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Review Endovascular Approaches to the Cavernous in the Setting of Dural

Justin Dye 1,*, Gary Duckwiler 2, Nestor Gonzalez 3, Naoki Kaneko 2, Robert Goldberg 4, Daniel Rootman 4, Reza Jahan 2, Satoshi Tateshima 2 and Viktor Szeder 2 1 Department of Neurosurgery, Loma Linda University, Loma Linda, CA 92354, USA 2 Division of Interventional Neuroradiology, Department of Radiological Sciences, David Geffen School of Medicine, University of California, Los Angeles, CA 90095, USA; [email protected] (G.D.); [email protected] (N.K.); [email protected] (R.J.); [email protected] (S.T.); [email protected] (V.S.) 3 Department of Neurosurgery, Cedars-Sinai Medical Center, Los Angeles, CA 90048, USA; [email protected] 4 Department of Ophthalmology, David Geffen School of Medicine, University of California, Los Angeles, CA 90095, USA; [email protected] (R.G.); [email protected] (D.R.) * Correspondence: [email protected]; Tel.: +1-909-558-6338

 Received: 16 July 2020; Accepted: 12 August 2020; Published: 14 August 2020 

Abstract: Dural arteriovenous fistulas involving the can lead to orbital pain, vision loss and, in the setting of associated cortical venous reflux, intracranial hemorrhage. The treatment of dural arteriovenous fistulas has primarily become the role of the endovascular surgeon. The venous anatomy surrounding the cavernous sinus and venous sinus that is often associated with these fistulas contributes to the complexity of these interventions. The current report gives a detailed description of the alternate endovascular routes to the cavernous sinus based on a single center’s experience as well as a literature review supporting each approach. A comprehensive understanding of the anatomy and approaches to the cavernous sinus available to the endovascular surgeon is vital to the successful treatment of this condition.

Keywords: cavernous sinus; carotid-cavernous fistula; neuroendovascular techniques

1. Introduction The cavernous sinuses (CS) are dural venous channels located on either side of the body of the . The CS has four walls, three of which consist of two layers of dura (outer meningeal and inner periostic). The medial wall, the only with a single layer of dura, makes up the lateral limit of the sella. The lateral wall contains (CN) III, IV, and V and lies just medial to the temporal pole. The superior wall, or roof of the CS, stretches from the diaphragma sellae medially to the anterior clinoid process laterally. The posterior wall contributes to the dura of the clivus [1]. The cavernous segment of the internal carotid (ICA) runs within the CS with CN VI running along its inferior and lateral border. The major tributaries to the CS are the superior ophthalmic (SOV), , superficial middle cerebral vein (SMCV), sphenoparietal (sphenobasal) sinus, and the contralateral sinus through the intercavernous (circular) sinus. The major egress of the CS includes the (SPS), (IPS), emissary to the , clival plexus to the posterior fossa and paraspinal , and the contralateral sinus through the intercavernous sinus. In 1985, Barrow et al. classified carotid cavernous fistulas (CCF) into direct (Type A) or indirect (Type B, C, or D) fistulas [2]. A direct CCF, commonly caused by trauma, is a direct connection between

Brain Sci. 2020, 10, 554; doi:10.3390/brainsci10080554 www.mdpi.com/journal/brainsci Brain Sci. 2020, 10, 554 2 of 16 the cavernous segment of the ICA and the CS. Indirect carotid cavernous fistulas (dural CCF) are a type of dural arteriovenous fistula (DAVF) that occurs when an abnormal connection forms between the CS and meningeal branches of the external carotid artery (ECA), meningeal branches of the (ICA), or the ICA itself. The presentation, work up, and management options for CCFs are well published [3–5]. Indications for treatment include progressively worsening symptoms, vision loss, and/or cortical venous reflux (CVR). For DAVFs in general, the goal of treatment is to block the fistulous connection. Many times, direct CCFs can be treated through a transarterial approach with access to the CS across the tear in the cavernous segment of the carotid artery [3,6]. The fistula can then be obliterated with a balloon or stent protecting the cavernous ICA. Secondary to multiple small arterial feeders, which may supply cranial nerves, dural CCFs are often treated with a transvenous approach to the CS followed by coil or liquid embolic embolization of the CS itself. [3,4,7]. Complex venous anatomy and sinus thrombosis, often associated with dural CCFs, make a detailed knowledge of CS anatomy essential for safe and effective endovascular treatment. The current report focuses on dural CCFs and the multiple transvenous routes to the CS available to the endovascular surgeon.

2. Inferior Petrosal Sinus Via the Internal The inferior petrosal sinus is a common route to the CS in the setting of dural CCFs [3,4,7,8]. The IPS originates in the posterior/inferior aspect of the CS. It travels posterolaterally within the inferior petrosal sulcus and passes through the anterior portion of the . The IPS then terminates in the anteromedial aspect of the jugular bulb. The junction of the IPS with the IJV has variable anatomy and was classified into four types by Shiu et al. in 1968 [9]. In their description, type I anatomy is a single IPS with a small caliber or no connection to the vertebral venous plexus (VVP). Type II anatomy is a single IPS with a large caliber connection to the VVP. In type III anatomy, a network of small veins make up the IPS and form the connection with the IJV. In type IV anatomy, there is no connection between the IPS and the IJV. More recently, Miller et al. classified the venous anatomy of 135 patients undergoing bilateral inferior petrosal sinus sampling (IPSS) [10]. The authors found true type IV anatomy in only 1% of patients and were successful in bilateral IPSS in 99% of patients. For the IPS approach via the IJV, the authors of the current article prefer to place a 5 Fr sheath in the left common femoral artery (CFA) and a 5 Fr catheter in the common carotid artery (CCA), to be used for diagnostic angiograms and roadmaps. A 6 Fr 23 cm sheath is then placed in the right common femoral vein (CFV), for operator comfort, and a 6 Fr guide catheter is navigated into the (IJV). Next, using roadmapping technique a curved microwire directed anteriorly and medially is used to select the IPS. The IPS is then navigated superiorly and medially until the tip of the microcatheter is advanced into the posterior CS. An intermediate catheter, such as a Distal Access Catheter (DAC) (Stryker Neurovascular, Fremont, CA, USA), can be used for extra support if necessary. In the case of a thrombosed IPS, access to the CS is still possible by “drilling” through the thrombus with a microsystem. A microwire is navigated in the direction of the expected IPS anatomy. A torque device is used to twist the wire repeatedly as gentle forward pressure is applied. The microcatheter is intermittently advanced to provide enough support for the wire to continue along its path. It is also possible to direct the wire into the clival venous plexus, which runs parallel to the IPS, and still reach the CS through this alternate pathway. The microwire drilling technique should be used with caution as perforation into the subarachnoid space can result in intracranial hemorrhage. Secondary to this risk, the authors recommend avoiding stiff microsystems during this approach (usually nothing stiffer than a 014” standard microwire). In general, the authors most commonly use a standard 0.010” or 0.014” microwire with a compatible microcatheter. A softer, more torqueable microwire is usually chosen first, followed by stiffer wires as needed. Microwires larger than 0.014” are rarely necessary. In longer approaches, such as with the middle temporal vein or to the SOV, a longer and softer microcatheter is selected such as Brain Sci. 2020,, 10,, 554x FOR PEER REVIEW 33 of of 16 selected such as the MicroVention Headway Duo 167 cm (Aliso Viejo, CA, USA) or the Medtronic theMarathon MicroVention 165 cm Headway(Irvine, CA, Duo USA). 167 cm When (Aliso torq Viejo,ueability CA, USA)and support or the Medtronic are needed Marathon in these 165longer cm (Irvine,approaches, CA, USA).usually When a 0.010 torqueability wire is used. and When support the areanatomy needed is inparticularly these longer tortuous approaches, a softer usually wire is a 0.010usually wire chosen is used. such When as thethe anatomy Medtronic is particularly Mirage 0.008” tortuous (Irvine, a softer CA, wire USA) is usually or the chosen Balt suchHybrid as the0.007”/0.012” Medtronic (Irvine, Mirage CA, 0.008” USA). (Irvine, CA, USA) or the Balt Hybrid 0.007”/0.012” (Irvine, CA, USA). When itit isis presentpresent and and patent, patent, the the IPS IPS provides provides a direct a direct route route to the to CS.the However,CS. However, when when this route this isroute not is available, not available, alternatives alternatives do exist. do exist.

