SU R G ICA L ANATOM Y AND TECH N IQ U E Direct Microsurgery of Dural Arteriovenous Malformation Type Carotid-Cavernous Sinus Fistulas: Indications, Technique, and Results J. D iaz Day, M .D ., Takanori Fukushima, M .D . Allegheny Neuroscience Institute, Allegheny University for the Health Sciences, Pittsburgh, Pennsylvania OBJECTIVE: There is a subgroup of patients with Barrow Type D carotid-cavernous sinus fistulas (CCFs) who have progressive neurological deficits despite endovascular attempts at obliteration. To effectively arrest the progres­ sion of neurological deficits, especially visual loss, these patients require direct operative intervention. We have used a direct approach to such lesions, which comprehensively occludes all fistulous connections of the C C F. METHODS: We present a series of nine patients with Type D CCFs for which attempts at endovascular embolization failed and that, because of persistent symptoms, required surgical intervention. These lesions characteristically had extensive multiple external carotid artery feeders, often bilateral, in addition to the internal carotid artery feeders. The operative approach used was a combined extra- and intradural full exposure of the cavernous sinus and its contents, with identification and direct obliteration of all arterial input and selective ablation of the venous outflow from the cavernous sinus. RESULTS: All nine patients experienced resolution of their symptoms, and complete ablation of the lesions, as demonstrated by postoperative angiography, was achieved. Transient diplopia and trigeminal hypesthesia was observed in all nine patients, which resolved by 6 months postoperatively. One patient suffered from a temporary hemiparesis and another from permanent hemiparesis. There were no deaths related to surgery in this series. CONCLUSIONS: Patients with Type D CC Fs who have persistent, progressive neurological deficits after failed endovascular attempts at obliteration may be treated by a direct surgical approach to ablate the fistulas. The pertinent anatomic concepts, indications for surgery, and operative techniques that are different from previously described methods are discussed. (Neurosurgery 4 1 :1 1 1 9-1126, 1997) Keywords: Anatomy, Carotid-Cavernous sinus fistula, Cerebrovascular, Surgery D ural arteriovenous m alform ation type carotid cavern ­ ous sinus fistulas (C CFs) fed by both internal and external carotid artery feeders (Type D according to Barrow [1]) are particularly challenging to successfully oblit­ erate. Endovascular m ethods are well established as the first line of therapy (4, 15) and are typically used in our practice. However, a subgroup has been identified that is com prised of lesions that are not successfully treated by endovascular tech­ niques alone and that require direct surgical obliteration jT 2, 15). Primarily, failure of an en dovascu lar approach to alt rapid and progressive visual loss has been our indication to Perf°rm a direct surgical attack as a m eans of preserving vision. Direct surgery of these lesions has been perform ed by sevgroups, all of whom used various m ethods of embolizing e flshilous connections (2, 6, 8 -1 3 ). The surgical strategy Ust'd f°r our patients differs from previous m ethods of direct surgery in that it directly exposes and obliterates all arterial and venous connections of the fistula, versus com pression and throm bosis, by packing foreign m aterial into the cavern ­ ous sinus. W e have determ ined this m ethod to be successful in com pletely obliterating the fistulous connections in the cavernous sinus and resulting in the resolution of sym ptom s. PATIENTS AND M ETHO DS Since 1985, we have treated nine patients with Barrow Type D (1) CCFs. The patients ranged in age from 11 to 71 years. There w ere 7 female and 2 male patients in the series. All patients presented with progressive visual loss that occurred during a period of weeks to several m onths as a com ponent of their sym ptom com plex. A diagnosis of Type D C C F was m ade using angiography in each case. Patients w ere evalu­ ated by ophthalm ological exam ination, w hich included acuity Neurosurgery , Vol. 41, No. 5, November 1997 1119 1120 Day and Fukushima and visual field testing. All nine patients w ere initially treated by endovascular m ethods using various types of embolic m aterials. Failure of endovascular therapy w as recognized in all nine patients, both angiographically and by persistence of visual com prom ise. The time interval betw een endovascular intervention and surgery varied from 12 hours to 1 week. All nine patients underw ent a combined intra- and extradu ral frontotem poral approach to the cavernous sinus for direct obliteration of the fistulous connections. The patient data are sum m arized in T a b le 1. Operative technique The general details of the surgical approach have been described previously (3, 5, 6). W e briefly describe the tech­ nique as applied in these cases. After satisfactory induction of general anesthesia, the head is placed in three-pin fixation and rotated ap proxim ately 45 degrees. A routine pterional type scalp incision is m ade. The tem poralis m uscle and fascia are incised