microsurgical anatomy of cerebral revascularization. part ... et al 2.pdfanterior, middle,...

LTHOUGH the usefulness of cerebral revasculariza-tion for intracranial arteriosclerotic diseases in theanterior circulation has been denied, investigators in

the Cooperative Study of Extracranial–Intracranial ArterialAnastomosis17 have made no reference to the use of cerebralrevascularization for intracranial arteriosclerotic diseases inthe posterior circulation. No randomized trial of cerebral re-vascularization to treat stenoocclusive disease in the poste-rior circulation has been performed. Therefore, the efficacyof this procedure for arteriosclerotic diseases remains un-determined. Nevertheless, cerebral revascularization in theposterior circulation is now well recognized as an impor-tant component in the treatment of complex and giant intra-cranial aneurysms, especially when they involve dominantvessels in that location.

In this study, we examined the microsurgical anatomy as-sociated with cerebral revascularization in the posterior cir-culation and demonstrated various procedures used for by-pass surgery.

Materials and MethodsThe microsurgical anatomy associated with cerebral revascular-

ization, including the donor and recipient vessels and the techniquesof revascularization, encompassing extracranial–intracranial bypassgrafting (STA–PCA, ECA–PCA, STA–SCA, OA–AICA, and OA–PICA anastomoses), arterial interposition grafting (OA–PICA anas-tomosis), and side-to-side anastomosis (PICA–PICA anastomosis),were examined in stepwise dissections performed in 22 adult ca-daveric specimens by using 3 to 403 magnification. Depending onthe thickness of the vessel wall, 10-0, 8-0, 7-0, or 6-0 nylon threads(Ethicon, Inc., Somerville, NJ) were used for suturing. The arteriesand veins of the specimens were perfused with colored silicone.Bone dissections were performed using a Midas Rex drill (FortWorth, TX).

ResultsArterial Relationships

Table 1 shows the diameters of vessels that are frequent-ly used for cerebral revascularization procedures.

J Neurosurg 102:132–147, 2005

132

Microsurgical anatomy of cerebral revascularization. Part II:Posterior circulation

MASATOU KAWASHIMA, M.D., PH.D., ALBERT L. RHOTON JR., M.D.,NECMETTIN TANRIOVER, M.D., ARTHUR J. ULM, M.D., ALEXANDRE YASUDA, M.D.,AND KIYOTAKA FUJII, M.D., PH.D.

Department of Neurological Surgery, University of Florida, Gainesville, Florida; and Department ofNeurosurgery, Kitasato University, School of Medicine, Kanagawa, Japan

Object. Revascularization is an important component of treatment for complex aneurysms, skull base tumors, and verte-brobasilar ischemia in the posterior circulation. In this study, the authors examined the microsurgical anatomy related tocerebral revascularization in the posterior circulation and demonstrate various procedures for bypass surgery.

Methods. The microsurgical anatomy of cerebral and cerebellar vessels as they relate to revascularization procedure andtechniques, including extracranial-to-intracranial bypass grafting, arterial interposition grafting, and side-to-side anastomo-sis, were examined by performing stepwise dissections in 22 adult cadaveric specimens. The arteries and veins in the spec-imens were perfused with colored silicone.

Dominant cerebral and cerebellar revascularization procedures in the posterior circulations include superficial temporalartery (STA)–posterior cerebral artery (PCA), STA–superior cerebellar artery (SCA), occipital artery (OA)–anterior infe-rior cerebellar artery, OA–posterior inferior cerebellar artery (PICA), and PICA–PICA anastomoses. These procedures areeffective in relatively small but critical areas including the brainstem and cerebellum. For revascularization of larger areasa saphenous vein graft is used to create a bypass between the PCA and the external carotid artery. Surgical procedures aregenerally difficult to perform in deep and narrow operative spaces near critical vital structures.

Conclusions. Although a clear guideline for cerebral revascularization procedures has not yet been established, it is im-portant to understand various microsurgical techniques and their related anatomical structures. This will help surgeons con-sider surgical indications for treatment of patients with vertebrobasilar ischemia caused by aneurysms, tumors, or athero-sclerotic diseases in the posterior circulation.