3. Via thethe AngularAngular VeinVein Another common common route route to to the the CS CS is through is through the theSOV, SOV, which which is often is oftendilated dilated in dural in CCFs. dural CCFs.Transfemoral Transfemoral access to access the SOV to the can SOV be canachieved be achieved by catheterization by catheterization of the angular of the angular vein, which vein, whichcommunicates communicates with the with SOV the via SOV the via nasofrontal the nasofrontal vein. The vein. frontal The frontal and supraorbital and supraorbital veins veinsjoin to join form to formthe angular the angular vein which vein which runs runsinferiorly inferiorly in an in oblique an oblique fashion, fashion, lateral lateral to the to theroot root of the of the nose, nose, down down to tothe the inferior inferior margin margin of ofthe the orbit orbit where where it itcontinues continues as as the the anterior anterior facial . vein. The The anterior anterior facial facial vein runs deepdeep toto thethe facialfacial artery,artery, superficial superficial to to the the masseter masseter muscle muscle and and joins joins the the retromandibular vein to formto form the the common common facial facial vein, vein, which which drains drains directly directly into the into IJV. the The IJV. common The facial can vein be selected can be withselected the with curved the tip curved of a micro- tip of or a guidewiremicro- or directedguidewire anteriorly directed at anteriorly approximately at approximately the midcervical the segmentmidcervical of thesegment IJV (near of the angleIJV (near of the the ) angle of (Figurethe mandible)1). In some (Figure cases, 1). the In retromandibular some cases, the veinretromandibular can be selected vein from can thebe selected external from jugular the vein extern (EJV).al jugular The angular vein (EJV). vein The is then angular navigated vein is with then a microsystemnavigated with and a roadmappingmicrosystem techniqueand roadmapping as it courses technique superiorly as it and courses medially. superiorly The nasofrontal and medially. vein, whichThe nasofrontal lies near the vein, medial which/superior lies near orbit, the is then medial/superior selected after obtainingorbit, is then a localized selected magnified after obtaining roadmap. a Next,localized the magnified SOV is selected roadmap. and is Next, followed the SOV posteriorly is selected and and inferiorly is followed where posteriorly it communicates and inferiorly with the superiorwhere it /communicatesanterior portion with of thethe CSsuperior/anterior (Figure2). When po planningrtion of the this CS approach, (Figure 2). careful When consideration planning this ofapproach, the length careful and consideration compatibility of of the the length coaxial and systems compatibility is critical. of the This coaxial route systems can be quiteis critical. long This and tortuousroute can requiring be quite along tri-axial and systemtortuous with requiring an intermediate a tri-axial catheter system for with support. an intermediate For example, catheter a shorter for intermediatesupport. For catheterexample, allows a shorter for the intermediate maximum amountcatheter of allows usable for microcatheter the maximum length amount to navigate of usable the tortuousmicrocatheter angles, length but if to it isnavigate too short, the you tortuous may not angles be able, but to if reach it is yourtoo short, target. you The may authors not commonlybe able to usereach an your 80 cm target. long sheathThe authors placed commonly in the IJV; ause 115–120 an 80 cmcm intermediatelong sheath placed catheter in is the placed IJV; ina 115–120 the angular cm vein,intermediate followed catheter by a microsystem is placed in to the access angular the CS.vein, followed by a microsystem to access the CS.

Figure 1.1.The The common common facial facial vein (CVF),vein anterior(CVF), facialanterior vein facial (AFV), vein angular (AFV), vein (AV),angular retromandibular vein (AV), veinretromandibular (RMV), middle vein temporal (RMV), veinmiddle (MTV), temporal superficial vein (MTV), temporal (STV), temporal and cavernous vein (STV), sinus and (X) arecavernous demonstrated. sinus (X) are demonstrated. Brain Sci. 2020, 10, 554 4 of 16 Brain Sci. 2020, 10, x FOR PEER REVIEW 4 of 16

Figure 2. The anterior facial vein (solid arrow), angula angularr vein (black arrow), and superior (white arrow) are shown.

Another technique to keep in mind when using this approach is the ability to “milk” the microcatheter in these superficial superficial subcutaneous facial veins. With With one one finger, finger, gentle pressure can be applied toto the the skin skin directly directly over over the microcatheter the microcat inheter a sweeping in a sweeping fashion towards fashion the towards eye. Alternatively, the eye. physicallyAlternatively, manipulating physically the manipulating skin and tissue the canskin change and tissue the angle can change of the vein the angle and allow of the the vein microcatheter and allow theto advance microcatheter or even to advance direct the or catheter even direct into the a desired catheter branch. into a desired This technique branch. This can technique be useful can when be usefulattempting when to attempting navigate a to di ffinavigatecult angle a difficult or gain angl moree supportor gain more by removing support theby slackremoving in the the system. slack in the system.Yu et al. reported endovascular embolization of 74 CCFs in 71 patients using a transvenous approach,Yu et withal. reported an overall endovascular success rate ofembolization 86.5% [11]. The of 74 IPS CCFs was used in 71 to patients access the using CS in a mosttransvenous patients. approach,However, inwith 10 an patients, overall the success IPS was rate not of accessible,86.5% [11]. andThe theIPS authors was used approached to access thethe CSCS throughin most patients.the SOV viaHowever, the angular in 10 veinpatients, (in one the patientIPS was the no SOVt accessible, was selected and the via authors the middle approached temporal the vein). CS throughPrior to adoptingthe SOV via this the transfacial angular vein approach, (in one the pati authorsent the had SOV a technicalwas selected success via the rate middle of 71.6%, temporal while vein).after employing Prior to adopting this technique, this transfacial their success approach rate, improved the authors to 100%.had a technical Berkman success et al. described rate of 71.6%, direct percutaneouswhile after employing puncture this of the techniqu facial veine, their using success ultrasound rate improved guidance to to 100%. treat aBerkman dural CCF et al. [12 described]. In their directreport, percutaneous multiple attempts puncture at transfemoral of the facial embolization vein using ultrasound had failed, guidance and the facial to treat vein a dural ended CCF in a [12]. web Inof smalltheir report, veins making multiple it impossibleattempts atto transfemoral traverse with embolization a microsystem. had Therefore,failed, and the the authors facial vein performed ended ina percutaneous a web of small puncture veins making of the infraorbital it impossible segment to traverse of the with facial a veinmicrosystem. using ultrasound Therefore, guidance the authors and a performed21-gauge micropuncture a percutaneous needle. puncture A 0.018-inch of the infraorbit wire wasal then segment passed of into the thefacial facial vein vein, using and ultrasound the needle wasguidance exchanged and a for21-gauge a 4 Fr sheath.micropuncture Using roadmapping needle. A 0.018-inch technique, wire a microsystem was then passed was then into navigatedthe facial vein,into the and angular the needle vein, was through exchanged the SOV, for a and 4 Fr subsequently sheath. Using into roadmapping the CS. After technique, embolization a microsystem with coils wasand n-BCAthen navigated glue, transfemoral into the angular angiograms vein, through showed completethe SOV, resolutionand subsequently of the fistula. into the The CS. authors After embolizationof the current with report coils have and used n-BCA a similar glue, techniquetransfemoral for directangiograms percutaneous showed puncture complete of resolution the angular of thevein fistula. itself. The authors of the current report have used a similar technique for direct percutaneous punctureThe angularof the angular vein/SOV vein approach itself. is not only useful in cases of IPS thrombosis but also when the fistulaThe site angular is located vein/SOV within theapproach anterior is CSnot and only does useful not in communicate cases of IPS withthrombosis the posterior but also CS. when This isthe a fistulacommon site occurrence is located secondarywithin the to anterior compartmentalization CS and does not of communicate the CS. The IPS with approach the posterior may only CS. provide This is aaccess common to the occurrence posterior CS,secondary while the to SOVcompartmentaliza allows the operatortion of tothe gain CS. access The IPS to anapproach anteriorly may located only providefistula site. access to the posterior CS, while the SOV allows the operator to gain access to an anteriorly located fistula site. 4. Superior Ophthalmic Vein Via the Middle Temporal Vein 4. Superior Ophthalmic Vein Via the Middle Temporal Vein As described in the study by Yu et al., the SOV can also be accessed via the middle temporal veinAs [11 ].described To reach in the the middle study by temporal Yu et al., vein, the the SOV retromandibular can also be accessed vein must via the first middle be accessed. temporal In veinmany [11]. patients, To reach the retromandibularthe middle temporal vein canvein, be the selected retromandibular from the EJV. vein In some must patients, first be theaccessed. common In many patients, the retromandibular vein can be selected from the EJV. In some patients, the common facial vein is first selected at the midcervical segment of the IJV, as described above. In the later approach, the retromandibular vein is selected off the common facial vein by directing a curved wire Brain Sci. 2020, 10, 554 5 of 16