and elevated with the scalp as a single layer flap. The m usculocutaneous flap is elevated to the m argin of the orbital rim and held anteriorly. A frontotem poral craniotom y is cut centered one-third above and tw o-thirds below the superior tem poral line. The dura is elevated aw ay from the frontal and tem poral cranial base, and the sphenoid ridge is then flattened using a high-speed drill. Com plete skeletonization of the cranial nerves in their respec­ tive canals is next perform ed. The optic canal is first unroofed, and then the anterior clinoid process is rem oved. The superior orbital fissure, foram en rotundum , and foram en ovale are next unroofed to skeletonize 5 to 8 m m of their contents. This extradural bone rem oval is critical to exposing several of the triangular entry spaces into the cavernous sinus. Arterial feed­ ers from the external carotid circulation are also exposed and occluded via this bone rem oval, both at the neural foram ina and traversing bone in between. The m iddle m eningeal artery is exposed at the foram en spinosum and divided. In som e cases, the posterolateral and posterom edial cavernous trian­ gles are opened via extradu ral rem oval of the petrous apex (5, 6). This dissection p rovides access to the posterior cavern­ ous sinus. The dura propria over the tem poral lobe is next separated from the outer cavern ou s m em brane. A s this layer is elevated, bleeding com es from small openings in the outer cavernous m em brane. These bleeding points are controlled by packing with small pieces of Surgicel. The dura p ropria is elevated to near the incisural edge and p etrous ridge. The anteromedial, anterolateral, and far lateral cavern ou s triangles are opened and packed with an ap propriate am ou n t of Surgicel. M edially, the dura is opened in an L-shaped incision that begins over the sylvian fissure and extends to the optic nerve sheath. The second limb of the incision is directed along the tuberculum sellae. The fibrous dural ring surrounding the carotid artery is next opened. The m edial, superior, and lat­ eral cavern ou s triangles are opened and packed with an ap­ propriate am ount of Surgicel. The p roced ure of sequential packing of the cavern ou s triangles results in complete oblit­ eration of the arterioven ou s fistula in the cavernous sinus. Illustrative C ase I A 6 0 -y e a r-o ld w o m a n p re se n te d w ith a 3 -m o n th h isto ry of wors­ e n in g ch e m o sis , a b d u c e n s p a ls y , a n d v is u a l lo ss in the left eye. Her v is u a l lo ss w a s c h a ra c te riz e d b y an e n la r g in g ce n tra l scotoma and w o rs e n in g a c u ity . T h e p a tie n t u n d e rw e n t a tra n s a rte ria l endovascular a p p ro a c h w ith e m b o liz a tio n of the e x te rn a l c a ro tid arterial feeding v e s se ls w ith p o ly v in y l a lc o h o l p a rtic le s . It w a s n o t p o ssib le to emboliz e the in te rn a l ca ro tid a rte ria l s u p p ly to the fis tu la (Fig. IA). There w a s no ch a n g e in the p a tie n t's s y m p to m s after e m b o liza tio n , and the p atie n t w a s tra n sfe rre d to M it s u i H o s p it a l in T o k y o for definitive th e ra p y. T h e p a tie n t u n d e rw e n t a fro n to te m p o ra l c ra n io to m y with intra­ d u r a l e x p o su re of the c a v e rn o u s s in u s . T h e s u p e rio r and lateral c a v e rn o u s tria n g le s w e re o p e n e d a n d the c a v e rn o u s sin u s packed w ith S u rg ic e l. T h e m e n in g o h y p o p h y s e a l tr u n k w a s exposed in the s u p e rio r tria n g le a n d lig a te d w ith a s m a ll a n e u r y s m d ip . Postopera­ tiv e a n g io g r a p h y d e m o n stra te d co m p le te o b lite ra tio n of the fistula (Fig. IB ). T h e p atie n t im p r o v e d p o s to p e ra tiv e ly , re g a in in g normal TABLE 1. Clinical Summary of Patients Undergoing Direct Microsurgical Embolization” Age (yr)/Sex 60/F 11/M 71/F 66/M 58/F 65/F 69/F 54/F 45/F Preoperative Symptoms Chemosis, visual loss Chemosis, orbital pain, visual loss Chemosis, visual loss Chemosis, visual loss Chemosis, visual loss Diplopia, chemosis, visual loss Chemosis, visual loss, diplopia Headache, diplopia, visual loss Headache, visual loss Persistent Deficits Endovascular Approach Embolic Agents Residual Feeders Tim e to Surgery' 2d 1 wk None None Arterial Arterial PVA PVA None Diplopia Hemiparesis None Arterial Arterial Arterial Arterial and venous PVA and gel foam PVA PVA GDC MHT MHT and vertebral arterial branches MHT MHT MHT MHT None Arterial and venous GDC MHT 2d None Arterial and venous GDC MHT 2d None Arterial and venous GDC and particles MHT 12 h a PVA, polyvinyl alcohol; G D C , Guglielmi detachable coils; M HT, meningohypophyseal trunk. Neurosurgery , Vol. 41, No. 5, N ovem ber 1997 2d 4d 1 wk 1d Microsurgery of Dural CC Fs 1121 FIG U R E 1. A, angiogram of the left ICA, obtained after embolization of external carotid arterial feeding vessels, demonstrating the persistent fistula (arrows), w hich is fed by the meningohypophyseal trunk. B, postoperative angiogram demonstrating occlusion of the fistula. An aneurysm clip (arrow) was placed across the meningohypophyseal trunk. vision. C h