma, right lower extremity plegia Intracerebral hematoma, left hemiplegia coma Left posterior frontal parietal lobes Left posterior frontal lobe M Seizures, headaches 14 M 9 10 46 42 M F 11 52 M SAH, intracerebral hematoma, right homonymous hemianopsia, right sixth nerve palsy SAH Intracerebral hematoma, SAH, right lower extremity plegia SAH Left temporal parietal lobes Left posterior periventricular parietoocciptal regions 12 13 28 22 F M SAH Intracerebral hematoma 14 30 F 15 16 42 18 F M 17 21 M Intracerebral hematoma, right hemiplegia SAH SAH, mild right hemiparesis (4/5) SAH Right posterior frontal, parietal lobes Left posterior frontal lobe Left medial posterior frontal Left middle temporal gyrus Left insular region Left insular region Postoperative (6 month activity) No deficit, normal activity No deficit, normal activity No dysphasia on routine testing, (3/4) upper and (4/5) lower extremity paresis, normal mental status Mild (4/5) right upper extremity paresis Minimal (5-/5) right lower extremity paresis Left upper extremity (1/5) and left lower extremity (4/5) paresis Asymptomatic, no aphasia Right homonymous hemianopsia Asymptomatic Right lower extremity paresis No deficit, normal activity Left motor cortex No deficit, normal activity Mild dysphasia, no motor weakness Mild right hemiparesis Right motor cortex Left motor cortex No deficit, normal activity No deficit, normal activity Right motor cortex No deficit, normal activity Abbreviations: SAH, subarachnoid hemorrhage; TIA, transient ischemic attack; 0/5, no function; 5/5, normal motor function. scription o f the surgical techniques most suitable for their resection and illustrative case reports. Three main types of venous drainage patterns have been recognized: single, multiple, and dual. Single In this type o f pattern, there is only one venous draining channel. This can be either superficial (cortical) or deep (galenic). Superficial. This AVM is usually small and located in the subcortical white matter (Figure 1). The only draining channel is a singular cortical vein draining into either the midline or lateral sinuses. Deep. The primary drainage is into the internal cerebral vein and the vein o f Galen. The AVM is located in deep white (periventricular) matter (Figure 2). There is no recognizable cortical draining vein. Single-A Type (Superficial): Case 1. A 32-year-old black woman was admitted after the sudden onset o f severe headaches and the rapid development of a flaccid, left lower-extremity monoplegia with only minimal drift of the left upper extremity and total sparing of the face. A CT scan showed a hematoma in the medial aspect o f the hemisphere and an AVM (Figure 1). At surgery, the main draining vein was followed from the cortical surface to the nidus of the AVM in retrograde fashion. The whole AVM was identified and totally resected. After surgery, the patient awoke rapidly with a total hemiplegia on the left; including face, arm, and leg equally. The full return of function to the face and the upper extremity was complete within 24 hours, and she could walk unaided in 2 weeks. At 6 months, Perivenous Resection of AVMs Surg Neurol 1987;27:323-30 325 Figure I. Single, superficial venous drainage. Preoperative (left) and postoperative (right) angiograms. her findings were limited to a minimal weakness of the lower extremities, characterized primarily by a 5-/5 left iliopsoas weakness, hyper-reflexia, and an upgoing toe on that side. Functionally, there was only a barely noticeable limp. Single B-Type (Deep): Case 2. An 11-year-old boy presented with the sudden onset of severe headache, difficulty with speech, and rapidly progressing right hemiplegia. When seen after a transfer from another hospital, he had aphasia, right hemiplegia, and did not follow verbal stimuli. An angiogram showed a deep AVM in the left frontal region with only a deep draining vein (Figure 2). At surgery, a cortical incision was made, and a hematoma encountered at about 2 cm below the cortex was evacuated. Arterial feeding vessels were identified and occluded. The deep draining vein was occluded last. Figure 2. Single deep venous drainage. Postoperatively, the patient had right hemiplegia and aphasia. His state of consciousness gradually improved, and he started to utter simple words about 7 days after surgery. His recovery was excellent, and he eventually returned to school. He plays recreational soccer although he has a significant 3/5 upper and 4/5 lower extremity spastic hemiparesis and mild dysphasia demonstrable through specific neuropsychological testing. In cases of a single superficial draining vein, the technique of perivenous resection as described by Malis is utilized [12]. In the case of a single deep draining vein, the precise localization of an AVM is essential as no visible marks are present on the cortical surface. This Figure 3. Multiple superficial venous drainage. A, primary vein,"B, lateral and C. medial secondary draining veins. 