Brain Sci. 2020, 10, x FOR PEER REVIEW 5 of 16 facial vein is first selected at the midcervical segment of the IJV, as described above. In the later approach,postero-laterally, the retromandibular as opposed to the vein anterior is selected facial ovein,ff the which common is selected facial by vein directing by directing the wire a curvedantero- wiremedially. postero-laterally, The retromandibular as opposed vein to the(AKA anterior posterior facial facial vein, vein) which is is formed selected by by the directing junction the of wire the antero-medially.superficial temporal The and retromandibular . vein It (AKAtravels posterior inferiorly facial within vein) the is parotid formed gland, by the deep junction to the of thefacial superficial nerve, before temporal it divides and maxillary into a posterior veins. It branch, travels inferiorlywhich communicates within the parotid with the gland, EJV deepand an to theanterior facial branch, nerve, which before combines it divides with into the a posterior anterior branch,facial vein which to form communicates the common with facial the vein. EJV andThe anretromandibular anterior branch, vein which is navigated combines superiorly, with the anteriorpast the facialanteriorly vein directed to form themaxillary common vein, facial where vein. it Thecontinues retromandibular as the posterior vein is and navigated superiorly superiorly, direct pasted superficial the anteriorly temporal directed vein. maxillary Next, vein,the middle where ittemporal continues vein as is the selected posterior as it and travels superiorly anteriorly directed and medially superficial where temporal it communicates vein. Next, with the the middle SOV temporal(Figures 1 vein and is 3). selected Since the as it superficial travels anteriorly temporal and and medially middle where temporal it communicates veins are superficial with the SOV (Figuresvessels, 1this and is3 ).anotherSince theapproach superficial in which temporal it is andpossible middle to temporalmanually veins manipulate are superficial the skin scalp in order vessels, to thischange is another the angle approach of the invein which or “milk” it is possible the microc to manuallyatheter underneath manipulate thethe skinskin in (Figure order to4). change This may the anglehelp to of traverse the vein ordifficult “milk” tortuous the microcatheter segments underneathin the vein. the In skinthe (Figurecase of4 angular). This may vein help thrombosis to traverse or dihypoplasia,fficult tortuous the segmentsmiddle temporal in the vein. vein In the serves case ofas angular a viable vein alternative thrombosis orto hypoplasia,access the theSOV middle and temporalsubsequently vein the serves anterior as a viableCS. alternative to access the SOV and subsequently the anterior CS.

Figure 3. TheThe middle middle temporal temporal vein vein (solid (solid arrow) arrow) and and its itsconnection connection (open (open arrow) arrow) with with the theSOV SOV are aredemonstrated. demonstrated. Brain Sci. 2020, 10, 554 6 of 16 Brain Sci. 2020, 10, x FOR PEER REVIEW 6 of 16

Figure 4. An example of “milking” the microcatheter along the middle temporal vein is shown. Figure 4. An example of “milking” the microcatheter along the middle temporal vein is shown.

5. Superior Superior Petrosal Petrosal Sinus Sinus Via the Transverse Sinus In 2002, Mounayer, et al. described described the the endovascular endovascular treatment treatment of a dural CCF utilizing the SPS for access to the CS [13]. [13]. In In their their patient, patient, the the IP IPSS could could not not be be catheterized, catheterized, and and approaching approaching the SOV via the facial vein was not possible. Therefore, Therefore, a a 5 5 Fr Fr sheath sheath was was placed placed in in the the IJV, IJV, and a 5 Fr guiding catheter was placed in the the transverse transverse sinus sinus (TS). (TS). Then, Then, the the SPS SPS was was catheteriz catheterizeded with with a a microsystem, microsystem, which allowed retrograde access to the CS. After th thee placement of detachable coils in the CS, final final angiograms showed no evidence of residual fistula.fistula. The The SPS SPS originates in the posteriorposterior/superior/superior portion of of the the CS CS at at the the petrous petrous apex, apex, travels travels poster posteriorior and and lateral lateral in the in superior the superior petrosal petrosal sulcus, sulcus, and drainsand drains into the into distal the distal transverse transverse sinus. sinus. The acut Thee acuteangle anglebetween between the SPS the and SPS the and TS the can TS make can this make a challengingthis a challenging approach. approach. Approaching Approaching the SPS the from SPS the from contralateral the contralateral TS across TS the across torcula the gives torcula a much gives morea much favorable more favorable angle and angle should and be should considered be considered when attempting when attempting this approach. this approach. Given the Givenanatomic the courseanatomic of this course approach, of this approach,there is a risk there of issubarachnoid a risk of subarachnoid hemorrhage hemorrhage in the event in of the vessel event breach. of vessel For thisbreach. reason, For thisit isreason, recommended it is recommended that soft microwires that soft microwires be utilized, be utilized,the wire thebe wireshaped be shapedwith a gentle with a curve,gentle and curve, forceful and forceful movements movements should should be avoided. be avoided.

6. Pterygoid Pterygoid Plexus Plexus Via Via the Maxillary Vein As one of the major egresses of the CS, the pterygo pterygoidid plexus can be used as an access route in the setting of dural CCFs. In In 1998, 1998, Jahan Jahan et al. de describedscribed the the endovascular endovascular treatment treatment of of a right-sided dural CCF via the contralateral pterygoid plexus [14] [14].. The The venous venous drainage drainage in in this this case case was was directed directed contralaterally through through the the intercavernous sinus sinus into into the the left left CS and then inferiorly into the left pterygoid plexus. Secondary Secondary to to thrombosis thrombosis of of the the bilateral bilateral SOVs SOVs and and a a lack of filling filling of the bilateral IPSs, the the authors authors chose chose to to approach approach the the right right CS CS from from the the left left pterygoid pterygoid plexus. plexus. The Theright right CS was CS then was accessedthen accessed through through the intercavernous the intercavernous sinus, sinus, and and coil coil placement placement within within the the right right CS CS resulted resulted in complete resolution of the fistula. The pterygoid plexus lies between the temporalis and the lateral pterygoid muscles. This venous plexus can be accessed by first selecting the common facial vein off the midcervical segment of the IJV. The retromandibular vein is then selected with a curved wire Brain Sci. 2020, 10, 554 7 of 16 complete resolution of the fistula. The pterygoid plexus lies between the temporalis and the lateral pterygoidBrain Sci. 2020 muscles., 10, x FOR This PEER venous REVIEW plexus can be accessed by first selecting the common facial vein o7ff ofthe 16 midcervical segment of the IJV. The retromandibular vein is then selected with a curved wire directed postero-laterally.directed postero-laterally. Next, the Next, anteromedially the anteromedially directed directed maxillary maxillary vein is selected. vein is selected. The maxillary The maxillary vein is avein direct is a tributary direct tributary of the pterygoid of the pterygoid plexus which plexus is which navigated is navigated with a microsystem with a microsystem using a localized using a magnifiedlocalized magnified roadmap. Theroadmap. pterygoid Theplexus pterygoid communicates plexus communicates with the anterior with/inferior the anterior/inferior CS through small CS unnamedthrough small veins unnamed of the foramen veins of of the Vesalius foramen (medial of Vesalius to the (medial foramen to ovale)the foramen and emissary ovale) and veins emissary of the foramenveins of the lacerum. foramen The lacerum. pterygoid The plexus pterygoid is often plexus an enlargedis often an emissary enlarged vein, emissary which vein, can bewhich navigated can be mediallynavigated and medially superiorly and tosuperiorly reach the to CS. reach Most the of CS. this Most approach of this is extracranialapproach is andextracranial may have and a lower may riskhave of a subarachnoidlower risk of subarachnoid hemorrhage than hemorrhage the “in-out-in” than the technique “in-out-in” of trying technique to navigate of trying a thrombosed to navigate or a stenoticthrombosed IPS. However,or stenotic the IPS. disadvantage However, the is the disadvanta technicalge di ffiis cultythe technical of traversing difficulty the tight of traversing net of vessels the thattight make net of up vessels the pterygoid that make plexus, up the and pterygoid therefore, plexus, it is generally and therefore, reserved it is forgenerally cases of reserved bilateral for IPS cases and SOVof bilateral thrombosis IPS and or absence.SOV thrombosis or absence.