KEY WORDS • microsurgical anatomy • cerebral revascularization • posterior circulation •bypass surgery

A

J. Neurosurg. / Volume 102 / January, 2005

Abbreviations used in this paper: AICA = anterior inferior ce-rebellar artery; BA = basilar artery; CBF = cerebral blood flow;CCA = common carotid artery; ECA = external carotid artery;ICA = internal carotid artery; OA = occipital artery; PCA = posteri-or cerebral artery; PCoA = posterior communicating artery; PICA =posterior inferior cerebellar artery; RA = radial artery; SCA = supe-rior cerebellar artery; STA = superficial temporal artery; VA = ver-tebral artery.

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Posterior Cerebral Artery

The PCA arises at the basilar bifurcation, is joined by thePCoA at the lateral margin of the interpeduncular cistern,encircles the brainstem as it passes through the crural andambient cisterns to reach the quadrigeminal cistern, and isdistributed to the posterior portion of the hemisphere. ThePCA not only supplies the posterior portion of the cerebralhemispheres, but also sends critical branches to the thala-mus, midbrain, and other deeply situated structures, includ-ing the choroid plexus and the walls of the lateral and thirdventricles. Each segment of the PCA is classified accordingto our already proposed system.64 The P1 segment is prox-imal to the PCoA. The P2 segment extends from the PCoAto the point at which the PCA enters the quadrigeminal cis-tern. The P2 segment is subdivided into equal parts: anteri-or (P2A) and posterior (P2P). The P2A segment begins at thePCoA and courses between the cerebral peduncle and un-cus, which form the medial and lateral walls of the cruralcistern, and then extends inferior to the optic tract and thebasal vein, which crosses the roof of the cistern, to enter theproximal portion of the ambient cistern. The P2P begins atthe posterior edge of the cerebral peduncle, at the junctionof the crural and ambient cisterns. It courses between thelateral midbrain and the parahippocampal and dentate gyri,which form the medial and lateral walls of the ambient cis-tern, to below the optic tract, basal vein, and geniculate bod-ies and the inferolateral portion of the pulvinar in the roof ofthe cistern, and superomedial to the trochlear nerve and ten-torial edge. The P3 segment begins at the posterior midbrain,courses within the quadrigeminal cistern, and ends at theanterior limit of the calcarine fissure. The P4 segment is thedistal branch of the P3 segment. In this study mean diame-ters of the P2A, P2P, and P3 were 2.13, 1.73, and 1.67 mm, re-spectively (Table 1). The PCA gives rise to three types ofbranches: 1) central perforating branches to the dienceph-alon and midbrain; 2) ventricular branches to the choroidplexus and walls of the lateral and third ventricles and ad-jacent structures; and 3) cerebral branches to the cerebralcortex and the splenium of the corpus callosum. The centralbranches include the direct and circumflex perforating arter-ies, including the thalamoperforating, peduncular perforat-ing, and thalamogeniculate arteries. The ventricular branch-es are the lateral and medial posterior choroidal arteries.The cerebral branches include the inferior temporal groupof branches, which are divided into the hippocampal and theanterior, middle, posterior, and common temporal branches,plus the parietooccipital, calcarine, and splenial branches.The long and short circumflex, thalamoperforating, and me-dial posterior choroidal arteries arise predominantly fromthe P1 segment, and the other PCA branches most frequent-ly arise from the P2 or P3 segment. The hippocampal, ante-rior temporal, peduncular perforating, and medial posteriorchoroidal arteries most frequently arise from the P2A seg-ment; and the middle temporal, posterior temporal, com-mon temporal, and lateral posterior choroidal arteries mostfrequently arise from the P2P segment. The thalamogenicu-late arteries are only slightly more frequently found to arisefrom the P2P segment than from the P2A segment. The cal-carine and parietooccipital arteries most frequently arisefrom the P3 segment (Fig. 1A and B).