e m o sis a n d the a b d u c e n s p a ls y re s o lv e d d u r in g se v e ra l days (Fig. 2). Illustrative Case 2 A 45-year-old w o m a n p re se n te d w ith a h is to r y o f s e v e ra l m o n th s' duration of headache a n d g ra d u a l v is u a l lo ss in the left eye. She w a s examined b y a n e u ro lo g ist w h o re fe rre d h e r for o p h th a lm o lo g ic a l evaluation, in c lu d in g m a g n e tic re so n a n ce im a g in g a n d m a g n e tic re s­ onance a n gio graph y. T h e o p h th a lm o lo g ic a l e v a lu a tio n w a s s ig n if i­ cant for an en larg ed ce n tra l sco to m a a n d in t ra o c u la r p re ssu re of 26 mm Hg. The resu lts of the m a g n e tic re so n a n ce a n g io g r a p h y w ere FIG U R E 3. A, preoperative lateral angiogram of the patient in the first illustrative case, demonstrating persistent flow via the ICA circulation. The external carotid artery feeders were obliterated using an endovascular approach. B, angiogram, obtained on postoperative Day 3, demonstrating complete obliteration of fistulous flow. p re ssu re in the left eye w a s 19 m m H g a n d the p atie n t's v is io n w a s im p r o v e d . T h e in tra o c u la r p re s s u re in the left eye s u b s e q u e n tly d ro p p e d to 14 m m H g b y 1 m o n th after s u rg e ry , a n d the p atie n t's v is io n h a d re tu rn e d to n o rm a l. P o sto p e ra tiv e a n g io g r a p h y c o n firm e d the o c c lu sio n of the fis tu la on p o sto p e ra tiv e D a y 3 (Fig. 3B). T h e p atie n t su ffe re d a tra n sie n t p a rtia l left o cu lo m o to r n e rv e p a re sis, w h ic h re s o lv e d c o m p le te ly b y the 2 n d w e e k after s u rg e ry . A t f o llo w -u p 1 y e a r after s u rg e ry , the p atie n t h a d e x p e rie n ce d n o re c u r­ suspicious for a C C F . T h e p a tie n t w a s then refe rre d fo r a n g io g r a p h y and endovascular o b lite ra tio n . A n g io g r a p h y re v e a le d a T y p e D C C F with bilateral external ca ro tid c irc u la t io n fe e d in g ve sse ls in a d d itio n to feeding vessels fro m the m e n in g o h y p o p h y s e a l tru n k . rence of s y m p to m s. The patient u n d e rw e n t a c o m b in e d tra n s a rte ria l a n d tra n sv e n o u s endovascular p ro ce d u re w ith p la ce m e n t of G u g lie lm i d e ta ch a b le c o ils and polyvinyl alco h o l m ic ro s p h e re s, w h ic h s u c c e s s fu lly o c c lu d e d the C om plete resolution of the C C Fs w as achieved in all nine patients, as docum ented by postoperative angiography. N one of the patients have suffered a recurrence of the fistulas to date. The follow-up period ranges from 1 to 14 years. N o late follow-up angiogram s have been obtained because none of the patients have experienced a return of sym ptom s. There were no m ortalities in the series. Vision w as preserved at the preoperative level or im proved p ostoperatively in all patients. The m inim um goal of the p rocedure w as to halt the progression of the visual deficit, w hich w as realized in all patients. Three patients had diplopia as part of their presenting sym ptom com plex. All three exp e­ rienced reversal of their ocular m otor disturbance by 3 m onths after surgery. One patient suffered from a new abdu­ cens nerve deficit, presum ably secondary to com pression by overpacking in Parkinson's triangle. The rem aining five pa­ tients had tem porary diplopia postoperatively, all of which resolved by 3 months. Chem osis and headache w ere also relieved postoperatively. One patient suffered a perm anent hem iparesis postopera­ tively. This w as one of the initial patients treated in the series. Postoperative angiography demonstrated occlusion of the ICA; otherw ise, the C C F w as occluded. A second patient suffered tem porary contralateral hem iparesis, w hich resolved within 1 week. A slight narrow ing of the cavernous ICA w as de­ tected using postoperative angiography for this patient. Initial postoperative com puted tom ography dem onstrated mild ce­ rebral hem ispheric edem a. external carotid fe e d ing v e sse ls to the m a lfo rm a tio n s . H o w e v e r, sat­ isfactory e m b olization of the fis tu la s u p p ly fro m the in te rn a l ca ro tid artery (IC A ) w as not a ch ie v e d (Fig. 3A ). T h e next m o rn in g , 1 2 h o u rs after em bolization, the in t ra o c u la r p re s s u re in the left e ye w a s u n ­ changed (24 m m H g ) a n d the p a tie n t re p o rte d d e te rio ra tio n in h er vision. At that tim e, the d e c is io n w a s m a d e to p e rfo rm d ire c t s u rg ic a l obliteration of the fistu la in an atte m p t to p re s e rv e the p atie n t's vision. A left frontotem poral c ra n io to m y w a s p e rfo rm e d w ith e x tra d u ra l exposure of the ca v e rn o u s s in u s . T h e a n te ro la te ra l, la te ra l, s u p e rio r, ' and medial cave rn o u s tria n g le s w e re o p e n ed a n d e m b o liz e d w ith careful packing of S u rg ic e l, as d e s c rib e d a b o ve . P o sto p e ra tiv e ly , the patient recovered w e ll. O n the m o rn in g after s u rg e ry , the in tra o c u la r FIG U R E 2. A, photograph, obtained on postoperative Day 1, demonstrating severe