7. Inferior Petrooccipital Vein ViaVia thethe InternalInternal JugularJugular VeinVein Kurata etet al. al. described described an alternativean alternative endovascular endova approachscular approach to the CS to via the inferiorCS via petrooccipital the inferior veinpetrooccipital (IPOV) [15 vein]. The (IPOV) IPOV [15]. was The first IPOV named was byfirst Trolard named in by 1868 Trolard when in he1868 discovered when he adiscovered small vein a thatsmall was vein distinct that was from distinct the IPS from [16]. the Katsuta IPS [16]. et al.Katsuta referred et al. to referred the IPOV to as the the IPOV inferior as the petroclival inferior vein.petroclival They vein. described They described it as a small it as veina small that vein may that become may become dilated dilated in the in setting the setting of DAVFs of DAVFs and serveand serve as an as alternative an alternative route route to theto the CS CS [17 [17].]. The The IPOV IPOV originates originates from from the the clivalclival (basilar)(basilar) plexus, coursescourses extracraniallyextracranially through through the the petrooccipital petrooccipital suture, suture, and oftenand contributesoften contributes to the anterior to the condylaranterior confluencecondylar confluence (ACC) (Figure (ACC)5). (Figure It can be5). accessedIt can be throughaccessed the through IJV by th firste IJV selecting by first theselecting ACC fromthe ACC the jugularfrom the bulb. jugular The bulb. IPOV The is then IPOV selected is then by selected directing by a directing microwire a directlymicrowire medial directly from medial the ACC from (more the medialACC (more than formedial selection than offor the selection IPS). The of IPOVthe IPS). is then The navigated IPOV is then superiorly navigated as it runssuperiorly roughly as parallel it runs androughly deep parallel to the IPS. and The deep basilar to the plexus IPS. The is then basilar navigated plexus with is then a localized navigated magnified with a localized roadmap magnified before the posteriorroadmap CSbefore is accessed. the posterior The IPOV CS is is oftenaccessed. mistaken The IPOV for the is IPS often given mistaken their parallel for the routes. IPS given However, their inparallel the case routes. of IPS However, thrombosis in the IPOVcase of may IPS remainthrombosis patent, the or IPOV even may be dilated, remain and patent, allow or access even be to thedilated, CS. and allow access to the CS.

Figure 5.5. The anterioranterior condylarcondylar vein,vein, inferiorinferior petroclivalpetroclival (petroocipital)(petroocipital) vein, inferiorinferior petrosalpetrosal sinussinus (IPS),(IPS), andand cavernouscavernous sinussinus areare demonstrated.demonstrated.

8. Intercavernous Connections (Intercavernous Sinus and Clival Plexus) The intercavernous sinus (aka circular sinus) is both a major egress as well as a major tributary to the CS. This venous pathway has an anterior limb, which runs in front of the pituitary stalk, and a Brain Sci. 2020, 10, 554 8 of 16

8. Intercavernous Connections (Intercavernous Sinus and Clival Plexus) The intercavernous sinus (aka circular sinus) is both a major egress as well as a major tributary to Brainthe CS.Sci. 2020 This, 10 venous, x FOR PEER pathway REVIEW has an anterior limb, which runs in front of the pituitary stalk,8 and of 16 a posterior limb, running behind the pituitary stalk. The anterior limb is generally larger than the posterior limb, running behind the pituitary stalk. The anterior limb is generally larger than the posterior limb, and together with the two CSs, they form the circular sinus. Depending on the venous posterior limb, and together with the two CSs, they form the circular sinus. Depending on the venous anatomy, the anterior limb, posterior limb, or both may be absent. anatomy, the anterior limb, posterior limb, or both may be absent. The clival plexus (aka basilar plexus) is a network of veins located between the two layers of the The clival plexus (aka basilar plexus) is a network of veins located between the two layers of the clival dura and drains into the anterior vertebral venous plexus. While the clival plexus primarily clival dura and drains into the anterior vertebral venous plexus. While the clival plexus primarily serves as an egress of the CS, because of its multiple interconnections, it also provides a pathway serves as an egress of the CS, because of its multiple interconnections, it also provides a pathway between the left and right CS. between the left and right CS. In the setting of CCFs, the venous drainage may be primarily through contralateral pathways. In the setting of CCFs, the venous drainage may be primarily through contralateral pathways. Therefore, the best endovascular approach to a left sided CCF may be through the right IPS. Once the Therefore, the best endovascular approach to a left sided CCF may be through the right IPS. Once the contralateral CS has been accessed, the ipsilateral CS can be accessed by crossing the intercavernous contralateral CS has been accessed, the ipsilateral CS can be accessed by crossing the intercavernous sinus, or more commonly through the clival plexus. The intercavernous connection is selected with a sinus, or more commonly through the clival plexus. The intercavernous connection is selected with a curved microwire directed either anteriorly or posteriorly. The microwire is then traversed across the curved microwire directed either anteriorly or posteriorly. The microwire is then traversed across the intercavernous connection and, if necessary, looped within the opposite CS to provide support for the intercavernous connection and, if necessary, looped within the opposite CS to provide support for microcatheter to follow (Figure6). This approach gives the operator the option of using virtually any the microcatheter to follow (Figure 6). This approach gives the operator the option of using virtually of the described approaches on the contralateral side of the fistula site. any of the described approaches on the contralateral side of the fistula site.

Figure 6. 6. DemonstratesDemonstrates access access of the of left the cavernous left cavernous sinus (X sinus) through (X) throughan intercavernous an intercavernous approach (arrows).approach (arrows).

9. Percutaneous TransorbitalTransorbital Puncture Puncture of of the the Cavernous Cavernous Sinus, Sinus, Inferior Inferior Ophthalmic Ophthalmic Vein, Vein, or or Superior Ophthalmic Vein When transfemoral access access to to the fistula fistula site is not possible, direct percutaneouspercutaneous transorbital puncture of the CS, SOV,SOV, oror IOVIOV cancan bebe anan effeffectectiveive alternative. alternative. KurataKurata etet al.al. described direct percutaneous puncture of the extraconal portion of the SOV in three patients with traumatic CCFs in which transarterial and IPS approaches failed [[18].18]. In In their approach, the extraconal portion portion of of the SOV is cannulated with an 18-gauge sheathed needle inserted into the upper portion of the medial orbital angle. The needle is guided by transfemoral angiographic roadmapping technique. The anterior apsidal vein located between the first and second segments (intraconal portion) of the SOV is used as a landmark. More commonly reported is direct puncture of the IOV. The IOV begins as a network of veins along the anterior/medial wall of the orbit. The IOV runs posteriorly along the lower half of the orbit, above the , until it divides into two branches. The inferior Brain Sci. 2020, 10, 554 9 of 16

