The surgical approach to arteriovenous malformations of the lateral and sigmoid dural sinuses
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1 J Neurosurg 59:32-39, 1983 The surgical approach to arteriovenous malformations of the lateral and sigmoid dural sinuses THORALF M. SUNDT, JR., M.D., AND DAVID G. I~EPGRAS, M.D. Cerebral Vascular Research, Mayo Foundation, Rochester, Minnesota v- Arteriovenous malformations (AVM s) of lateral and sigmoid sinuses are acquired lesions evolving from a previously thrombosed dural sinus. Their natural history is usually that of gradual progression and hence surgery is frequently necessary. The preferred surgical treatment is complete excision coupled with packing of the sigmoid sinus. The operative approach is illustrated and discussed in detail. Results and complications are reviewed in 27 patients whose symptomatology had progressed under conservative management; 22 of these cases harbored primary lesions and five had recurrences. There were 22 excellent, one good, and two poor results (both of the latter from blindness that preceded surgery). There were two deaths, both in patients previously operated on with incomplete removal or obliteration of the AVM by attempted embolization. KEY WORDS " arteriovenous malformation 9 dural arteriovenous malformation 9 lateral sinus 9 sigmoid sinus 9 operative approach 9 neurosurgical procedure RTERIOVENOUS malformations (AVM s) of the lateral and sigmoid dural sinuses are relatively uncommon lesions. However, our experience to date suggests that their natural history is often one of relentless progression, and that ultimately surgical excision is usually required. Patients with this anomaly represent an important group for the attention of neurosurgeons. In a previous communication 3 we have reviewed the clinical symptomatology of these malformations, the relatively sparse literature on the subject, l 2 4-1~ and their angiographic appearance. We presented evidence that these are acquired abnormalities, evolving from revascularization of a previously thrombosed sinus. We will consider in this report the surgical approach to these lesions. Clinical Material From January, 1973, to November, 1982, 27 patients underwent surgery at the Mayo Clinic for excision of an AVM of the lateral sinus. These patients ranged in age from 18 months (the only malformation considered to be truly congenital) to 76 years, with a mean age (excluding the child) of 54 years. There were 17 females and 10 males in this group. Sixteen lesions were located on the left lateral sinus and 11 on the right. Five cases had undergone surgery previously. These patients presented with a variety of complaints, including headache, pulsatile tinnitus, transient ischemic events, and obscuration of vision. Papilledema was a common finding, and two patients were blind from chronically increased intracranial pressure (ICP). The most common presenting symptom in these patients was pulsatile tinnitus and the most common finding on neurovascular examination was a bruit over the occipital area. Table 1 summarizes the number of primary complaints identified in the 27 patients reported here. All patients underwent preoperative angiograms. Early in the series postoperative angiograms were performed only when clinically indicated. Later in the series, following the introduction and standardization of transfemoral angiographic techniques, these studies were performed commonly. The epicenter of the AVM was most often found at the junction between the lateral TABLE 1 Frequency of most common clinical symptoms and signs in 27 patients Symptoms and Signs No. of Cases pulsatile tinnitus 25 bruit 24 headache 11 impaired vision 9 papilledema 7 32 J. Neurosurg. / Volume 59/July, 1983
2 AVM s of lateral and sigmoid dural sinuses FIG. 1. Cerebral angiograms of a dural arteriovenous malformation. Left: Anteroposterior projection, showing crossfilling through the torcula to the opposite lateral sinus. Right: Lateral projection illustrating the major contribution from the occipital artery and its major branches to the malformation. Note the neovascularity of the dura superior, inferior, and anterior to the lesion. and sigmoid sinuses. The occipital artery was the dominant feeder in most cases. The incidence of associated sinus occlusions or identifiable thrombi within the sinuses is summarized in Table 2. In addition to the 27 patients reported here, we saw three patients in consultation. Two of these were managed conservatively; one had a small lesion which spontaneously thrombosed, and the other patient was lost to follow-up review. A third patient was treated with selective embolization. Results of surgery were graded in four categories: excellent, if the patient returned to employment or normal retired life with no residual neurological deficit; good, if he/she resumed normal living