326 Surg Neurol 1987;27:323-30 Hubschmann and Krieger Figure 4. Preoperative preparation. Arterial phase (/e_~), 1.'enousphase (middle). and the composite sketchings ~right) shou'ing the relative relationship.~ of artertal and venous structures. Figure 5. Three different types of surgical approaches dictated by the t),pe of renous drainage [rom the AVM. The sequence of steps taken in occluding the vascular channels is indicated by numbers and arrows. I SIN6LE vENous DRAINAGE A. 51N6LE-SUPERFICIAL DEEPVEIN ' ARTERIES I~. 5 1 N G L E - D E E P , ~.~5~CONB',R'Y --VEIN IIIDUAL-SUPERFICIAL/DEEPBJ ~ Perivenous Resection of AVMs Surg Neurol 1987;27:323-30 327 trary to all other types of AVMs where early occlusion of selected draining veins is performed deliberately and where such occlusion facilitates the AVM resection. Multiple In this type of AVM there are two or more major draining veins from the AVM. Depending on circumstances, these can be one of the following. Type A--Superficial. Primary drainage is into either medial or lateral sinuses, usually both (Figure 3). Type B--Deep. We have not yet encountered an AVM with purely deep multiple draining veins. The technique for single-deep draining veins would be used if this was encountered. Figure 6. Dual venous drainage. A, deep draining channel," B and C, superficial draining channels. venous pattern is obviously not suitable for the perivenous technique and the classical technique should be used. In both of these types of AVMs, it is obvious that utmost care be taken not to occlude the draining veins prior to a complete resection of the AVM. This is con- The Multiple Type A (Superficial): Case Report. A 33year-old right-handed man presented with a history of several years of headaches and a seizure disorder. A recent subarachnoid hemorrhage necessitated his admission. On admission, he had only a mild hemiparesis (4/5) in the proximal muscles of the right upper extremity, hyperreflexia, and minimal spasticity. There was, however, a significant degree of functional impairment of the hand, specifically, clumsiness of the fingers and thumb during rapid alternating movements. His angiogram and the relationship of the AVM to the motor strip is seen in Figure 4. At surgery, a total resection of the AVM was achieved. After surgery, the patient exhibited a total Figure 7. Corrosionpreparation of A VM showing that dissection along a draining vein (B) will lead directly to the nidus of th'e AVM (A_). The more deeply located arterial supply comesfrom both the anterior and middle cerebralarteries (C). (Courtesy Dr. H. KaplanJ 328 Surg Neurol 1987;27:323-30 hemiplegia of the arm, face, and leg, although he was fully awake. The initial return of function began in the legs and proximal muscles of the upper extremity on the fourth day; and in 2 weeks the patient was able to walk with minimal assistance and lift his arm about 40 °. At 6 weeks, he had findings similar to the preoperative ones except for the hand, but he was able to feed himself. At 6 months, his neurological examination was virtually the same as it was preoperatively, although the hyperreflexia and the spasticity were somewhat greater than before surgery. In this type of AVM there are several cortical draining veins of various sizes. One or two large ones are termed primary. They are identified on angiogram by their size and how early the dye enters during angiography. During surgery they are protected, while all the others are transected and followed toward the nidus in a sequential manner. The main arterial feeders are clipped in depth after the cortical (secondary) venous drainage channels are transected. These maneuvers result in a substantial decrease in size of the AVM which is then delivered on the last remaining large draining vein toward the sinus (Figure 5). Dual (Superficial and Deep) The AVM has two or more major draining channels, one draining into superficial, lateral, or medial sinuses, and another into the galenic system. There are usually several draining veins (Figure 6). Case Report. A 58-year-old man presented with a history of several years of headaches and seizures that had recently increased in frequency. The seizures necessitated the performance of a CT scan which demonstrated a large AVM located in the left temporal lobe (Figure 6). Cerebral angiogram had confirmed the presence of an extensive AVM in both the temporal and parietal lobes. At surgery, total removal of the AVM was achieved. Postoperatively the patient did well, was afebrile, but had a significant receptive dysphasia. Computed tomography scan showed evidence of postoperative swelling which persisted for several weeks. The dysphasia gradually improved, but 6 weeks after surgery, a drainage from the wound was noted. The cultures were positive, and