chemosis of the left eye. B, photograph, obtained 3 months postoperatively, demonstrating resolution of chemosis. RESULTS N e u r o s u rg e r y , Vol. 4 /, No. 5, Novem ber 1997 1 12 2 Day and Fukushima Anterolateral triangle DISCUSSION Surgical anatomy The m icrosurgical anatom y of the cavernous sinus has been well described in recent publications (7). The pertinent details of the surgical anatom y of the cavernous sinus for treatm ent of CCFs are reliant on the features of the triangular entry corridors, which have been detailed elsew here (5, 6) and are illustrated in F ig u r e 4 . Crucial in dim inishing surgical com pli­ cations is an intimate working know ledge of these triangular entry corridors. The success of the proced ure relies on pack­ ing a sufficient am ount of oxidized cellulose (Surgicel) in the correct position within each triangular corridor. O verpacking in any one direction, in any particular corridor, can lead to carotid occlusion a n d /o r com pression of cranial nerves. Therefore, the following descriptions form the basis for su c­ cessful obliteration of Type D C C Fs using our approach. Anteromedial triangle The anterom edial triangle contains the subclinoidal seg­ ment of the carotid artery. This segm ent of the vessel fre­ quently is surrounded by an extension of the cavernous ve­ nous plexus and in cases of C C Fs m ust therefore be packed. The subclinoidal segm ent of the carotid artery is alm ost in­ variably exposed in these procedures as a m eans of exposing and controlling the distal carotid artery. Fleavy packing of oxidized cellulose in any direction has the potential to occlude the carotid artery. The anterolateral triangle is extrem ely im portant in cases of C CFs. The superior ophthalm ic vein typically communicates with the cavern ou s sinus via this area. Therefore, it is invari­ ably opened as a m eans of occluding this im portant venous connection. Packing tow ard the orbit m ay be performed with im punity. H ow ever, p osterior packing has the potential to occlude the carotid artery and m ay com p ress the sixth nene near its entrance to the superior orbital fissure. Far lateral triangle This space, bounded by V2 and V3, com m only contains the sphenoidal em issary vein in close relation to the foramen ovale. This vein com m un icates the cavern ou s sinus with the pterygoid venous plexus and m ay be substantial in cases of C CFs. As in the case of the anterolateral triangle, packing tow ard the base, occluding the vein, is perform ed with impu­ nity. H ow ever, p osterior packing has the potential to occlude the carotid artery as it enters the cavern ou s sinus space via the foram en lacerum . Medial triangle Packing the m edial triangle in the lateral and anterior di­ rections carries risk to the Illrd cranial nerve and the ascend­ ing portion of the cavern ou s carotid artery. The posterior and inferior directions lead to the cavernous sinus communications with the basilar venous plexus of the clivus and the inferior petrosal sinus. Therefore, a large am ount of embolic material may be directed in this direction without consequence. Superior triangle This space p rovides the route to the m ost typical origin site of the m eningohypophyseal trunk. O cclusion of this vessel m ay be achieved via this space. Packing of embolic material m ay be perform ed in the p osterior and m edial directions, w hich augm ents occlusion of the basilar venous plexus and inferior petrosal sinus via the larger m edial triangle. Packing anteriorly and laterally will risk occlusion of the cavernous carotid artery and m ay result in com pression of the Vlth cranial nerve. Lateral triangle FIG U RE 4. Illustration of the critical anatomic triangular entry corridors to the cavernous sinus used in direct oblitera­ tion of CCFs. T, anteromedial triangle; 2, medial triangle; 3 , superior triangle; 4, lateral triangle; 5, posterolateral trian­ gle; 6, posteromedial triangle; 7, anterolateral triangle; 8, far lateral triangle; AE, arcuate eminence; G G , geniculate ganglion; mma, middle meningeal artery; PC, posterior cli­ noid process; SOF, superior orbital fissure; ttm, tensor tym­ pani muscle; III, oculomotor nerve; IV, trochlear nerve; V, trigeminal nerve; VI, abducens nerve; n., nerve; a., artery; Ant., anterior; Post, comm., posterior communicating; Sup., superior. Parkinson's triangle is relatively hazard ous in terms of generous placem ent of em bolic m aterial. Packing in the lateral and anterior directions poses a high risk to the sixth n e rv e , VI and the carotid artery. Posteriorly directed packing also risks com pression of the sixth nerve. The m edial direction is gen­ erally safe as a m eans of occluding the communication to the inferior petrosal sinus. Posterolateral triangle Known as G lasscock's triangle, this space houses the hori­ zontal intrapetrous carotid artery. This triangle may need to be opened for proxim al control of the intracavernous carotid artery and to occlude fistulous connections through bone to Neurosurgery, Vol. 41, No. 5, Novem ber 1997 Microsurgery of Dural C C Fs the pterygoid venous plexus. C are m ust be taken during packing to preserve paten cy of the carotid