but with some impairment in function, whether related to a preoperative deficit or not; poor, if he/she did not recover sufficient function to be classified as good; and death. An illustrative case is presented. Case 12. This 77-yearoold woman came to the Mayo Clinic in 1975 because of a loud noise in her left ear TABLE 2 Associated frequency of sinus thrombosis Type of Occlusion No. of Cases occlusion of ipsilateral sinus 11 thrombus, ipsilateral sinus 3 thrombus, contralateral sinus 2 bilateral sinus occlusions 2 which prevented normal sleep. She indicated that this had been present for 2 years, during which time it had gradually increased in intensity. On neurological examination no focal deficits were found, but she did have evidence of early papilledema. Computerized tomography (CT) was normal. Cerebral angiograms (Fig. 1) revealed a large malformation of the left lateral sinus with cross-drainage through the torcula to the opposite sinus. The patient underwent surgery in October, 1975 (Figs. 2 and 3). The estimated blood loss for the operation was 8 units, approximately one-half of which was lost in a 4-minute interval that followed elevation of the bone plate. The patient awoke promptly from the operation and made a good recovery. She was discharged 10 days thereafter and remained well until mid-1981 when she developed mild symptoms of senility believed to be unrelated to the AVM. Positioning the Patient Surgical Approach The patient can be positioned semi-prone, as was the patient in the illustrative case (Fig. 2), or supine with the head turned sharply (Fig. 4A). In either case, it is necessary that the surgeon have ready access to the region between the inion and the mastoid. A malleable lumbar spinal needle is placed for later drainage of cerebrospinal fluid (CSF). J. Neurosurg. / Volume 59 ~July,
3 T. M. Sundt, Jr. and D. G. Piepgras current just below their insertion onto the occipital bone. Invariably a number of large feeding and draining vessels are encountered here, which require coagulation or even clipping. The pericranium is now incised and stripped away from the bone along the path for the craniotomy (Fig. 4B). FIG. 2. A curvilinear scalp incision extending inferior to the lateral sinus. It is shaped so that this structure can be exposed, with retraction, from the petrous bone to torcula. Scalp Flap The incision used is shaped much like a question mark (Figs. 2 and 4A). There is more than average bleeding from the scalp margins which must be controlled and secured well to prevent troublesome or unnoticed blood loss during the remainder of the case. The scalp flap is reflected to its base exposing the mastoid process, and the occipital margin retracted to the inion. In so doing, a greatly enlarged occipital artery and posterior auricular artery is doubly ligated and divided, along with the many of its branches. In some instances, the major blood supply to the malformation has thereby been interrupted. Soft- Tissue Dissection After the scalp flap is reflected, the deep cervical fascia and nuchal musculature are incised with a cutting Craniotomy The craniotomy is effected using the cutting bit of the air drill (Figs. 3 left and 4B). This is a very important step, and considerable care and thought are required to avoid potentially catastrophic bleeding. The craniotome should not be used here, as a laceration of the highly vascular dura or sinus (both of which are quite adherent to the bone) could produce a fatal hemorrhage -- analogous to the rupture of an intracranial aneurysm before the bone plate is elevated. The air drill must be held at an angle of approximately 30* to the bone; if it is held vertically it tends to drill through the bone. As the craniotomy is deepened, the drill bit is switched to a smaller one which allows better visualization in the depth of the cut and lessens the risk of a dural tear. The dura can be visualized through a thin layer of bone when the craniotomy has been carried to a sufficient depth. The surgeon is now in position to elevate the bone plate. Prior to removing the bone, preparations should be made for the possibility of a major loss of blood in a very short time. This is variable and seemingly is related to amount of venous drainage which has developed from the AVM through the diplofi of the bone. We have found it helpful to lower the blood pressure and to start a rapid transfusion of blood at the time the bone plate is elevated. In spite of the above measures the rapid loss of blood can be shocking to the patient and staggering to the surgeon. We have calculated blood loss to approach 300 ml/minute on several occasions. Although FIG. 3. Left: Craniotomy is performed using a high-speed air drill. It extends above and below the lateral sinus and from the petrous bone almost to the midline. The proximal portion of the sigmoid sinus is visible through this craniotomy. Right: The dura is opened above and below the lateral sinus to facilitate resection of this structure. 34 J. Neurosurg. / Volume 59 ~July, 1983