Superior Cerebellar Artery

The SCA arises in front of the midbrain, usually from the

BA near the apex, and passes below the oculomotor nerve.Its proximal portion courses medial to the free edge of thetentorium cerebelli around the brainstem near the ponto-mesencephalic junction, and its distal portion passes belowthe tentorium, making it the most rostral of the infratentori-al arteries. All SCAs that arise as a single vessel bifurcateinto two major trunks—one rostral and one caudal—mostcommonly near the point of maximal caudal descent of theartery on the lateral side of the brainstem. The SCA is divid-ed into four segments: anterior pontomesencephalic, lateralpontomesencephalic, cerebellomesencephalic, and cortical.The anterior pontomesencephalic segment begins at the ori-gin of the SCA and extends below the oculomotor nerve tothe anterolateral margin of the brainstem. In this study themean diameter of the vessel in that segment was 1.67 mm(Table 1). The lateral pontomesencephalic segment beginsat the anterolateral margin of the brainstem and frequentlydips caudally onto the lateral side of the pons. This segmentterminates at the anterior margin of the cerebellomesen-cephalic fissure. The mean diameters of the rostral and cau-dal trunks in this segment were 1.25 and 1.15 mm, respec-tively. In cadavers in which there was a single trunk, themean diameter of this segment was 1.51 mm (Table 1). Thecerebellomesencephalic segment courses within the cere-bellomesencephalic fissure, giving rise to branches thatpenetrate the fissure’s opposing walls. The cortical segmentincludes branches distal to the cerebellomesencephalic fis-sure that pass under the tentorial edge and are distributed tothe tentorial surface (Fig. 1B–D).

Anterior Inferior Cerebellar Artery

The AICA originates from the BA, usually as a singletrunk, and encircles the pons near the abducent, facial, andvestibulocochlear nerves. After coursing near and sendingbranches to nerves entering the acoustic meatus and to thechoroid plexus protruding from the foramen of Luschka, theAICA passes around the flocculus on the middle cerebel-lar peduncle to supply the cerebellopontine fissure and the


Cerebral revascularization: posterior circulation

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TABLE 1Diameters of arteries frequently used for cerebral

revascularization procedures in the posterior circulation*

Artery Mean Diameter (mm)

PCAP2A segment 2.13 6 0.38P2P segment 1.73 6 0.33P3 segment 1.67 6 0.16

SCAant pontomesencephalic segment 1.67 6 0.16lat pontomesencephalic segment

single trunk 1.51 6 0.12rostral trunk 1.25 6 0.17caudal trunk 1.15 6 0.30

AICAant pontomesencephalic segment 1.34 6 0.28cortical segment 1.07 6 0.29

PICAant medullary segment 1.84 6 0.45tonsillomedullary segment (caudal loop) 1.68 6 0.38

OAat digastric groove 2.05 6 0.48at level of the superior nuchal line 2.01 6 0.45

* Values are expressed as means 6 standard deviations.

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134 J. Neurosurg. / Volume 102 / January, 2005

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petrosal surface. It commonly bifurcates near the facial–vestibulocochlear nerve complex to form rostral and caudaltrunks. The AICA is divided into four segments: anteriorpontine, lateral pontine, flocculonodular, and cortical. Eachsegment may include more than one trunk, depending onthe level of bifurcation of the artery. In this study the meandiameters of the anterior pontine and cortical segmentswere 1.34 and 1.07 mm, respectively (Table 1). The mostcommon pattern is for the AICA to supply the majority of

the petrosal surface; however, overlapping of the SCA onthe upper portion of the petrosal surface and overlapping ofthe PICA on the lateral portion of the suboccipital surfaceare not uncommon, depending on the size of the AICA (Fig.1C and D).

