NeurovascularImaging DOI10.1007/978-1-4614-9212-2_1-1 #SpringerScience+BusinessMediaNewYork2014 – ICA ECA Collaterals MaximMokina,bandAdnanH.Siddiquia,b,c,d,e* aDepartmentofNeurosurgery,SchoolofMedicineandBiomedicalSciences,UniversityatBuffalo,StateUniversityof NewYork,Buffalo,NY,USA bDepartmentofNeurosurgery,GatesVascularInstitute/KaleidaHealth,Buffalo,NY,USA cDepartmentofRadiology,SchoolofMedicineandBiomedicalSciences,UniversityatBuffalo,StateUniversityof NewYork,Buffalo,NY,USA dToshibaStrokeandVascularResearchCenter,UniversityatBuffalo,StateUniversityofNewYork,Buffalo,NY,USA eJacobsInstitute,Buffalo,NY,USA Abstract Knowledgeandidentificationofmultipleanastomoticconnectionsbetweentheexternalcarotidartery and the internal carotid artery branches are paramount for the diagnosis and treatment of vascular diseases of the brain, head, neck, and spine. In this chapter, common extracranial–intracranial anastomoses of the ophthalmic artery, internal carotid artery, and of the posterior circulation that are critical for the proceduralist to recognize in order to avoid complications during embolization procedures or open surgery are reviewed. Finally, the role of noninvasive imaging in the evaluation ofthecollateral circulationandcerebrovascularreserveinclinical conditionsassociatedwitharterial occlusivedisease isdiscussed. Keywords External carotid artery; Internal carotid artery; Anastomosis; Stroke; Collaterals; Angiography List of Abbreviations AP Anteroposterior CRA Central retinal artery ECA External carotid artery ICA Internal carotid artery MMA Middle meningeal artery OA Ophthalmic artery *Email:[email protected] *Email:[email protected] Page1of11 NeurovascularImaging DOI10.1007/978-1-4614-9212-2_1-1 #SpringerScience+BusinessMediaNewYork2014 Introduction Knowledge and identification of multiple anastomotic connections between the external carotid artery (ECA) and the internal carotid artery (ICA) branches are paramount for the diagnosis and treatmentofvasculardiseasesofthebrain,head,neck,andspine.Theexpandingroleofminimally invasive approaches for the treatment of cerebrovascular diseases, including arteriovenous malformations, fistulas, moyamoya disease, and other conditions, such as epistaxis and head and necktumors,requirescarefulexplorationofthearterial supplytothesestructurestoensuresuccess fromtheintervention.Inthischapter,commonextracranial–intracranialanastomosesthatarecritical fortheproceduralisttorecognizeinordertoavoidcomplicationsduringembolizationproceduresor open surgery are reviewed. The role of noninvasive imaging in the evaluation of the collateral circulation and cerebrovascular reserve in clinical conditions associated with arterial occlusive disease is discussed. The development of the cranial vascular supply during embryonic stages and a comprehensive review of all potential extracranial–intracranial anastomoses are beyond the scope of this chapter. Readers are referred to the classic work by Lasjaunias et al. [1] for a more detailed description of vascular anatomy on this subject. Ophthalmic Artery Anastomoses The ophthalmic artery (OA) most commonly arises from the paraclinoid segment of the ICA in adults.VariationsintheOAorigincanbeseenonangiography,suchasfromthecavernousportion of the ICA (the so-called “dorsal OA”), from the middle meningeal artery (MMA), or from the middle cerebral artery (MCA) [2–4]. The order and appearance of the OA branches depend on the course of this artery in relationship to the optic nerve [5]. The OA branches are commonly divided intothreegroups:ocular,orbital,andextraorbital.Theretinaandchoroidaresuppliedbythecentral retinal artery (CRA) and the ciliary arteries. Their visualization on angiography is critical to avoid occlusionoftheCRA,whichwillresultinmonocularblindness.TheCRAisthefirstbranchofthe OA, when the OA crosses above the optic nerve. When the OA crosses below the optic nerve, the lateralposteriorciliaryarteryoriginatesfromtheOAfirstandtheCRAsecond.Incasesinwhichthe CRAcannotbereliably identifiedondiagnostic angiographyandembolizationisplanned,provoc- ativetestingwithsuperselectiveinjectionofsodiumamobarbitalandlidocaineshouldbeconsidered to identify whether potential anastomoses to the eye exist at or distal