artery. Posteromedial triangle This triangle roughly describes the p etrous apex and is known as Kawase's triangle. R em oving the bone in this area provides access to the posterior cavern ou s sinus region. This may be important in occluding fistulous connections to the superior petrosal sinus, inferior petrosal sinus, and petrosal veins. In principle, all of the cavern ou s triangles are opened and packed in these cases. These Type D C C Fs are diffuse lesions; therefore, they generally require full exp osure for successful obliteration. How ever, the surgical ap proach m ay be tailored in individual cases, based on the results of postem bolization angiography. For exam ple, if after em bolization the sole re­ maining feeding vessel is the m eningohypophyseal trunk, selective opening of the superior or lateral triangle with liga­ tion of the vessel m ay suffice. This w as the situation in our first illustrative case. Clinical considerations The contemporary first-line th erap y for any type of C C F that is symptomatic is an en dovascu lar ap proach to embolize the fistula. Patients w ho present with rapid visual loss con ­ stitute urgent cases requiring im m ediate therapy to save vi­ sion. Clearly, it is the rare patient w ho does not respond to endovascular obliteration of the C C F (1, 4, 15). The initial five patients in this series w ere treated before the advent of trans­ venous approaches and G uglielm i detachable coils. The last four patients were treated using a com bination of transarterial and transvenous approaches. Despite these contem porary techniques, these patients failed to respond to therapy. Those patients who fail en dovascular p roced ures and continue to suffer visual loss and diplopia are candidates for a direct obliteration procedure. The optim al tim ing of surgery after a supposedly failed en dovascular p roced ure is uncertain. In this series of patients, the interval varied from 12 hours to 1 week. This variance w as secon dary to several factors. Some patients were treated en dovascularly outside the authors' in­ stitution and were transferred to us after failing to realize any lrnprovement. Patients w ho w ere operated m ore p roxim ate to the endovascular procedure had intervention because of per­ sistence of the fistula on an giogram s, the continued severity of svmptoms, and the presum ed im m inent threat to their vision. The selection of the surgical ap proach should optim ally en­ sure patency of the carotid artery while resulting in com plete fistula occlusion. Other techniques have been used and presented. In 1965, Parkinson (11) reported direct surgical obliteration of a C C F under conditions of hypotherm ic card iac arrest. His surgical Tproach aimed to directly interrupt the fistulous connections ln the cavernous sinus (1 1 ,1 2 ). A lthough successful in cases of YPe A CCFs, the com plexity of Type D fistulas does not lend 'P'Of to this limited approach through the lateral triangle. itionally, advances in surgical technique have now obviated the necessity for hypotherm ic card iac arrest in such 1123 cases. Mullan (10) is also recognized for his pioneering work on this com plicated problem via direct venous occlusion of the cavernous sinus via the anterolateral triangle and other routes. The early series of 33 patients presented by Mullan (10) produced uniform ly excellent results, with no case of carotid occlusion. A s in our series, cranial nerve deficits w ere uniform ly im proved postoperatively. The m ethod presented by M ullan (10) is essentially incorporated into a m ore com ­ prehensive approach to surgical obliteration with our m ethod. Isam at et al. (9) published a som ew hat sim ilar technique with m uscle packing through a transdural approach used in four patients with high-flow, Type A C CFs. Although the results reported w ere good, this is an im precise technique that does not guarantee carotid patency nor accu rate obliteration of all venous spaces in the cavernous sinus. Such techniques rely on a sophisticated sensitivity to packing pressure and volum e by an experienced surgeon to prevent overpacking and carotid com prom ise. Complication avoidance The dom inant concept that requires study and com prehen­ sion is the triangular entry corridor organization of cavern ­ ous sinus anatom y. A voiding com pression of the intra­ cavernous carotid artery, the abducens nerve, and the nerves within the lateral wall relies on an intim ate know ledge of this anatom ic organization. A sense of how m uch em bolic m ate­ rial can be placed in any particular direction is crucial. This is a "subjective" m atter of packing pressure, w hich has been com m ented on by M ullan (10). One patient early in our series suffered from perm anent hem iparesis, w hich w as secondary to occlusion of the carotid artery from overpacking, as ob­ served on the postoperative angiogram . A second patient suffered transient contralateral hem iparesis postoperatively, w hich resolved within several days. Postoperative com puted tom ographic scans showed som e elem ent of cerebral hem i­ spheric edem a, possibly as a result of retraction. This patient m ay have also had som e elem ent of vasospasm