Posterior Inferior Cerebellar Artery

The PICA has the most complex, tortuous, and variablecourse of the cerebellar arteries. This vessel arises from theVA near the inferior olive and passes posteriorly aroundthe medulla oblongata. After it passes the lateral aspect ofthe medulla, the PICA courses around the cerebellar tonsil,enters the cerebellomedullary fissure, and passes posteriorto the lower half of the roof of the fourth ventricle. On ex-iting the cerebellomedullary fissure, the branches of thePICA are distributed to the vermis and the suboccipital sur-face of the hemisphere. Most PICAs bifurcate into medi-al and lateral trunks. The medial trunk supplies the vermisand the adjacent portion of the hemisphere, and the later-al trunk supplies the cortical surface of the tonsil and thehemisphere. The PICA is divided into five segments: ante-rior medullary, lateral medullary, tonsillomedullary, telo-velotonsillar, and cortical. The anterior medullary segmentbegins at the origin of the PICA, anterior to the medulla ob-longata, and extends backward to the inferior olivary prom-inence, passing near the hypoglossal rootlets. The lateralmedullary segment begins at the site where the artery pass-es the most prominent point of the inferior olive and ends atthe level of the origin of the glossopharyngeal, vagus, andaccessory rootlets. The tonsillomedullary segment begins atthe point at which the PICA passes posterior to the glosso-pharyngeal, vagus, and accessory nerves and extends medi-ally across the posterior aspect of the medulla, near the cau-dal half of the tonsil. It ends at the point at which the arteryascends to the midlevel of the medial surface of the tonsil.This segment commonly passes medially between the lowermargin of the tonsil and the medulla oblongata before turn-ing rostrally along the medial surface of the tonsil. The looppassing near the lower part of the tonsil, referred to as thecaudal loop, forms a caudally convex loop that coincideswith the caudal pole of the tonsil, but it may also course su-periorly or inferiorly with respect to the caudal pole of thetonsil without forming a loop. In our investigation the meandiameter of the caudal loop, which is one of the largest dis-tal vessels in the cerebellar arteries, was 1.68 mm (Table 1).The telovelotonsillar segment begins at the midportion ofthe PICA’s ascent along the medial surface of the tonsiltoward the roof of the fourth ventricle and ends at the pointat which the PICA exits the fissures between the vermis andtonsil on one side and the hemisphere on the other side toreach the suboccipital surface. This segment commonlyforms a loop with a convex rostral curve, called the crani-al loop. The apex of the cranial loop usually overlies thecentral portion of the inferior medullary velum, but its loca-tion varies from the superior to the inferior margin and fromthe medial to the lateral boundary of the inferior medullaryvelum. The cortical segment begins at the site where thetrunks and branches leave the groove between the vermisand tonsil medially and the hemisphere laterally, and in-cludes the terminal cortical branches (Fig. 1C–F).