to the site of microcatheter placement. Visualizationofachoroidalblush(bestappreciatedduringangiographyonlateralviewsasathin crescent of contrast material) on ECA injections should raise suspicion for potential anastomoses with the OA [6]. However, it should be noted that absence of the choroidal blush does not exclude the existence of such anastomoses. For example, when embolization is executed in the territory known to have potential connections with the OA, repeat diagnostic angiographic runs should be performed, as dangerous anastomoses might become visible only following occlusion of ECA branches with embolic agents. Identification of OA–MMA anastomoses can also help avoid visual complications in cranial base surgery, such as during resection of meningiomas [7]. AnisolatedOAoriginoftheMMAisarareanatomicvariant,especiallywhenpresentbilaterally [8,9].Insuchcases,theentireMMAorsomeofitsbranchesarenotvisualizedonaselectiveECA injection.AnICAinjectionwillopacifytheMMAinaslightlydelayedfashion,viatheproximalOA Page2of11 NeurovascularImaging DOI10.1007/978-1-4614-9212-2_1-1 #SpringerScience+BusinessMediaNewYork2014 Fig. 1 Ophthalmic origin of the middle meningeal artery. Cerebral angiogram, lateral projection, early (a) and late arterial phase (b)ofselectiveleftinternalcarotidarteryinjectiondemonstratereconstitution ofthemiddlemeningeal artery(whitearrows)viatheophthalmicartery(blackarrow)throughtherecurrentmeningealartery(blackarrowhead). (c) Notice that the middle meningeal artery does not opacify on the selective external carotid artery injection. sta superficialtemporalartery,imainternalmaxillaryartery through the superior orbital fissure (Fig. 1). Embolization of a lesion supplied by such anomalous meningeal vessels is challenging because of the high risk for emboli into OA branches, causing retinal ischemia [10]. Multiple anastomoses between branches of the ECA and OA exist, and only the most clinically relevantvariantswillbedescribedhere.Foramoredetailedreview,thearticlesbyHayreh[11]and Perrini et al. [5] are recommended. The recurrent meningeal artery is a critical anastomosis when attempting embolization of convexity meningiomas. It typically projects posteriorly to the OA through the superior orbital fissure. Anotherimportantgroupofanastomosesisbetweentheanteriorandposteriorethmoidalbranches of the OA and the distal branches of the internal maxillary artery, namely, the sphenopalatine and greater palatine arteries (Fig.2). The presence of suchanastomoses should beexplored on cerebral angiography when planning embolization for epistaxis [12]. AdditionalexamplesofpotentialanastomosesinvolvingtheOAincludethesuperficialtemporal artery branches such as the zygomatico-orbital artery, terminal nasal branches of the facial artery, and the infraorbital branch of the internal maxillary artery (Fig. 3). Extracranial–intracranial anastomoses have been described between the MMA, superficial temporal artery, occipital artery, and the cortical leptomeningeal arteries [13] (Fig. 4). Page3of11 NeurovascularImaging DOI10.1007/978-1-4614-9212-2_1-1 #SpringerScience+BusinessMediaNewYork2014 Fig. 2 Ophthalmic artery–internal maxillary artery anastomoses. Cerebral angiogram in a patient with chronic right internalcarotidarteryocclusion(asteriskonanteroposterior[AP]view),AP(a)andlateral(b)views,showsreconsti- tutionoftheophthalmicartery(whitearrows)throughtheanteriorandposteriorethmoidalbranches(blackarrowspoint tothenasalblushatthesiteofanastomoseswithinthenasalcavity).Whitearrowhead–infraorbitalarteryoftheinternal maxillaryartery.Blackarrowhead–cavernousinternalcarotidartery;imainternalmaxillaryartery Fig. 3 Superficial temporal artery anastomoses to the ophthalmic artery. Cerebral angiogram, AP (a) and lateral (b) views,showsopacificationoftheophthalmicartery(blackarrows)andthesupraclinoidinternalcarotidartery(black arrowheads)viathezygomatico-orbitalbranch(whitearrow)ofthesuperficialtemporalartery.Anotheranastomosis involvestheinfraorbitalbranch(whitearrowheads)oftheinternalmaxillaryartery(ima) Page4of11 NeurovascularImaging DOI10.1007/978-1-4614-9212-2_1-1 #SpringerScience+BusinessMediaNewYork2014 Fig.4 Corticalleptomeningealanastomoses.Cerebralangiogram,earlyarterialintracranialAP(a)andlateral(b)views