4 AVM s of lateral and sigmoid dural sinuses the loss is great, it can usually be slowed and controlled by digitally compressing a large piece of Surgicel reinforced with a surgical sponge packing over the entire expanse of the exposed dura. The margins are then gradually enlarged as the pack is withdrawn and bleeding points individually arrested with bipolar coagulation until the pack is removed (Fig. 4C and D). Sinus Ligation After achieving good hemostasis, the margins of the dura are firmly affixed to the margins of the craniotomy with tacking sutures placed about 2 cm apart. These numerous sutures are required to obliterate the epidural space, which is more vascular than normal because of its participation in the drainage pattern of the AVM. The lateral sinus lies in the mid-area of the craniotomy (Fig. 4E). Two dural incisions are made parallel to the long axis of the sinus, one superior and the other inferior to the sinus. These are enlarged by secondary incisions vertical to them so that two T s are created above and below the sinus (Fig. 4E). Then 30 to 40 ml of CSF is withdrawn through the malleable needle FIG. 4. A: Schematic representation of skin incision and area of bone to be excised. B: Bone plate is elevated using air drill which is held at a 30* angle to prevent perforation of the dura. The area of osteotomy is gradually increased peripherally around the margin of the bone plate until the dur ~ is just barely visible through a thin layer of cortical bone. The bone plate is then elevated using a periosteal elvator. C and D: Following removal of bone plate, dural bleeding can be profuse. This is controlled with bipolar coagulation of bleeding points and a large piece of Gelfoam which is placed over the entire expanse of exposed dura and held in place with uniform digital compression. The margins of the dura are then gradually exposed as the packing is retracted and bleeding points individually coagulated. E: Preparations are made for excision of the lateral sinus by opening the dura above and below the lateral sinus with incisions that parallel the long axis of the sinus. J. Neurosurg. / Volume 59 ~July,
5 T. M. Sundt, Jr. and D. G. Piepgras FIC. 4. F: After the dura has been opened, it is tacked up to the margins of the craniotomy securely with multiple closely placed dural tacking sutures. The sinus is then incised between two hemostats occluding the sinus proximally and distally. G: The medial portion of the sinus is closed with a running dural suture. The lateral portion of the sinus containing the arteriovenous malformation (AVM) is elevated from the wound using a hemostat and excised from the tentorium. Major bleeding points on the tentorium are best controlled with hemostatic clips. In cases with a large vein of Labb6 it is occasionally possible to save this vein by carrying the incision directly into the sinus itself and then closing the sinus with a running suture so that the vein of Labb6 can drain into the superior petrosal sinus. H: The AVM is excised as far lateral as the petrosal bone and a considerable portion of the petrosal bone is removed with a high-speed air drill. Bleeding from this area can be profuse but is controlled with cauterization of the bone using the cutting current of the Bovie coagulator and bone wax. Examination of the excised specimen will often reveal a thrombus in situ. I: Following excision of the lateral sinus at its junction point with the sigmoid sinus, the sigmoid sinus is packed with Surgicel and then closed with a running suture to the dural or fascial patch. previously placed in the lumbar spinal space. Bridging veins off the occipital pole and superior cerebellum are coagulated with the bipolar coagulator and divided. Two curved hemostats are next placed with an intervening distance of at least 1.5 cm across the sinus, followed by two more if necessary, lateral and medial, respectively, to the first pair (Fig. 4F). The sinus is now cut with curved scissors (Fig. 4F). The medial sinus is closed with a running suture, and these hemostats are removed. Resection of the A VM The lateral hemostats are used to elevate the sinus and its AVM from the wound (Fig. 4G). With minimal retraction of the occipital lobe and superior cerebellum, the tentorium is exposed and incised bit by bit with curved scissors. The traction applied to the hemostats securing the cut edge of the lateral sinus places tension on the tentorium. Large feeding dural vessels are best controlled with small hemostatic clips. In this manner, the sinus is isolated from the dura overlying the cerebellum and occipital lobe and from the tentorium (Fig. 4G). This brings us to the epicenter of the AVM which invariably is located at the junction point between the lateral and sigmoid sinuses. The chief source of bleeding now seems to be the petrous bone itself from large feeding arteries contained in it. Some of these bleeding points can be arrested with the cutting current of the Bovie unit but others are best handled with Surgicel or Avitene packed firmly into the vascular channels. In spite of the major bleeding which continues to develop as the bone is removed, it is necessary to resect the margins of petrous bone adjacent to anterior surface of the proximal one-third of the sigmoid sinus in order to be certain that the arterial supply to the AVM has been 36 J. Neurosurg. / Volume 59 / July, 1983