Occipital Artery

The OA arises from the posterior portion of the ECA, op-



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FIG. 1. Photographs obtained in cadaveric specimens, showingarterial relationships. A and B: Inferior and anterosuperior viewsof the PCA. This artery arises at the basilar bifurcation, is joined bythe PCoA at the lateral margin of the interpeduncular cistern, encir-cles the brainstem passing through the crural and ambient cisternsto reach the quadrigeminal cistern above the edge of the cerebellartentorium, and is distributed to the posterior portion of the hemi-sphere. The PCA is divided into segments P1 to P4. The artery givesrise to three types of branches: 1) central perforating branches to thediencephalon and midbrain; 2) ventricular branches to the choroidplexus and walls of the lateral and third ventricles and adjacentstructures; and 3) cerebral branches to the cerebral cortex and thesplenium of the corpus callosum. C and D: Anterolateral and ante-rior views of the brainstem and the cerebellum, SCA, AICA, andPICA. The SCA arises in front of the midbrain, usually from the BAnear the apex, and passes below the oculomotor nerve. Its proximalportion courses medial with regard to the free edge of the tentoriumcerebelli around the brainstem near the pontomesencephalic junc-tion, and its distal portion passes below the tentorium, making it themost rostral of the infratentorial arteries. All the SCAs that arise asa single vessel bifurcate into two major trunks—one rostral and onecaudal—most commonly near the point of maximal caudal descentof the artery on the lateral side of the brainstem (see panel B). TheAICA originates from the BA, usually as a single trunk, and en-circles the pons near the abducent, facial, and vestibulocochlearnerves. After coursing near and sending branches to nerves enteringthe acoustic meatus and to the choroid plexus protruding from theforamen of Luschka, the AICA passes around the flocculus on themiddle cerebellar peduncle to supply the cerebellopontine fissureand the petrosal surface. The PICA arises from the VA near the infe-rior olive and passes posteriorly around the medulla oblongata. Eand F: Posterior and posterolateral views of the brainstem, cerebel-lum, and PICA. After passing the lateral aspect of the medulla ob-longata, the PICA courses around the cerebellar tonsil, enters thecerebellomedullary fissure, and passes posterior to the lower halfof the roof of the fourth ventricle. On exiting the cerebellomedul-lary fissure, the PICA’s branches are distributed to the vermis andthe suboccipital surface of the hemisphere. In the tonsillomedullarysegment of the PICA, the loop passing near the lower portion of thetonsil, referred to as the caudal loop, forms a caudally convex loopthat coincides with the caudal pole of the tonsil. The PICA may alsocourse superior or inferior to the caudal pole of the tonsil withoutforming a loop. The telovelotonsillar segment commonly forms aloop with a convex rostral curve called the cranial loop. The apex ofthe cranial loop usually overlies the central portion of the inferiormedullary velum. A. = artery; A.Ch.A. = anterior choroidal artery;A.I.C.A. = interior inferior cerebellar artery; Bas. = basilar; Caud. =caudal; Chor. Plex. = choroid plexus; CN = cranial nerve; Cond. =condylar; Fiss. = fissure; Horiz. = horizontal; L.P.Ch.A. = lateralposterior choroidal artery; M.P.Ch.A. = medial posterior choroidalartery; P.C.A. = posterior cerebral artery; P.Co.A. = posterior com-municating artery; Pet. = petrosal; P.I.C.A. = posterior inferior cere-bellar artery; Post. = posterior; P1, P2A, P2P, P3 = segments andsubsegments of the PCA; Rost. = rostral; S.C.A. = superior cerebel-lar artery; Str. = straight; Suboccip. = suboccipital; Sup. = superior;Tent. = tentorial; Tr. = trunk; Trans. = transverse; V. = vein; Ver. orVert. = vertebral.

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FIG. 2. Graft extraction. Photographs of cadaveric specimens,showing right posterior and posterolateral views of the OA. The OAarises from the posterior portion of the ECA and ends in the posteriorportion of the scalp. The OA ascends to the area between the trans-verse process of the atlas and the mastoid process of the temporal bone,and passes horizontally backward, grooving the surface of the mastoidbone, because the vessel is covered by the sternocleidomastoid andsplenius capitis muscles, and resting on the superior oblique and semi-spinalis capitis muscles. The OA then changes its course and runs ver-tically upward, pierces the fascia connecting the cranial attachment ofthe trapezius muscle with the sternocleidomastoid muscle, and ascendsin a tortuous course in the superficial fascia of the scalp, where it di-vides into numerous branches that reach as high as the vertex of theskull and anastomose with the posterior auricular artery and the STA.The terminal portion of the OA is accompanied by the greater occipi-tal nerve. Cap. = capitis; C2 = C-2 vertebra; Gr. = great; Inf. = inferi-or; M. = muscle; Maj. = major; N. = nerve; Obl. = oblique; Occip. =occipital; Rec. = rectus; Sag. = sagittal; Semispin. = semispinalis;Splen. = splenius; Sternocleidomast. = sternocleidomastoid.