andlatearterialintracranialAP(c)andlateral(d)views,showscorticalleptomeningealanastomosesbetweenthemiddle meningealartery(blackarrows)andthemiddlecerebralartery(whitearrows) Internal Carotid Artery Anastomoses ImportantanastomoseswithinthepetrocavernoussegmentoftheICAaredescribedbelow.Theycan often be identified on cerebral angiograms in cases of cervical ICA occlusion and are a critical component of dural arteriovenous malformations in this region. TheinferolateraltrunkisaremnantofthedorsalOAandconsistsofseveralbranchesthatprovide supplytothecranialnervesandthegasserianganglion.Anteroinferiorly,acharacteristicserpentine- like anastomosis with the maxillary artery through the artery of the foramen rotundum can be observed (Fig. 5). Other anastomoses include the recurrent artery of foramen lacerum (which connects with the ascending pharyngeal artery), branches of the MMA (seen laterally through the foramenspinosum),branchesoftheaccessorymeningealartery(seenposteriorly),andbranchesof the ascending pharyngeal artery (carotid branch of the superior pharyngeal branch through the foramen lacerum) (Fig. 6). A rare finding on cerebral angiography is hypertrophy of the vasa vasorum after complete occlusion of the cervical ICA [14] (Fig. 7). Extensive proliferation of the vasa vasorum can lead Page5of11 NeurovascularImaging DOI10.1007/978-1-4614-9212-2_1-1 #SpringerScience+BusinessMediaNewYork2014 Fig.5 Arteryofforamenrotundum.Cerebralangiogram,APview,demonstratesacharacteristicserpentine-likeartery of foramen rotundum (white arrows) directed at the base of the sella, which is an anastomosis between the internal maxillaryartery(ima)andthecavernoussegmentoftheinternalcarotidartery(blackarrow).oaophthalmicartery Fig. 6 Ascending pharyngeal artery anastomosis. Cerebral angiogram, AP(a) and lateral (b) views, shows a typical appearanceoftheascendingpharyngealartery.Thesuperiorpharyngealbranchofthepharyngealtrunk(whitearrows) givesoffthecarotidbranch,whichcreatesananastomosiswiththeinferolateraltrunk(notshown).ccacommoncarotid artery,fafacialartery,imainternalmaxillaryartery,oaoccipitalartery Page6of11 NeurovascularImaging DOI10.1007/978-1-4614-9212-2_1-1 #SpringerScience+BusinessMediaNewYork2014 Fig.7 Vasavasorumoftheinternalcarotidartery.Cerebralangiogram,cervicalAP(a)andlateral(b)viewsandcranial AP(c)andlateral(d)viewsinacaseofchroniccervicalleftinternalcarotidarteryocclusion.Thepetroussegmentofthe internalcarotidartery(blackarrows)reconstitutesviaaprominentnetworkofvasavasorum,whichappearastortuous channelsfollowingtheexpectedcourseofthecervicalinternalcarotidartery(whitearrows) toanterograderecanalizationoftheICAdistally,suchasatthelevelofthepetrocavernoussegment, and can be confused with anastomoses originating from the ascending pharyngeal artery. Visuali- zationoftortuousvascularchannelsthatprojectovertheexpectedcourseofthecervicalICArather than the ascending pharyngeal artery helps in differentiating the two conditions. The ascending pharyngeal artery typically originates from the posterior wall of the ECA trunk, although rarely its origin can be seen from the proximal cervical ICA. ThemeningohypophysealtrunkoftheICAsuppliesthepituitarygland,theclivalregion,andthe meninges of the tentorium. Through its tentorial branches, which are seen more anteriorly, it can form anastomoses with petrous branches of the MMA. Another common anastomosis of the Page7of11 NeurovascularImaging DOI10.1007/978-1-4614-9212-2_1-1 #SpringerScience+BusinessMediaNewYork2014 Fig. 8 Occipital artery–vertebral artery anastomosis. Cerebral angiogram, lateral view, selective occipital artery (oa) injection, demonstrates opacification of the vertebrobasilar system (white arrows) via the C1 segmental artery (blackarrow) meningohypophyseal trunk involves its lateral clival artery and neuromeningeal branches of the ascending pharyngeal artery. Posterior Circulation Anastomoses Early during embryologic development of the central nervous system, the posterior circulation forms primitive anastomoses with the ICAs (the trigeminal, otic, hypoglossal, and proatlantal connections) that eventually disappear, except for the posterior communicating arteries, which remain in adults. The most common anastomosis