an infected bone flap was diagnosed. At surgery, an epidural collection of pus communicating with a small intracerebral extension was evacuated and the bone flap was removed. Postoperatively his dysphasia rapidly improved and he was discharged. Four months later he was readmitted for a cranioplasty. His postoperative course was uneventful and cosmetic results were excellent. There Hubschmann and Krieger was no evidence of dysphasia or any other neurological impairment at the time of discharge. In this instance, as in all types with dural venous drainage, the resection was started superficially in the temporal tip where there were several draining veins emptying into the sphenoparietal sinus. The resection then proceeded towards the lateral aspects up to the vein of LabbC which was preserved. The veins were transected in a gradual fashion and retrograde dissection was continued until the edge of the AVM was identified. Dissection was then directed towards the medial aspect where both deep venous drainage as well as the main arterial supply entering the AVM were identified and ligated. The AVM was then delivered on the vein of Labbd, which was then transected before entering the sinus (Figure 5). Discussion Recently several excellent reviews have summarized the natural history of AVMs. It is generally thought that about 5 million people in the United States and Canada harbor AVMs [5]. Serious neurological disability is generally produced by either a hemorrhage, which takes place in approximately 50% of all patients, or by a dementia-like syndrome related to a combination of relative ischemia of the normal tissue due to shunting through the AVM and its pulsatile force [5,7,10,13]. Even though the relative risks of dying from cerebral hemorrhage in patients with AVMs are less than in those harboring aneurysms, they still remain formidable. It is estimated that in those patients where hemorrhage was the initial presenting symptom, the likelihood of further bleeding is between 4 % and 6 % per year. In those where the initial symptom was either headache, seizure, or progressive neurological deficit, the likelihood of further bleeding is 1 % - 2 % per year [5,10]. It is further reported that approximately half of those that suffered a non-fatal hemorrhage are left with a fixed neurological deficit. It is clear, therefore, that the best surgical candidates in prevention of morbidity and severe disability are young patients whose longer life expectancy makes them statistically more likely to suffer fatal hemorrhage. Similarily, patients where the AVM is located in a vital area and where even a small hemorrhage leads to a significant fixed neurological deficit are theoretically the best candidates. This is the group of patients, however, where the risks are the greatest. Surgical risks can be divided into two main groups. The risks to life have been significantly reduced, although not totally eliminated, in recent years. In the larger series, Drake [4] reported the mortality rate of 3% for supratentorial AVMs in 166 cases; and there Perivenous Resection of AVMs were several smaller series where no mortality was reported [8,11,18]. The risks to neurological function have attained greater significance as the risks to life have lessened and surgeons become bolder in attempting to resect AVMs from more and more sensitive areas o f the brain. While it is clear that resection o f AVMs from vital areas of the brain is possible without producing a new neurological deficit, such surgery remains technically difficult. Several authors reported such results several years ago, and the number of neurosurgeons capable of duplicating those results has increased recently with the widespread application of microsurgical techniques [3,4,6,8,11,17,19-22]. The main causes of mortality are the development of uncontrollable bleeding which takes place upon unplanned entry into the AVM, tear o f major AVM channels, inadvertent occlusion of the main venous drainage channel, or as reported recently, the socalled "breakthrough" bleeding [2,15,16]. While the former causes could, at least theoretically, be eliminated with improved techniques, the breakthrough bleeding is thought to be due to a loss of autoregulation caused by a sudden change in the pressure and blood flow through normal brain upon rapid clipping of the AVM. Some authors, however, suggested that in some cases such bleeding may be due to an incomplete removal of the AVM [14]. At surgery, in most instances, the draining veins are encountered first as they lay more superficially than the arterial blood supply. In some instances, no vessels are visible on the cortex, or the remaining visible structure is the only draining vein, premature occlusion o f which would result in a "blow out" of the AVM. The basic technique o f occluding the feeding artery first is both a logical and time tested