SOV is cannulated with an 18-gauge sheathed needle inserted into the upper portion of the medial orbital angle. The needle is guided by transfemoral angiographic roadmapping technique. The anterior apsidal vein located between the first and second segments (intraconal portion) of the SOV is used as a landmark. More commonly reported is direct puncture of the IOV. The IOV begins as a network of veins along the anterior/medial wall of the orbit. The IOV runs posteriorly along the lower half of the orbit, above the inferior rectus muscle, until it divides into two branches. The inferior branch passes through the inferior orbital fissure and contributes to the pterygoid plexus. The superior branch passes through the superior orbital fissure (SOF) and either enters the anterior CS directly or, more commonly, joins the SOV before draining into the CS. White et al. described their series of eight patients with CCFs treated by direct transorbital puncture of the IOV or CS and subsequent coil embolization [19]. All eight patients experienced complete obliteration of their CCF in a single procedure, and there were no permanent periprocedural complications. In this approach, transfemoral access is first obtained to investigate the fistula as well as to provide transarterial diagnostic angiograms. Once it is discovered that the traditional venous pathways are not accessible, the ipsilateral orbit is prepped and draped in the usual sterile fashion. A 21-gauge needle and a 4 French micropuncture kit are used for percutaneous access. The 21-gauge spinal needle, attached to aspiration tubing, is inserted into the inferolateral aspect of the orbit and gradually advanced along the orbital floor. Under live fluoroscopic guidance, the tip of the needle is directed towards the superior orbital fissure (SOF). The SOF is separated from the by placing the AP tube in an oblique 45-degree projection, while keeping the floor of the orbit flat. Care is taken to not damage the within the optic canal. While the needle is advanced, gentle aspiration is applied to the tubing with a 5 mL syringe until venous return is obtained. The tubing is then removed, and the micropuncture wire (0.018 gauge) is inserted through the needle. Next, the needle is exchanged for a 4 French introducer sheath (alternatively the needle can be left in place and direct injections through the needle can be performed). A venogram is performed through the sheath to confirm positioning within the IOV or the CS itself. Care must be taken to perform only gentle injections in these settings to avoid applying increased pressure in what is already an over pressurized system as this can lead to vessel rupture and significant morbidity. Next, using roadmapping technique a microcatheter is advanced coaxially over a microwire into the CS (Figure7). Once the embolization is complete, a diagnostic angiogram is performed through the arterial catheter to confirm resolution of the fistula. The microcatheter and sheath are then removed, and gentle pressure is applied to the puncture site. A dressing is generally not necessary. This approach is particularly useful in fistulas located within the anterior CS which have prominent drainage into the ophthalmic veins. Additionally, the direct percutaneous access to the CS avoids the need for surgical exposure of the ophthalmic veins. It is important to note, however, that perforation of an orbital vein carries higher consequences than perforation of a facial (angular) vein. Therefore, this approach should be reserved for patient0s in which lower risk approaches are not possible. It is recommended that ophthalmology be available for emergent optic nerve and/or globe decompression if necessary. Brain Sci. 2020, 10, 554 10 of 16

Brain Sci. 2020, 10, x FOR PEER REVIEW 10 of 16

Figure 7. DemonstratesDemonstrates percutaneous percutaneous transo transorbitalrbital puncture of the cavernous sinus (X) via the inferior ophthalmic vein (arrow).

10. Surgical Surgical Exposure Exposure of the SOV or IOV An alternative that should be considered for anteriorly located dural CCFs with venous drainage drainage through dilateddilated ophthalmicophthalmic veins veins is is surgical surgical exposure exposure of of the the SOV SOV or IOV.or IOV. Surgical Surgical exposure exposure of the of SOV the SOVand theand IOV the have IOV been have previously been previously described described [20–24]. [20–24]. Surgical Surgical exposure exposure of the SOV of isthe more SOV commonly is more performedcommonly andperformed is described and below.is described Just as inbelow. the direct Just percutaneousas in the direct approach, percutaneous transfemoral approach, access transfemoralis first obtained access to investigate is first obtained the fistula to investigate as well as tothe provide fistula transarterialas well as to diagnostic provide transarterial angiograms. diagnosticOnce this isangiograms. done, an ophthalmologist Once this is done, makes an ophthalmologist a 15 mm curvilinear makes incision a 15 mm just curvilinear below the eyebrow.incision justUsing below blunt the dissection, eyebrow. Using the SOV blunt is identified,dissection, isolated,the SOV is and identified, secured isolated, just below and the secured superior just orbitalbelow therim superior at the level orbital of the rim trochlea. at the level Ultrasound of the trochlea may be. Ultrasound helpful in may locating be helpful the SOV. in locating Systemic the heparin SOV. Systemicis avoided heparin to promote is avoided thrombosis to promote of the thrombosis CS and reduce of the the CS risk and of reduce hemorrhage. the risk Once of hemorrhage. the SOV is Onceexposed, the SOV a 21-gauge is exposed, needle a 21-gauge is used to needle puncture is used the to vein puncture within the the vein middle within third the of middle the visualized third of thesegment. visualized Next, segment. the micropuncture Next, the micropuncture wire is introduced wire is through introduced the needlethrough and the guidedneedle and into guided the CS intounder the live CS fluoroscopy.under live fluoroscopy. In general, In the general, SOV runs the SOV medial runs to medial lateral to as lateral it courses as ittowards courses towards the SOF. theHowever, SOF. However, if the wire ifdoes the wire not passdoes easily not pass in this easily direction, in this adirection, lateral to a medial lateral approachto medial canapproach be tried can as beanatomic tried as variations anatomic orvariations loops in or the loops vein in can the exist. vein Next,can exist. the needleNext, the isexchanged needle is exchanged for the 4 Fr for dilator the 4 Frfrom dilator a standard from a micropuncturestandard micropuncture kit (Cook kit Medical, (Cook Bloomington,Medical, Bloom IN,ington, USA) IN, and USA) is advanced and is advanced coaxially coaxiallyapproximately approximately 2–5 cm. A 2–5 standard cm. A angiocathstandard IVangiocath catheter, IV which catheter, is shorter which than is shorter the 4 Fr than dilator, the is4 anFr dilator,alternative is an if alternative the microwire if the does microwire not have does enough not have “landing enough room” “landing prior room” to a tight prior turn. to a Silk tight sutures turn. Silk sutures are used to secure the sheath to the vein in order to prevent losing access during the procedure. A venogram is then performed through the sheath to confirm positioning within the SOV Brain Sci. 2020, 10, 554 11 of 16 are used to secure the sheath to the vein in order to prevent losing access during the procedure. ABrain venogram Sci. 2020, 10 is, x then FOR performedPEER REVIEW through the sheath to confirm positioning within the SOV (Figure11 of8 16). The inner diameter of the dilator is 0.038”, which will accept up to a size 17 microcatheter, which is (Figure 8). The inner diameter of the dilator is 0.038”, which will accept up to a size 17 microcatheter, then advanced over a microwire into the CS using roadmapping technique. A venogram through the which is then advanced over a microwire into the CS using roadmapping technique. A venogram microcathter is performed prior to embolization with coils and/or embolic glue material. Once the through the microcathter is performed prior to embolization with coils and/or embolic glue material. embolization is complete, a diagnostic angiogram is performed through the arterial catheter to confirm Once the embolization is complete, a diagnostic angiogram is performed through the arterial catheter resolution of the fistula. The microcatheter and sheath are then removed, and the SOV, which is no to confirm resolution of the fistula. The microcatheter and sheath are then removed, and the SOV, longer under arterial pressure, is typically sutured or cauterized on either side of the puncture site. which is no longer under arterial pressure, is typically sutured or cauterized on either side of the In some situations where orbital venous drainage is very tenuous, maintaining patency of outlet veins puncture site. In some situations where orbital venous drainage is very tenuous, maintaining patency can be attempted without cauterization to prevent stagnation or thrombosis. Balanced with the risk of of outlet veins can be attempted without cauterization to prevent stagnation or thrombosis. Balanced bleeding, consideration should be given to postoperative anticoagulation with initiation of a heparin with the risk of bleeding, consideration should be given to postoperative anticoagulation with drip to maintain venous drainage. The wound is closed in layers, and the skin is re-approximated initiation of a heparin drip to maintain venous drainage. The wound is closed in layers, and the skin cosmetically. Prior to attempting this approach, non-invasive cerebral vascular imaging should be is re-approximated cosmetically. Prior to attempting this approach, non-invasive cerebral vascular reviewed carefully to evaluate the SOV anatomy. A small, atretic SOV is a contraindication to this imaging should be reviewed carefully to evaluate the SOV anatomy. A small, atretic SOV is a technique. However, a thrombosed SOV with a large diameter is not necessarily a contraindication contraindication to this technique. However, a thrombosed SOV with a large diameter is not and may be able to be traversed by the previously described “drilling” technique. Surgical exposure of necessarily a contraindication and may be able to be traversed by the previously described “drilling” the SOV or IOV allows for direct visualization and immobility of the arterialized vessel, which may technique. Surgical exposure of the SOV or IOV allows for direct visualization and immobility of the carry a lower risk of vessel rupture than percutaneous puncture. arterialized vessel, which may carry a lower risk of vessel rupture than percutaneous puncture.