involves the occipital artery and the vertebral artery connecting at the C1 or C2 segmental levels (Fig. 8). Other examples of anastomotic connections with the vertebral artery include the ascending pharyngeal artery and the ascending cervical and deep cervical arteries. Noninvasive Imaging Modalities Catheter angiography remains the gold standard for the identification of specific anastomotic connections between the ECA and ICA branches because of its excellent spatial resolution and the proceduralist’s ability to perform superselective catheterization of individual vessels. Noninva- sive imaging can beusedin clinical practice asaway toestimate the ability of suchconnections to provide adequate cerebral blood flow in conditions such as occlusive disease of the ICA and the vertebrobasilar system and moyamoya disease. Measurement of cerebrovascular reserve can help predictstrokeriskinpatientswithcarotidstenosisorocclusion,basedonameta-analysisofstudies evaluating cerebrovascular reserve impairment [15]. The techniques used most commonly to evaluate cerebrovascular reserve include computed tomographicandmagneticresonanceperfusionimaging,single-photonemissioncomputedtomog- raphy, and positron emission tomography [16–20] (Fig. 9). Systemic administration of cerebral Page8of11 NeurovascularImaging DOI10.1007/978-1-4614-9212-2_1-1 #SpringerScience+BusinessMediaNewYork2014 Fig.9 Watershedperfusiondeficit.Inapatientwithchronicocclusivediseaseoftheleftinternalcarotidartery,thereisa perfusiondeficitintheanteriorcerebralartery(ACA)–middlecerebralarterywatershedterritory(indicatedbydotted lines) Fig.10 Acetazolamidechallenge.(a)Inapatientwithchronicrightinternalcarotidarteryocclusion,thereisdecreased cerebral blood flow in the right internal carotid artery territory, in comparison to the contralateral side. (b) A robust increaseincerebralbloodflowwithintherighthemisphereisseenafteradministrationofacetazolamide,indicatinggood cerebrovascularreserve Page9of11 NeurovascularImaging DOI10.1007/978-1-4614-9212-2_1-1 #SpringerScience+BusinessMediaNewYork2014 vasodilator agents that can cross the blood–brain barrier, such as acetazolamide, allows the calcu- lationofchangesincerebralbloodflowandvisualizationofreactivityinspecificvascularterritories in which vasoocclusive disease is present [21] (Fig. 10). Arterial spin-labeling magnetic resonance imaging is another technique that can assess temporal dynamics of arterial blood inflow and identify brain regions with impaired hemodynamics [18, 22, 23].ItcanbeusedtovisualizetheperfusionterritoryoftheECAinordertodepictthestatusofthe collateral circulation and quantitatively compare flow pre- and postoperatively [23]. Summary To ensure success and safety when treating cerebrovascular diseases of the head and neck, proceduralists should be aware of dangerous extracranial–intracranial carotid arterial anastomoses, which are highly variable in their appearance and location. Catheter angiography remains the gold standard for the identification of such anastomotic routes and should be carefully reviewed before performing embolization of arteriovenous malformations, tumors, or epistaxis. Noninvasive imag- ing can estimate the ability of such connections to provide adequate cerebral blood flow in conditions such as occlusive disease of the ICA and the vertebrobasilar system. References 1. LasjauniasP,BerensteinA,terBruggeK(2001)Surgicalneuroangiography:1clinicalvascular anatomy and variations. Springer, Berlin 2. Sade B, Tampieri D, Mohr G (2004) Ophthalmic artery originating from basilar artery: a rare variant. AJNR Am J Neuroradiol 25:1730–1731 3. 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Plas B, Bonneville F, Dupuy M, Sol JC, Chaynes P (2013) Bilateral ophthalmic origin of the middle meningeal artery. Neurochirurgie 59:183–186 9. Royle G, Motson R (1973) An anomalous origin of the middle meningeal artery. J Neurol Neurosurg Psychiatry 36:874–876 10. Trivelatto F, Nakiri GS, Manisor M, Riva R, Al-Khawaldeh M, Kessler I, Mounayer C (2011) Preoperative onyx embolization of meningiomas fed by the ophthalmic artery: a case series. AJNR Am J Neuroradiol 32:1762–1766 11. Hayreh SS (2006) Orbital vascular anatomy. Eye (Lond) 20:1130–1144 Page10of11