6 AVM s of lateral and sigmoid dural sinuses interrupted. This is best accomplished using a diamond burr on the air drill (Fig. 4H). Earlier in our experience we attempted to resect the sigmoid sinus, but later we found this to be unnecessary if we opened it and securely occluded it by packing it tightly with Surgicel (Fig. 4I). This has the distinct advantage of leaving a cuff of dura which allows sufficient purchase for a tight homologous dural or fascia lata graft closure, a matter of some importance to avoid the possibility of CSF leaking through resected mastoid air cells (Fig. 4I). Vein of Labb~ Bridging veins that are red can be divided with relative impunity, as they are draining the AVM rather than the brain. Those that are black must be respected and this is particularly true of the vein of Labb6 which fortunately rarely interferes (see Discussion). Closure The dura is replaced with a homologous dural graft or a piece of fascia lata. The bone plate is wired to the skull with four or five wires. The scalp is closed with a single layer of vertical mattress sutures. Operative Results There were 22 excellent, one good, and two poor results in the group. The two poor results were in patients who did not recover useful vision, both having been legally blind from chronic papilledema prior to the surgery. Two patients died. One of these deaths was from a cardiac arrest related to blood loss in an infant 18 months of age. This was the only AVM which we considered congenital. The child had been operated on previously. The other death occurred in a patient with a high-flow AVM which was producing a progressive deficit and which had been operated on and embolized previously. The usual external carotid system supply was replaced with multiple dural vessels arising from the internal carotid and vertebral arteries. When the bone plate was elevated, a torrent of blood followed and the patient exsanguinated. Compression of the convexity dura was of no avail as the entire dura overlying the posterior aspect of the petrous bone was simply a pulsating arterial sinus. There have been no recurrences of symptoms other than transient bruits in two patients early in the series. The meaning of these was unclear, as both subsided with time. Two patients developed venous infarctions 1 to 2 days postoperatively. One of these was in an obese patient with a large bridging vein from the occipital pole that drained to the lateral sinus medial to the AVM. This vein was coagulated and divided at the time the sinus was ligated. It was not visualized on the angiogram. The other venous infarction resulted from occlusion of a vein of Labb6 and was predictable. In this case the vein could not be saved. The first of these patients ultimately achieved an excellent result with no visual field deficit. The other was classified as a poor result on the basis of a failure to regain useful vision, in turn the result of chronic papilledema. This was an elderly patient and the true impact of the venous infarction in the nondominant temporal lobe was difficult to ascertain. Both hemorrhagic infarcts were surgically evacuated; both were primarily hemorrhages with displacement of surrounding tissue. Symptomatology Discussion Although this has been reviewed previously, 3 and it was not the purpose of this paper to discuss the clinical presentation of these cases, a few brief comments are necessary for completeness. A bruit which is annoying to some patients and incapacitating to others is usually present. However, this is not invariable and some report no noise. Headaches are the next most common complaint. These are relatively nonspecific in character. They may be due to intracranial hypertension. Other symptoms of increased ICP are manifested by visual obscurations, dimness in vision, and blindness. Papilledema may be present on examination. Two primary causes for symptoms of increased ICP and the findings of papilledema should be considered. One is simply the impairment of venous run-off from associated major sinus occlusion and the other is from an increase in ICP as a result of high flow into the draining sinuses with an elevation in the intra-sinus pressure. Retrograde