Figure 8. Demonstrates access to the cavernous sinus (X) via surgical exposure and cannulation of the Figure 8. Demonstrates access to the cavernous sinus (X) via surgical exposure and cannulation of the SOV (arrows). SOV (arrows).

11. Surgical Exposure of the Cavernous Sinus Despite the the multiple multiple routes routes to to the the CS CS available available to tothe the endovascular endovascular surgeon, surgeon, in some in some cases, cases, the venousthe venous anatomy anatomy and andlocation location of the of fistula the fistula site make site make treatment treatment with endovascular with endovascular techniques techniques alone inadequate.alone inadequate. In these In thesecases, cases, open open microsurgical microsurgical exposure exposure of ofthe the CS CS combined combined with with endovascular embolization may be an option. Staged Staged microsurgica microsurgicall obliteration obliteration of of residual residual DAVFs DAVFs after incomplete endovascular embolization is well published [4,25,26]. However, simultaneous open surgery and endovascular embolization of CCFs are less commonly reported. Krisht et al. reported the treatment of a dural CCF in which the lateral wall of the CS was surgically exposed and dissected prior to cannulation and coil embolization [27]. Geurrero et al. reported a similar case in which a pretemporal, Brain Sci. 2020, 10, 554 12 of 16 endovascular embolization is well published [4,25,26]. However, simultaneous open surgery and endovascular embolization of CCFs are less commonly reported. Krisht et al. reported the treatment Brain Sci. 2020, 10, x FOR PEER REVIEW 12 of 16 of a dural CCF in which the lateral wall of the CS was surgically exposed and dissected prior to cannulation and coil embolization [27]. Geurrero et al. reported a similar case in which a pretemporal, extradural approach to the lateral CS was utilized for treatment of a dural CCF. Once the lateral wall extradural approach to the lateral CS was utilized for treatment of a dural CCF. Once the lateral wall was exposed, the CS was cannulated under ultrasound guidance prior to embolization of the fistula was exposed, the CS was cannulated under ultrasound guidance prior to embolization of the fistula with coils [28]. We have reported the treatment of a paracavernous venous plexus fistula with an with coils [28]. We have reported the treatment of a paracavernous venous plexus fistula with an open open surgical approach combined with endovascular embolization [29]. Through a pterional surgical approach combined with endovascular embolization [29]. Through a pterional craniotomy, an craniotomy, an intradural pretemporal approach to the lateral wall of the cavernous sinus was intradural pretemporal approach to the lateral wall of the cavernous sinus was performed. Using a performed. Using a preoperative CT angiogram and intraoperative neuronavigation, the exact preoperative CT angiogram and intraoperative neuronavigation, the exact location of the fistula site location of the fistula site within the paracavernous venous plexus was identified. Next, the tip of a within the paracavernous venous plexus was identified. Next, the tip of a spinal needle, registered to spinal needle, registered to and guided by neuronavigation, was introduced into the fistula. An and guided by neuronavigation, was introduced into the fistula. An angiogram through the spinal angiogram through the spinal needle was then performed to confirm positioning within the fistula needle was then performed to confirm positioning within the fistula sac without filling of the ICA sac without filling of the ICA (Figure 9). After injection of Onyx embolic material into the fistula, (Figure9). After injection of Onyx embolic material into the fistula, intraoperative transfemoral intraoperative transfemoral angiogram confirmed complete obliteration of the fistula. Secondary to angiogram confirmed complete obliteration of the fistula. Secondary to the risks involved with open the risks involved with open surgery, this type of combined approach is generally reserved for surgery, this type of combined approach is generally reserved for fistulas that have failed embolization fistulas that have failed embolization by traditional endovascular routes. However, as in the above by traditional endovascular routes. However, as in the above report, DAVFs with fistula sites in report, DAVFs with fistula sites in paracavernous locations can make treatment by traditional paracavernous locations can make treatment by traditional transvenous routes technically impossible. transvenous routes technically impossible. It is in these cases that combined open surgical and It is in these cases that combined open surgical and endovascular embolization can be useful. endovascular embolization can be useful.

Figure 9. DemonstratesDemonstrates surgical surgical exposure exposure of ofthe the lateral lateral wall wall of the of theright right cavernous cavernous sinus sinus via a via pre- a pre-temporaltemporal approach approach (left). (left). The Thearrow arrow shows shows the site the siteof spinal of spinal needle needle puncture puncture in the in thelateral lateral wall wall of the of thecavernous cavernous sinus. sinus.

12. Transarterial ViaVia thethe CavernousCavernous SegmentSegment ofof thethe ICAICA (Direct(Direct CCF)CCF) oror ViaVia ICA ICA/ECA/ECA Meningeal Meningeal Branches (Dural CCF) In thethe setting setting of directof direct CCFs, CCFs, the tear the in tear the cavernousin the cavernous segment ofsegment the ICA of provides the ICA an endovascularprovides an routeendovascular to the CS. route A primary to the CS. transarterial A primary approach transarter canial often approach be used can to often embolize be used these to fistulas. embolize Prior these to attemptingfistulas. Prior a primary to attempting embolization a primary of the embolization fistula, a complete of the fistula, angiogram a complete should angiogram be completed, should and be if adequatecompleted, cross-filling and if adequate is identified, cross-filling a balloon is identified, test occlusion a balloon (BTO) test occlusion is recommended. (BTO) is recommended. If the patient remainsIf the patient neurologically remains neurologically unchanged, the unchanged, most effective the most treatment effective is often treatment complete is often ICA occlusion.complete ICA It is importantocclusion. toIt is remember important that to theremember carotid that occlusion the caro shouldtid occlusion extend across should the extend fistula across site both the proximallyfistula site andboth distally proximally to prevent and distally retrograde to prevent filling retrograde of the fistula filling from of collateral the fistula circulation. from collateral In the circulation. case of failed In BTO,the case the of fistula failed mustBTO, the be treatedfistula must while be maintaining treated while patency maintaining of the patency ICA. In of this the case,ICA. theIn this authors case, oftenthe authors use a two-catheter often use a systemtwo-catheter with a microcathetersystem with a in microcatheter the cavernous in sinus the forcavernous embolization sinus andfor embolization and a Scepter balloon catheter (MicroVention, Tustin, CA, USA) to protect the ICA. Using roadmapping technique, a microsystem is then navigated through the tear in the cavernous ICA into the affected CS. An occlusion balloon, or a stent, is placed within the cavernous ICA across the fistula site to protect the ICA during embolization. Coils, Onyx (Covidien, Irvine, CA, USA), or a combination of both are then used to obliterate the fistula. Alternatively, in some cases of direct CCF, Brain Sci. 2020, 10, 554 13 of 16 a Scepter balloon catheter (MicroVention, Tustin, CA, USA) to protect the ICA. Using roadmapping technique, a microsystem is then navigated through the tear in the cavernous ICA into the affected CS. An occlusion balloon, or a stent, is placed within the cavernous ICA across the fistula site to protect the ICA during embolization. Coils, Onyx (Covidien, Irvine, CA, USA), or a combination of both are Brain Sci. 2020, 10, x FOR PEER REVIEW 13 of 16 then used to obliterate the fistula. Alternatively, in some cases of direct CCF, a combined transarterial aand combined transvenous transarterial approach and is transvenous the safest and approach most e isffective the safest way and to embolizemost effective the fistula. way to Figureembolize 10 thedemonstrates fistula. Figure a right 10 sided demonstrates direct CCF a withright venous sided drainagedirect CCF through with thevenous intercavernous drainage through sinus into the a intercavernousdilated left CS. Insinus this into case, a thedilated authors left firstCS. navigatedIn this case, a Hyperformthe authors balloon first navigated (Covidien, a Hyperform Irvine, CA, balloonUSA) across (Covidien, the tear Irvine, in the CA, right USA) ICA. Next,across a the microsystem tear in the was right navigated ICA. Next, through a microsystem the left IPS, intowas navigatedthe left CS, through and subsequently the left IPS, into into the the intercavernous left CS, and subsequently sinus. With into the balloonthe intercavernous inflated to preventsinus. With coil themigration balloon into inflated the right to ICA,prevent theintercavernous coil migration sinus into wasthe embolizedright ICA, with the coils,intercavernous effectively obliteratingsinus was embolizedthe fistula. with Final coils, angiograms effectively showed obliterating no evidence the fistula. of residual Final fistula,angiograms and the showed patient no had evidence complete of residualresolution fistula, of her and preoperative the patient symptoms. had complete resolution of her preoperative symptoms.