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posite the external maxillary artery and near the lower mar-gin of the posterior belly of the digastric muscle, and endsin the posterior portion of the scalp. At its origin, the OAis covered by the posterior belly of the digastric muscleand the stylohyoid muscles. The hypoglossal nerve windsaround this artery from behind and forward. Higher, the OAcrosses the ICA, the internal jugular vein, and the vagusand accessory nerves. The OA ascends to the side betweenthe transverse process of the atlas and the mastoid processof the temporal bone and passes horizontally backward,grooving the surface of the mastoid process, because thevessel is covered by the sternocleidomastoid, splenius capi-tis, longissimus capitis, and digastric muscles, and restingon the rectus capitis lateralis, superior oblique, and semispi-nalis capitis muscles. In this study the mean diameter of theOA was 2.05 mm at its exit from the digastric groove (Ta-ble 1). There the OA changes course and runs vertically up-ward, pierces the fascia connecting the cranial attachmentof the trapezius and sternocleidomastoid muscles, and as-cends in a tortuous course in the superficial fascia of thescalp, where it divides into numerous branches that reach ashigh as the vertex of the skull and anastomose with the pos-terior auricular artery and the STA. In this study the meandiameter of the OA was 2.01 mm at the level of the supe-rior nuchal line (Table 1). The length of the OA from itsexit from the digastric groove to the level of the superiornuchal line was measured in three specimens (four sides).The mean length of this segment was 81.9 mm. Its termi-nal portion is accompanied by the greater occipital nerve(Fig. 2).

Superficial Temporal Artery

The STA, the smaller of the two terminal branches of theECA, appears, from its direction, to be the continuation ofthat vessel. The STA begins in the substance of the parotidgland, behind the neck of the mandible, and crosses over theposterior root of the zygomatic process of the temporalbone. The STA divides into two branches: frontal and pari-etal. The frontal branch (anterior temporal) runs tortuouslyupward and forward to the forehead, supplying the muscles,integument, and pericranium in this region and anastomos-ing with the supraorbital and frontal arteries. The parietalbranch (posterior temporal) is larger than the frontal branchand curves upward and backward on the side of the head,lying superficial to the temporal fascia and anastomosingwith its contralateral counterpart as well as with the posteri-or auricular and occipital arteries.

Procedures for Cerebral Revascularization

The STA–PCA Anastomosis. This anastomosis is per-formed via a subtemporal route. After positioning the tem-ple region flat on the table, the STA is outlined either bypalpation or by using a portable Doppler device. Once dis-section of the STA has been completed, the temporal mus-cle and fascia are incised at the site of the craniotomy forthe subtemporal approach. After the dura mater has beenopened, the temporal lobe is elevated until the tentorial edgeis identified. Care should be taken not to damage the veinof Labbé or the posterior temporal veins as they enter thetransverse sinus. The PCA is dissected free from the arach-noid as the vessel courses around the cerebral peduncle. Itis not necessary to expose the P1 segment of the PCA. The

segment of the vessel that is isolated for temporary occlu-sion is the P2A. A portion of the P2A segment, approximately1.5 cm in length and having no perforating vessels, is select-ed for the anastomosis. Care should be taken to avoid dam-aging vessels that pass near the anastomotic site, includingthe long and short circumflex, thalamoperforating, medialand lateral posterior choroidal, hippocampal, anterior tem-poral, middle temporal, posterior temporal, common tem-poral, and peduncular perforating arteries. It may be diffi-cult to see the PCA in the center of the operative field whenthe artery courses the upper portion of the cistern around thebrainstem. Nevertheless, excess retraction of the temporallobe should be avoided to protect the temporal lobe and thebridging veins. After the PCA has been exposed, the sev-ered end of the STA is stripped of its fascial layer and a7- to 8-mm portion of the vessel is exposed. The tip of theSTA is then cut into a shape that is suitable for the anas-tomotic site. The recipient vessel is prepared by placingtemporary clips across the vessel and performing a smallarteriotomy. After two stay sutures have been placed, anas-tomosis of the STA to the recipient vessel is performed us-ing 10-0 nylon interrupted sutures (Fig. 3A–C).