from m anip­ ulation of the carotid artery, w hich m ay have caused this problem. The m ethod presented by M ullan (10) of trans­ venous obliteration of C CFs sim ilarly relies on this technical point for success w ithout com plication from overpacking. The pathological m echanism of visual loss involves venous hypertension leading to raised intraocular pressures. High intraocular pressure results in a partial ischem ic deficit (14). This m echanism requires that intraoperatively, the patient's blood pressure is kept at least at a norm otensive level. Intra­ operative hypotension m ay lead to retinal hypoperfusion be­ cause of an inability to overcom e high intraocular pressures from venous obstruction. Therefore, w e m aintain adequate perfusion pressures to prevent further ischem ic retinal d am ­ age during the procedure. Because of the com prehensive nature of our surgical ap ­ proach, m ost elem ents of the cavernous sinus region are ex­ posed and m anipulated. This results in at least tem porary dysfunction of the affected nerves. In our series of nine pa­ tients, all had tem porary diplopia, which resolved at varying times within 3 months postoperatively. This raises the im por­ N e u r o s u rg e r y , Vol. 4 /, No. 5, Novem ber 1997 1124 Day and Fukushima tant point of tailoring the surgical approach for each specific case. The necessary elem ents of the surgical approach are determ ined by careful review of the postem bolization angio­ gram s. These films are critical to specifically exposing and embolizing the areas that were not treated by the en dovascu ­ lar approach. It is unnecessary and introduces added ele­ ments of risk to expose and pack segm ents of the anatom y that are already treated. 10. M u lla n S: T re a tm e n t o f c a r o tid -c a v e rn o u s fis tu la s b y cavernous s in u s o c c lu sio n . J Neurosurg 5 0 :1 3 1 -1 4 4 , 19 79 . 1 1 . P a r k in s o n D : A s u rg ic a l a p p ro a c h to the c a v e rn o u s portion of the ca ro tid a rte ry : A n a to m ic a l s tu d ie s a n d case rep ort. J Neurosurg 2 3 :4 7 4 -4 8 3 , 1965. 12 P a r k in s o n D , D o w n s A R , W h y te h e a d L L , S y s la k W B: Carotid c a v e rn o u s fis tu la : D ire c t r e p a ir w ith p re s e rv a tio n of carotid. Sur­ g e ry 76 :8 8 2-8 8 9 , 1974. 13 P e d ro A , P o la in a M , T r u jillo F , R o m e ro J: D ire c t carotid sinus a p p ro a c h to tre atm e n t o f b ila te r a l c a ro tid -c a v e rn o u s fistulas J Neurosurg 6 9 :9 4 2-9 4 4 , 1988. CO N CLU SIO N S 14 . S a n d e rs M D , H o y t W F : H y p o x ic o c u la r seq uelae of carotid- W e have treated nine patients with Type D C C Fs via direct surgical obliteration of the fistula after en dovascular attem pts at treatm ent failed. This is a highly select group of patients who required a direct surgical approach. The m ainstay of current therapy for C CFs of all types is en dovascular em bo­ lization. H ow ever, som e patients continue to have sym ptom s after endovascular therapy. W hen the patient's vision is threatened, a direct surgical proced ure to occlude the fistula is indicated. Our m ethod results in com plete obliteration of the venous connections of the cavernous sinus, as well as any rem aining arterial input to the fistula. Reliable use of this technique depends on the surgeon's having an intim ate w ork­ ing knowledge of the triangular entry corridors into the cav ­ ernous sinus. With proper application, it has a high rate of success in obliterating CCFs with a m inim um of m orbidity. Received, D e ce m b e r 18 , 1996. Accepted, June 18, 1997. Reprint requests: J. D ia z D a y , M .D ., L a h e y H itc h c o c k M e d ic a l C e n te r, D e p a rtm e n t of N e u ro s u rg e ry , 41 M a ll R o a d , B u r lin g to n , M A 01805. REFERENCES 1. B a rro w D L , Sp e cto r R H , B ra u n IF , L a n d m a n J A , T in d a ll S C , T in d a ll G T : C la s s if ic a t io n a n d treatm en t of s p o n ta n e o u s c a ro tid ca v e rn o u s s in u s fis tu la s. J Neurosurg 6 2 :2 4 8 -2 5 6 , 1985. 2. B la c k P, U e m a tsu S, P e ro v ic M , W a lk e r E A : C a r o t id -C a v e r n o u s fistu la : A co n tro lle d e m b o lu s te ch n iq u e for o c c lu sio n of fistu la w ith p re se rv a tio n of ca ro tid b lo o d flo w : T e c h n ic a l note. J N euro­ surg 3 8 :1 1 3 - 1 1 8 , 19 73. 3. D a y JD , G ia n n o tta S L , F u k u s h im a T : E x t ra d u r a l te m p o ro p o la r ap p ro a ch to le sio n s of the in fra c h ia s m a t ic a n d u p p e r c liv a l re ­ g io n s. J Neurosurg 8 1:2 3 0 -2 3 5 , 1994. 4. D e b ru n G , L a c o u r P, V in u e la F, Fox A , D r a k e C G , C a r o n JP: Tre atm e n t of 54 tra u m a tic c a ro tid -c a v e rn o u s fistu la s. J Neurosurg 5 5 :6 78 -6 9 2, 19 8 1. 5. F u k u s h im a T , D a y JD : O p e ra tiv e m a n a g e m e n t of c a v e rn o u s s in u s n e o p la sm s, in S c h m id e k H , Sw eet W (eds): Operative Neurosurgical Techniques. P h ila d e lp h ia , W .B . S au n d e rs C o ., 1995, ed 3, p p 4 9 3 -5 10 . 