Figure 10. DemonstratesDemonstrates a a right right sided sided direct direct carotid carotid cavernous fistulas fistulas (CCF). An occlusion balloon is placed within the right cavernous in internalternal carotid carotid artery artery (ICA) (ICA) (white (white arrow) arrow) across across the the fistula fistula site. site. Coils are placed within the intercavernous sinus (b (blacklack solid arrow) through a transvenous inferior petrosal sinus (IPS) (IPS) approach approach (white (white solid solid arrow). arrow). No Notete the the superior superior petrosal petrosal sinus sinus (black (black arrows), arrows), in thein the lateral lateral projection, projection, with with its itsacute acute angle angle off o theff the transverse transverse sinus. sinus.

For dural CCFs, a transarterial approach with embolization of the dural ICA or ECA feeders can be an effective effective treatment strategy. However, navigating multiple small arterial feeders can be difficult difficult and time consuming. Furthermore, Furthermore, given given the the added added risk risk of of cranial nerve deficit deficit with occlusion of mengingeal , the authors prefer the tran transvenoussvenous approach for most dural CCFs and use the transarterial approach sparingly.

13. Discussion Discussion The key to approach approach selection lies in careful careful study study of of initial initial diagnostic diagnostic angiography. angiography. In particular particular the venousvenous phasephase isis reviewed reviewed looking looking at at the the connections connections of of the the internal internal and and external external jugular jugular veins veins and andtheir their respective respective venous venous outlet outlet anatomy. anatomy. Characterization Characterization of the of connections the connections of the of SOV the toSOV the to facial the facialvenous venous system system is of critical is of critical importance. importance. The absence The absence of any viableof any endovascularviable endovascular route may route require may requiremore direct more access direct to access the cavernous to the cavernous sinus. sinus. While this work represents a detailed review of the commonlycommonly used endovascular approaches to the CS, it is not intendedintended to be comprehensive.comprehensive. Other, approaches have been described including direct transovale access to the CS. Gil etet al.al. described percutaneous percutaneous puncture puncture of of a CCF that was refractory to standard approaches through the fora foramenmen ovale in order to completely obliterate the fistulafistula [30]. [30]. Ghosh Ghosh et et al. al. descri describedbed a apatient patient who who underwent underwent image-guided image-guided burr burr hole hole placement placement to allow catheterization of the Sylvian vein and subsequently access the CS and then embolize the patient’s CCF [31]. Endoscopic-assisted transsphenoidal access to the CS for CCF treatment has also been described [32]. These approaches, and more, highlight the creativity of the endovascular surgeon and the multitude of options available. The transvenous approach to the CS is an effective management strategy for the treatment of dural CCFs. The venous anatomy associated with the cavernous sinus can be complex and highly variable, with hypoplasia and venous thrombosis commonly seen [1,33]. CCF mimics, such as fistulas Brain Sci. 2020, 10, 554 14 of 16 to allow catheterization of the Sylvian vein and subsequently access the CS and then embolize the patient’s CCF [31]. Endoscopic-assisted transsphenoidal access to the CS for CCF treatment has also been described [32]. These approaches, and more, highlight the creativity of the endovascular surgeon and the multitude of options available. The transvenous approach to the CS is an effective management strategy for the treatment of dural CCFs. The venous anatomy associated with the cavernous sinus can be complex and highly variable, with hypoplasia and venous thrombosis commonly seen [1,33]. CCF mimics, such as fistulas of the paracavernous sinus, clival plexus, laterocavernous sinus, and dura of the sphenoid wing can further complicate treatment of these DAVFs [29,34]. A detailed knowledge of the multiple pathways to the CS, as well as the surrounding venous anatomy, can be the difference between successful fistula obliteration and a failed attempt. Many benign dural CCFs will resolve spontaneously with time, and conservative management should be discussed as a treatment option in the absence of worsening vision, increasing intraocular pressure, or CVR [35]. However, waiting too long to intervene can lead to venous outflow obstruction and increase the technical difficulty, and risks, of treatment. Once the decision to intervene has been made, it is important to keep in mind the goals of therapy, as well as the priority of each goal. The highest risk of death or major disability in a patient with a CCF is intracranial hemorrhage secondary to venous hypertension. For this reason, the authors prefer to disconnect the site of CVR first before addressing orbital symptoms. For example, in a CCF with reflux into both the SMCV and SOV, the authors will first block the venous outlet into the SMCV in the posterior CS (with coils and/or liquid embolic material) and then reposition the microcather into the anterior CS to block the reflux into the SOV. Remember that all injections should be done gently especially within orbital veins or the CS itself in order to avoid over pressurizing an abnormally high-pressure system, which can lead to vessel rupture with intraorbital and/or intracranial hemorrhage. Above all, the fistula site itself must be completely obliterated to avoid redirecting venous outflow into alternate pathways, which can turn a symptomatic CCF with reflux only into the SOV into a life-threatening fistula with reflux into cortical veins. The evaluation and management of patients with a CCF has largely become the responsibility of the endovascular surgeon. When intervention is indicated in a patient with a dural CCF, a transvenous approach through the IPS is commonly used. However, in the absence of a patent IPS multiple alternative routes do exist, and an understanding of and experience with each approach can greatly enhance the technical success of these procedures.

Author Contributions: Conceptualization, J.D. and G.D.; methodology, J.D., G.D., and N.K.; validation, N.G., R.G., D.R., R.J., S.T., and V.S.; formal analysis, G.D. and N.K.; investigation, G.D., N.G., R.G., D.R., R.J., S.T., and V.S.; writing—original draft preparation, J.D.; writing—review and editing, G.D., N.K., N.G., S.T., and V.S. All authors have read and agreed to the published version of the manuscript. Funding: This research received no external funding. Conflicts of Interest: The authors declare no conflict of interest.

References

1. Campero, A.; Campero, A.A.; Martins, C.; Yasuda, A.; Rhoton, A.L., Jr. Surgical anatomy of the dural walls of the cavernous sinus. J. Clin. Neurosci. Off. J. Neurosurg. Soc. Australas. 2010, 17, 746–750. [CrossRef] [PubMed] 2. Barrow, D.L.; Spector, R.H.; Braun, I.F.; Landman, J.A.; Tindall, S.C.; Tindall, G.T. Classification and treatment of spontaneous carotid-cavernous sinus fistulas. J. Neurosurg. 1985, 62, 248–256. [CrossRef][PubMed] 3. Gemmete, J.J.; Ansari, S.A.; Gandhi, D.M. Endovascular techniques for treatment of carotid-cavernous fistula. J. Neuro Ophthalmol. Off. J. North Am. Neuro Ophthalmol. Soc. 2009, 29, 62–71. [CrossRef][PubMed] 4. Klisch, J.; Huppertz, H.J.; Spetzger, U.; Hetzel, A.; Seeger, W.; Schumacher, M. Transvenous treatment of carotid cavernous and dural arteriovenous fistulae: Results for 31 patients and review of the literature. Neurosurgery 2003, 53, 836–856. [CrossRef] Brain Sci. 2020, 10, 554 15 of 16