procedure. In some instances, however, such a procedure results in undue retraction or blind section of the cortex, which in itself may produce an irreversible neurological deficit. In such instances, primary dissection of veins has been recommended [12]. Our current technique is as follows: After the angiogram is reviewed, a line drawing o f the major arteries and veins is completed on transparent paper. This composite picture utilized sequential arteriograms in both early arterial and late venous phases to include as many details as possible about both the normal and abnormal vessels. This careful tracing sometimes reveals important relationships that may have escaped notice during a routine review o f the angiogram. Outlines of the skull are also included with the drawing. This allows for a more precise placement of the bone flap (Figure 4). The recent availability of a rapid sequence o f computerized pictures obtained with intraarterial digital subtraction angiography allows a repeated review o f stored angiograms. Although this is often helpful in clarifying specific points Surg Neurol 1987;27:323-30 329 on the angiogram, it does not fully replace the line drawing described above [8]. Retrograde dissection along the draining vein into the nidus allows dissection to be limited to the AVM (Figure 7). Such an approach is particularly useful in dealing with smaller AVMs in the motor strip or speech area where surrounding cortical structures carry essential neurological function. In both dual and multiple types, there is an early, deliberate occlusion of some of the draining vessels when more than one o f each type (superficial/deep) is present. Following a review of an angiogram, the largest draining vein is termed primary, and all others are termed secondary draining channels. The first step is a retrograde perivenous dissection along one of the secondary veins. Once the edge of the AVM is identified, the vein is occluded, transected, and used as a handle to resect the rest of the lesion. The glial plane is entered, and resection is continued towards another secondary vein. The arterial feeders and small vessels entering the AVM from the surrounding brain are identified and coagulated using bipolar cautery or surgical clips depending on the size of the vessel to be occluded. The primary draining channel is left for last and the AVM is delivered upon it as on a stalk. The dissection is carried out using either a microscope or magnifying surgical loops, bipolar cautery, and gentle traction if necessary. We no longer routinely use a microscope for resection of the entire AVM. Usually we reserve its use only for specific portions of the malformation such as dissection along a main draining vein, or if the AVM is very small. In none of our cases did early occlusion of one or several draining veins result in a premature rupture o f the AVM. In fact it appeared to have allowed a more direct access to the glial plane and feeding vessels. Similarly, we have not encountered a single instance o f the so-called breakthrough bleeding. It appears that the sequential occlusion of several of the secondary venous draining channels causes a gradual increase in the resistance to the flow within the AVM and some return of autoregulation. The utilization of the retrograde dissection of the proximal end of the draining vein leads to the nidus of the AVM in most instances. It can be used repeatedly at several sites, provided one or two main draining veins are preserved. The three different techniques that we have utilized according to the three different patterns of the venous drainage of the AVM are shown in Figure 5. We have reserved the classical approach for instances where the main feeding arteries are readily available for clip application, or where there is no visible pathology on the cortical surface. We feel that the utilization of the transvenous technique helps to achieve greater success in resection of AVMs from vital areas of the brain. 330 Surg Neurol 1987;27:323-30 The authors are grateful to Dr. H. Kaplan who graciously allowed us to use Figure 7 and whose early anatomical studies have made the surgery of arteriovenous malformations easier for all of us. References l. Amacher AL, Allocock JM, Drake CG. Cerebral angiomas: the sequelae of surgical treatment. J Neurosurg 1972;37:571-5. 2. Day AL, Friedman WA, Sypert GW, et al. Successful treatment of the normal perfusion pressure breakthrough syndrome. Neurosurgery 1982;11:625-30. 3. Drake CG. Surgical removal ofarteriovenous malformations from the brain stem and cerebello-pontine angle. J Neurosurg 1975;43:661-79. 4. Drake CG. Cerebral arteriovenous malformations: considerations for and experience with surgical treatment in 166 cases. Clin Neurosurg 1979;26:145-208. 5. Drake CG. Arteriovenous malformations of the brain. 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