6. F u k u s h im a T , D a y JD , T u n g H : In tra c a v e rn o u s ca ro tid a rte ry a n e u ry s m s , in A p u z z o M L J (ed): Brain Surgery: Complication Avoidance and Management. C h u r c h ill L iv in g s to n e , N e w Y o r k , 1993, p p 9 25 -9 4 4 . 7. H a r r is F S , R h o to n A L Jr: A n a to m y of the ca v e rn o u s s in u s : A m ic ro s u rg ic a l s tu d y . J Neurosurg 4 5 :16 9 -18 0 , 1976. 8 . H o s o b u c h i Y : E le ctro th ro m b o sis of c a ro tid -c a v e rn o u s fistu la . J Neurosurg 4 2 :7 6 -8 5 , 19 75. 9. Isa m a t F , F e rre r E , T w o se J: D ire c t in tra c a v e rn o u s o b lite ra tio n of h ig h -flo w c a ro tid -c a v e rn o u s fis tu la s. J Neurosurg 6 5 :7 7 0 -7 7 5 , 1986. c a v e rn o u s fis tu la : S t u d y of the ca u se s o f v is u a l fa ilu re before and after n e u ro s u r g ic a l tre atm e n t in a s e rie s o f 25 cases. Br J Oph­ thalmol 5 3 :8 2 -9 7 , 1969. 15 . V in u e la F, Fo x A J, D e b ru n G M , P e e rle ss SJ, D r a k e C G : Spontane­ o u s c a r o tid -c a v e rn o u s fis tu la s : C lin ic a l, ra d io lo g ic a l, and thera­ p e u tic c o n s id e ra tio n s . J N eurosurg 6 0 :9 76 -9 8 4 , 1984. CO M M ENTS The authors rep ort the results of direct surgical treatment for nine patients with T ype D carotid -cavern ou s sinus fistulas (CCFs). A ttem pts at en dovascu lar em bolization failed in these patients. Surgery w as accom plished using the "triangular en­ try co rrid o rs" to the cavern ou s sinus, selectively packing those areas of the cavern ou s sinus involved in the fistula. E ndovascular therapy failed in all patients in the study, and the authors rep ort that Type D C C Fs are challenging to suc­ cessfully obliterate using the en dovascu lar approach. This is true for transarterial ap proaches. H ow ever, since 1985 (the time fram e of this stu d y), m icrogu id ew ires and microcatheter ad vances have m ad e the transven ou s endovascular approach the treatm ent of choice for T ype D C C Fs (1). These cases for which treatm ent by a com bination of transarterial and trans­ venous em bolization failed are difficult to manage, and these patients m ay be candidates for further endovascular treat­ m ent options. For exam ple, in the illustrative case, a woman with deterioration in her vision 12 hours after incomplete em bolization of a C C F w as taken to su rgery because of visual loss. The an giogram , how ever, show s no drainage into the superior ophthalm ic vein (SOV) but instead potential pial venous drainage through the posterior asp ect of the fistula A transvenous ap proach to the fistula w ould likely have been successful. H ow ever, it is well know n that visual deteriora­ tion m ay occu r for a period of time despite effective obliter­ ation of the fistula. The indications for su rgery w ere persistent or progressive neurological deficit related to the C C F, including "rapid and progressive visual loss." As p art of the natural history, pa­ tients frequently experience w orsening of vision and visual acuity as a fistula throm boses (3). The w orsening is usual!' caused by petrosal vein throm bosis that causes re d ire c tio n ot flow to, or throm bosis of, the SOV. The cavernous sinu' sinusoids m ay throm bose, becom e less com pliant, and acutd) increase pressure in the orbit. H ow ever, continued th ro m b ’ sis usually leads to fistula throm bosis before severe visual lobecom es perm anent. A nticoagulation m ay improve some ot the acute vision deterioration. In our experience, there is111 evidence that surgery preserves vision and that failure Neurosurgery, Vol. 41, No. 5, N ovem ber 1997 Microsurgery of Dural CCFs perform surgery would have led to vision loss. Therefore, the indications of direct su rgery are infrequent. A possible indi­ cation for the illustrative case w ould be persistent C C F with pial venous drainage. Of the nine patients treated using direct su rgery, one (11%) patient had a p erm an en t isch em ic co m p licatio n and one (11%) had a transient ischem ic com plication. The perm anent morbidity in an early case m ay have been treated before fully understanding the volum es required for packing. In our ex­ perience, the CCF can be packed via triangular corridors and then unpacked to avoid excessive com pression of the intra­ cavernous internal carotid artery (ICA ) or the cranial nerves ! (3). However, current en dovascu lar techniques have recently invalidated the need for direct surgical treatm ent for Type D direct CCFs. It is clear from the au th ors' detailed discussion of their surgical experience with the "trian gu lar co rrid o r" anatom y that they have a superb know ledge and understanding of the spatial relationship of the cavern ou s sinus and its relationship to the intracavernous ICA and the an astom otic netw ork of dural arteries. This anatom ic expertise has led them to ad­ vance the pioneering m ethod ology for C C F obliteration pre­ sented by Mullan (2). The authors docum ent an anatom ic understanding of the direct surgical treatm ent of dural C CFs, and the detailed m ethodology will be appreciated by neuro­ surgeons who treat this problem . Their sophisticated tech­ nique relies on precise angiographic identification of arterial feeders to the CCF for selection of the ap propriate triangular [• corridors to be packed in a stepw ise fashion to obliterate the t CCF without com prom ising in tracavern ous ICA flow or the cranial nerves of the lateral wall. Joh n M. Tew , Jr. it 8 8 C in c in n a t i, O h io ----------------1 Halbach V V , D o w d C R , H ig a s h id a R T , H e is h e im a G B : T r a n s ­ venous coil treatm ent of C C F , in T o m s ic k T A (ed): Carotid Cav­ ernous Fistulas. C in c in n a t i, D ig it a l E d u c a tio n P u b lis h in g , Inc., 1997, p p 1 6 3 -1 7 5 . 