5. Malan, J.; Lefeuvre, D.; Mngomezulu, V.; Taylor, A. Angioarchitecture and treatment modalities in posttraumatic carotid cavernous fistulae. Interv. Neuroradiol. J. Perither. Neuroradiol. Surg. Proced. Relat. Neurosci. 2012, 18, 178–186. [CrossRef] 6. Luo, C.B.; Teng, M.M.; Chang, F.C.; Chang, C.Y. Traumatic indirect carotid cavernous fistulas: Angioarchitectures and results of transarterial embolization by liquid adhesives in 11 patients. Surg. Neurol. 2009, 71, 216–222. [CrossRef] 7. Korkmazer, B.; Kocak, B.; Tureci, E.; Islak, C.; Kocer, N.; Kizilkilic, O. Endovascular treatment of carotid cavernous sinus fistula: A systematic review. World J. Radiol. 2013, 5, 143–155. [CrossRef] 8. Miller, N.R. Diagnosis and management of dural carotid-cavernous sinus fistulas. Neurosurg. Focus 2007, 23, E13. [CrossRef] 9. Shiu, P.C.; Hanafee, W.N.; Wilson, G.H.; Rand, R.W. Cavernous sinus venography. Am. J. Roentgenol. Radium Ther. Nucl. Med. 1968, 104, 57–62. [CrossRef] 10. Miller, D.L.; Doppman, J.L.; Chang, R. Anatomy of the junction of the inferior petrosal sinus and the internal jugular vein. Am. J. Neuroradiol. 1993, 14, 1075–1083. 11. Yu, S.C.; Cheng, H.K.; Wong, G.K.; Chan, C.M.; Cheung, J.Y.; Poon, W.S. Transvenous embolization of dural carotid-cavernous fistulae with transfacial catheterization through the superior ophthalmic vein. Neurosurgery 2007, 60, 1032–1037. [CrossRef][PubMed] 12. Berkmen, T.; Troffkin, N.A.; Wakhloo, A.K. Transvenous sonographically guided percutaneous access for treatment of an indirect carotid cavernous fistula. Am. J. Neuroradiol. 2003, 24, 1548–1551. [PubMed] 13. Mounayer, C.; Piotin, M.; Spelle, L.; Moret, J. Superior petrosal sinus catheterization for transvenous embolization of a dural carotid cavernous sinus fistula. Am. J. Roentgenol. 2002, 23, 1153–1155. 14. Jahan, R.; Gobin, Y.P.; Glenn, B.; Duckwiler, G.R.; Vinuela, F. Transvenous embolization of a dural arteriovenous fistula of the cavernous sinus through the contralateral pterygoid plexus. Neuroradiology 1998, 40, 189–193. [CrossRef] 15. Kurata, A.; Suzuki, S.; Iwamoto, K.; Nakahara, K.; Inukai, M.; Niki, J.; Satou, K.; Yamada, M.; Fujii, K.; Kan, S.; et al. A new transvenous approach to the carotid-cavernous sinus via the inferior petrooccipital vein. J. Neurosurg. 2012, 116, 581–587. [CrossRef] 16. Trolard, P. Anatomie du Système Veineux de L’encéphale et du Crane. Ph.D. Thesis, Faculté de Médecine de Paris, Paris, France, 1868. 17. Katsuta, T.; Rhoton, A.L., Jr.; Matsushima, T. The jugular foramen: Microsurgical anatomy and operative approaches. Neurosurgery 1997, 41, 149–201. [CrossRef] 18. Kurata, A.; Suzuki, S.; Iwamoto, K.; Miyazaki, T.; Inukai, M.; Abe, K.; Niki, J.; Yamada, M.; Fujii, K.; Kan, S. Direct-puncture approach to the extraconal portion of the superior ophthalmic vein for carotid cavernous fistulae. Neuroradiology 2009, 51, 755–759. [CrossRef] 19. White, J.B.; Layton, K.F.; Evans, A.J.; Tong, F.C.; Jensen, M.E.; Kallmes, D.F.; Dion, J.E.; Cloft, H.J. Transorbital puncture for the treatment of cavernous sinus dural arteriovenous fistulas. Am. J. Neuroradiol. 2007, 28, 1415–1417. [CrossRef] 20. Miller, N.R.; Monsein, L.H.; Debrun, G.M.; Tamargo, R.J.; Nauta, H.J. Treatment of carotid-cavernous sinus fistulas using a superior ophthalmic vein approach. J. Neurosurg. 1995, 83, 838–842. [CrossRef] 21. Goldberg, R.A.; Goldey, S.H.; Duckwiler, G.; Vinuela, F. Management of cavernous sinus-dural fistulas. Indications and techniques for primary embolization via the superior ophthalmic vein. Arch. Ophthalmol. Chic. III 1960 1996, 114, 707–714. [CrossRef] 22. Quinones, D.; Duckwiler, G.; Gobin, P.Y.; Goldberg, R.A.; Vinuela, F. Embolization of dural cavernous fistulas via superior ophthalmic vein approach. Am. J. Neuroradiol. 1997, 18, 921–928. [CrossRef][PubMed] 23. Oono, S.; Matsui, Y.; Saito, I.; Nakamatsu, T.; Katou, A. Dural carotid-cavernous fistula successfully treated by embolization via inferior ophthalmic vein Case report. Neuro Ophthalmol. 1998, 20, 69–74. [CrossRef] 24. Michels, K.S.; Ng, J.D.; Falardeau, J.; Roberts, W.G.; Petersen, B.; Nesbit, G.M.; Barnwell, S.L. Transvenous embolization of a dural carotid-cavernous sinus fistula via the inferior ophthalmic vein. Ophthalmic Plast. Reconstr. Surg. 2007, 23, 480–482. [CrossRef][PubMed] 25. Natarajan, S.K.; Ghodke, B.; Kim, L.J.; Hallam, D.K.; Britz, G.W.; Sekhar, L.N. Multimodality treatment of intracranial dural arteriovenous fistulas in the Onyx era: A single center experience. World Neurosurg. 2010, 73, 365–379. [CrossRef][PubMed] Brain Sci. 2020, 10, 554 16 of 16

26. Vougioukas, V.I.; Coulin, C.J.; Shah, M.; Berlis, A.; Hubbe, U.; Van Velthoven, V. Benefits and limitations of image guidance in the surgical treatment of intracranial dural arteriovenous fistulas. Acta Neurochir. 2006, 148, 145–153, discussion 153. [CrossRef] 27. Krisht, A.F.; Burson, T. Combined pretemporal and endovascular approach to the cavernous sinus for the treatment of carotid-cavernous dural fistulae: Technical case report. Neurosurgery 1999, 44, 415–418. [CrossRef] 28. Guerrero, C.A.; Raja, A.I.; Naranjo, N.; Krisht, A.F. Obliteration of carotid-cavernous fistulas using direct surgical and coil-assisted embolization: Technical case report. Neurosurgery 2006, 58, E382, discussion E382. [CrossRef] 29. Dye, J.A.; Buchanan, C.C.; Gonzalez, N.R. Integrated open surgical and endovascular embolization treatment of a paracavernous venous plexus fistula: Case report. J. Neurosurg. 2015, 122, 933–938. [CrossRef] 30. Gil, A.; Lopez-Ibor, L.; Lopez-Flores, G.; Cuellar, H.; Murias, E.; Rodriguez-Boto, G. Treatment of a carotid cavernous fistula via direct transovale cavernous sinus puncture. J. Neurosurg. 2013, 119, 247–251. [CrossRef] 31. Ghosh, R.; Al Saiegh, F.; Mahtabfar, A.; Mouchtouris, N.; Khanna, O.; Sweid, A.; Chalouhi, N.; Lebovitz, J.; Tjoumarkaris, S.; Gooch, M.; et al. Burr hole-assisted direct transsylvian venous catheterization for caotid-cavernous fisutla embolization: A case report. Oper. Neurosurg. 2020, 19, E196–E200. [CrossRef] 32. Tang, C.L.; Liao, C.H.; Chen, W.H.; Shen, S.C.; Lee, C.H.; Lee, H.T.; Tsuei, Y.S. Endoscope-assisted transsphenoidal puncture of the cavernous sinus for embolization of carotid-cavernous fistula in a neurosurgical hybrid operating suite. J. Neurosurg. 2017, 127, 327–331. [CrossRef][PubMed] 33. San Millan Ruiz, D.; Fasel, J.H.; Rufenacht, D.A.; Gailloud, P. The of breschet: Does it exist? An anatomic study. Am. J. Neuroradiol. 2004, 25, 112–120. [PubMed] 34. Shi, Z.S.; Ziegler, J.; Feng, L.; Gonzalez, N.R.; Tateshima, S.; Jahan, R.; Martin, N.A.; Vinuela, F.; Duckwiler, G.R. sphenoidal region dural arteriovenous fistulas: Anatomic and treatment considerations. Am. J. Neuroradiol. 2013, 34, 373–380. [CrossRef][PubMed] 35. Bujak, M.; Margolin, E.; Thompson, A.; Trobe, J.D. Spontaneous resolution of two dural carotid-cavernous fistulas presenting with optic neuropathy and marked congestive ophthalmopathy. J. Neuro Ophthalmol. Off. J. North Am. Neuro Ophthalmol. Soc. 2010, 30, 222–227. [CrossRef][PubMed]

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