flow was a common finding in patients with AVM s of the lateral sinus. A retrospective analysis of the case material has revealed that, invariably, patients with papilledema either had associated sinus occlusions or an AVM of a magnitude sufficient to produce retrograde flow with or without an occluded sinus. Focal neurological symptoms have included classic transient ischemic attacks and seizures. Both have been attributed to increased venous pressure in the area of the AVM. Spontaneous subarachnoid hemorrhage (SAH) is uncommon in our experience. Pathogenesis and Pathophysiology Houser, et al., 3 have presented convincing evidence that these are acquired lesions evolving from organization and vascularization of a previously thrombosed sinus. According to this hypothesis, the sinus thrombosis is the primary event, be it spontaneous or traumatic. Subsequently the clot in the sinus undergoes organization and in the process develops a dural blood supply with the potential for communicating with the patent portion of the sinus. The gradual hypertrophy of these vessels ultimately results in a dural AVM. Sequential angiograms have documented the progression of a thrombosed sinus to a dural AMV and the concurrence of an occluded sinus and dural AVM in our experience is common. If this theory is correct, and we believe that it is, then surgery will ultimately be required in most cases, as the J. Neurosurg. / Volume 59 / July,
7 T. M. Sundt, Jr. and D. G. Piepgras AVM will continue to enlarge and progressively increase the intracranial venous pressure, producing the symptomatology discussed briefly above. Nevertheless, these are often elderly patients with other ailments, and a delay in surgery with a period of observation to follow the progression of the illness is acceptable. Insofar as SAH s are uncommon, they do not create emergency situations. When signs of increased ICP become present, surgical intervention is mandatory. Diagnostic Studies Computerized tomograms are usually normal. Angiograms clearly establish the diagnosis. Arterial Supply In primary (unoperated or untreated cases) AVM s, the arterial blood supply is derived from five general sources: 1) the occipital artery and its major branches; 2) a vascularized petrous bone; 3) meningeal arteries in the dura overlying the cerebellum; 4) branches of the middle meningeal artery in the dura of the temporal and occipital lobes; and 5) branches of the meningohypophyseal artery in the tentorium. The occipital artery is usually the dominant feeder. In recurrent cases, the occipital and more superficial dural arteries have been ligated and the blood supply has been driven deeper, much as it is in parenchymal AVM s that have had partial and inadequate resection. There seems to be a particular propensity for the dura overlying the posterior aspect of the petrous bone to become the primary zone of supply. This creates a very dangerous situation, as control of this bleeding is extraordinarily difficult. It may represent an indication for profound hypothermia. Venous Drainage and Bridging Veins These AVM s often drain primarily through the opposite lateral sinus if the sigmoid sinus is occluded (although sometimes both sigmoid sinuses are occluded). In other instances, the exact source of drainage is not clear from the angiogram and in these cases one should expect it to be via the diplo~ of the overlying bone. The secondary run-off can be comprised of various routes including the superior petrosal sinus, the epidural space and hence to the diplo6, and bridging veins. Thus, with removal of the bone plate and ligation of the medial portion of the lateral sinus, the venous drainage has in many instances been largely compromised. Although this increases bleeding from the AVM, it is unavoidable. In any case, by this point in the procedure, in unoperated (but not recurrent) cases of AVM the major blood supply has been interrupted. Prior to the operation it behooves the surgeon to examine in great detail the venous drainage of the temporal and occipital lobes. It is virtually impossible to preserve major perforating veins from the lateral occipital pole or posterior temporal lobe. Fortunately, however, the occlusion of the sigmoid sinus followed by the development of the AVM has interfered with the normal venous drainage, and major functional bridging veins are uncommon as the venous drainage has sought and found other avenues of escape. The reverse is, in fact, often the case with reversal of flow and the presence of red veins. These, as indicated previously, can be severed with impunity. The vein of Labb6 is a vessel of special importance. In aneurysm surgery it is a maxim that this vein should be preserved if at all possible. In dural AVM cases it is usually not prominent, perhaps because it never was large, explaining in part the low flow through the nondominant