2. Mullan S: Tre atm e n t of c a r o tid -c a v e rn o u s fis tu la s b y c a v e rn o u s sinus occlusion. J Neurosurg 5 0 :1 3 1 -1 4 4 , 1979. 3. Tomsick T A : T y p e s B, C , a n d D ( D u r a l) C C F : E tio lo g y , p re v a ­ lence, and n a tu ra l h is to ry , in T o m s ic k T A (ed): Carotid Cavernous Fistulas. C in c in n a ti, D ig it a l E d u c a tio n P u b lis h in g , In c., 19 97, p p 5 9 -7 3 . Day and Fukushima describe a d irect m icrosurgical ap ­ proach for a complex subgroup of C C Fs supplied by both ■nternal and external carotid artery feeders (Barrow Type D CCFs). They appropriately state that en dovascu lar techniques ave become the m ainstay of treatm ent for C C Fs, but there 1rt s'tuations in which en dovascu lar approaches are inade­ quate. The authors present nine cases of Type D CCFs for u hich endovascular therapy had failed and that w ere subse­ quently treated using m icrosu rgery to achieve direct obliterf ahon. Their indications for direct m icrosu rgery w ere clear and PPropriate. Candidates for open su rgery w ere patients who, n Ihe surgeon's opinion, had continued rapid progressive 1125 visual loss despite attem pts at treatm ent with available en do­ vascular techniques. The authors include an ap propriate dis­ cussion of the m icrosurgical anatom y relevant to the ap ­ proach. Results of their interventions are concisely discussed and sum m arized in table format. It is interesting to note that all nine of their endovascular failures w ere at least partially secondary to inadequate occlu­ sion of the m eningohypophyseal trunk (M HT) feeders. Endo­ vascular therapy failed in four of these cases despite the use of transvenous approaches. C atheterization of the M HT from the ICA is often difficult because of its size, and a transvenous approach with endovascular packing of the cavernous sinus is frequently required. If the standard transvenous approach via the inferior petrosal or other sinus fails, one should consider an SOV approach via an orbital lid cu tdow n (2). In our expe­ rience, this approach can be successful even w hen other en­ dovascular procedures fail. The SOV approach is possible w hen the SOV is an enlarged prom inent draining vein from the C CF. If this also fails or is not possible, the m icrosurgical approach is indicated. Direct ligation of the M HT feeder with an aneurysm clip or suture is possible through the superior triangle, as described in the authors' first illustrative case. In the few cases for which all en dovascular approaches fail to obliterate the M HT feeders, this direct ligation m ay be the only m ethod available to obliterate the CCFs. M ost of the unique risks of this m icrosurgical approach are related to the difficulty of packing the cavernous sinus trian­ gles to an optim al pressure that occludes the fistula while only m inim ally disturbing the ICA and cranial nerves. The authors state that such techniques rely on a "sophisticated sensitivity to packing pressure and volum e by an experienced surgeon," and they discuss the "subjective" nature of this crucial step to prevent overpacking. H ow ever, even with the excellent tech­ nical skills of these authors and their com bined surgical ex­ perience with this type of lesion, they still encountered a 22% (2 of 9 patients) incidence of com plications directly attribut­ able to overpacking the triangles, with subsequent ICA com ­ prom ise. H ow ever, if they perform ed significantly less pack­ ing, there could have been persistence of the C C F and failure of treatm ent. There are several com bination approaches available that could eliminate or reduce the risk of ICA com prom ise from overpacking during this m icrosurgical procedure. End ovas­ cular tem porary balloon test occlusion with hypotensive chal­ lenge during the initial transarterial procedure is a simple m aneuver that m ight have prevented the tw o cases of hem i­ paresis secondary to ICA com prom ise (3). This test could ascertain which patients m ight not tolerate aggressive triangle packing before the open surgical procedure, perhaps indicat­ ing that increased precautionary m easures are needed. Intraoperative angiography is another simple procedure that can be used during the open m icrosurgical obliteration of a com plex CCF. If a catheter rem ains in the carotid artery intraoperatively, each stage of packing can be evaluated with the "gold standard" to ensure patency of the ICA and oblit­ eration of the fistula. This information w ould obviously be invaluable in preventing com plications secondary to ICA o c­ clusion or narrow ing, such as the authors experienced. Also, Neurosurgery, Vol. 41, No. 5, Novem ber 1997