sinus (thought to be a major factor in cases of spontaneous occlusion of a lateral sinus). If it is prominent, it should be preserved if possible and allowed to drain into the superior petrosal sinus. Obviously, in this situation a radical resection of the sinus must be substituted with a less ambitious undertaking in which the dural supply and petrous bone are still resected, but in which a total resection of the sinus is replaced by a subtotal resection (see the legend to Fig. 4G). In these cases, the margin of the sinus serving the superior petrosal sinus is preserved, allowing a reversal of flow and thus drainage from the vein of Labb6 through the petrosal sinus. Technical Notes The notorious vascularity of these malformations leads one to consider the possibility of placing the patient in a sitting position. In our judgment this is ill advised. The sitting position for this operation is hazardous as the wide open venous channels in the diplo~ make a major air embolism almost a certainty. The second temptation is to attempt to piecemeal resection of the bone (in effect making a craniectomy) using rongeurs rather than to elevate the bone as a single plate. Not only does this result in a less satisfactory cosmetic result but, more importantly, the bleeding is greater as the exposure and isolation of the arterial inflow and venous run-off are more difficult to control. Embolization through the external carotid artery may be a definitive form of treatment in those cases with exclusively external carotid artery feeders. However, it may provide only a transient improvement and ultimately compound the problem for the reasons cited above. It should be undertaken cautiously and with the patients followed rather closely thereafter. In those cases in which the age of the patient or other medical ~onditions mitigate against excision of the lesion, embolization is a reasonable approach. Fine particulate emboli or perhaps even tissue adhesives are useful in these cases because it is necessary to occlude the finest distal branches of the lesion rather than simply to obstruct the major feeding arteries. Embolization may be a consideration in selected, extremely vascular lesions as a preoperative treatment in an attempt to reduce some of the blood supply immediately prior to the operation. 38 J. Neurosurg. / Volume 59 / July, 1983
8 AVM s of lateral and sigmoid dural sinuses Every attempt should be made to excise the malformation as completely as possible with the initial procedure. The five cases with recurrence were technically a great deal more difficult than the primary lesions, and the two deaths were in patients in this group. It is our experience that recurrent lesions are more difficult primarily because the primary blood supply to the malformations is no longer from the external carotid artery but rather from deep branches originating from the internal carotid artery. We have not found the operating microscope particularly helpful in this procedure because of the extraordinary vascularity of the lesions and the size of the operative field. However, magnification loupes have been most helpful. References 1. Aminoff M J: Vascular anomalies in the intracranial dura mater. Brain 96: , Handa J, Yoneda S, Handa H: Venous sinus occlusion with a dural arteriovenous malformation of the posterior fossa. Surg Nenrol 4: , Houser OW, Baker HL Jr, Rhoton AL Jr, et al: Intracranial dural arteriovenous malformations. Radiology 105: 55-64, Hugosson R, Bergstr6m K: Surgical treatment of dural arteriovenous malformation in the region of the sigmoid sinus. J Neurol Neurosurg Psychiatry 37:97-101, Kosnik EJ, Hunt WE, Miller CA: Dural arteriovenous malformations. J Neurosurg 40: , Ktihner A, Krastel A, Stoll W: Arteriovenous malformations of the transverse dural sinus. J Neurosurg 45: 12-19, Lamas E, Lobato RD, Esparza J, et al: Dural posterior fossa AVM producing raised sagittal sinus pressure. Case report. J Neurosurg 46: , Magidson MA, Weinberg PE: Spontaneous closure of a dural arteriovenous malformation. Surg Neurol 6: , Newton TH, Cronqvist S: Involvement of dural arteries in intracranial arteriovenous malformations. Radiology 93: , Nicola GC, Nizzoli V: Dural arteriovenous malformations of the posterior fossa. J Neurol Neurosurg Psychiatry 31: , Obrador S, Soto M, Silvela J: Clinical syndromes of arteriovenous malformations of the transverse-sigmoid sinus. J Neurol Neurosurg Psychiatry 38: , 1975 Manuscript received October 13, Accepted in final form January 18, This investigation was supported by Research Grant NS6663 from the National Institutes of Health, Public Health Service. Address reprint requests to: Thoralf M. Sundt, Jr., M.D., Cerebral Vascular Research, Alfred Building, Room 4-437, St. Mary s Hospital, Rochester, Minnesota J. Neurosurg. / Volume 59 ~July,
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