The ECA–PCA Anastomosis. Either a saphenous vein graftor an RA graft is used for this bypass procedure. The CCA,ICA, and ECA are exposed in the carotid triangle by mak-ing a cervical incision along the anterior aspect of the ster-nocleidomastoid muscle. The zygomatic arch is drilled tofashion a conduit for the graft when it is placed in the preau-ricular position. After a craniotomy has been performed forthe subtemporal approach, dissection of the P2 segment ofthe PCA is performed through the subtemporal route. TheP2 segment, which is thick and has the least number of sidebranches, is chosen and mobilized for the anastomosis. Careshould be taken to avoid damaging the perforating arteries.The distal anastomosis between the P2 segment and the graftis performed in an end-to-side fashion by using interrupted8-0 nylon sutures. After completion of the distal anasto-mosis, the cervical ECA is occluded proximally and distal-ly. The graft is then pulled down through the subcutaneoustunnel. An arteriotomy, approximately 6 to 8 mm long, ismade on the ECA. The graft is anastomosed to the artery inan end-to-side fashion by using 6-0 nylon sutures (Fig. 3Dand E).

The STA–SCA Anastomosis. The STA–SCA anastomosisis performed in the same operative view as described for theSTA–PCA anastomosis. After dissection of the STA hasbeen completed, the tentorial edge is identified through thesubtemporal space. The edge of the tentorium is elevat-ed and sectioned to provide more exposure. The flap of thetentorium is retracted and reflected, and it is anchored to amore lateral aspect of the tentorium. Care is taken not todamage the fourth cranial nerve, which courses beneath thetentorial edge. The SCA is then identified in its lateral pon-tomesencephalic segment. The artery usually has no perfo-rating branches because it courses from the lateral portionof the midbrain to the superior portion of the cerebellum. Ifthere are branches to the brainstem, a portion of the SCAbeyond the area containing the brainstem branch is selectedfor the anastomosis. Because the SCA frequently divides in-to rostral and caudal branches in this segment, the larger ofthe two branches is used for the anastomosis. After the SCAhas been exposed, the severed end of this vessel is stripped



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FIG. 3. Photographs of cadaveric specimens demonstrating an STA–PCA anastomosis on the right side (A–C) and an ECA–PCA anastomo-sis on the left side performed using a saphenous vein graft (D and E). A: The STA–PCA anastomosis is performed via the subtemporal route.After the dura mater has been opened, the temporal lobe is elevated until the tentorial edge is identified. Care should be taken not to damagethe vein of Labbé or the posterior temporal veins as they enter the transverse sinus. The tentorial edge has been removed to expose the SCAand the fourth cranial nerve. The PCA is dissected free from the arachnoid as it courses around the cerebral peduncle. The portion of the ves-sel that is isolated for temporary occlusion is the P2A segment of the PCA. A portion of this segment, approximately 1.5 cm in length and hav-ing no perforating vessels, is selected for the anastomosis. Care should be taken to preserve vessels passing near the anastomotic site, includ-ing the long and short circumflex, thalamoperforating, medial and lateral posterior choroidal, (FIG. 3. continued��

)

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of its fascial layer and a 7- to 8-mm portion of the vessel isexposed. The tip of the STA is then cut into a shape that issuitable for the anastomotic site. The recipient vessel is pre-pared by placing temporary clips across the vessel and per-forming a small arteriotomy equal in length to one preparedon the SCA. After two stay sutures have been placed, anas-tomosis of the STA to the recipient vessel is performed us-ing 10-0 nylon interrupted sutures (Fig. 4).

The OA–AICA Anastomosis. The course of the OA shouldbe outlined on the scalp by using a portable Doppler de-vice. The OA can be dissected from its point of penetrationthrough the occipital muscle to its most distal appearance. Itis important to dissect a sufficiently long piece of the OA tobe able to reach the cerebellar arteries; therefore, the dissec-tion may need to extend to the level of the mastoid process.This dissection is generally difficult because the OA is moretortuous and lies deeper than the STA. The OA is gently re-tracted off the field, and a lateral suboccipital craniotomy iscompleted from the foramen magnum to the transverse si-nus and from the edge of the mastoid process to the midline.Generally, removal of the arch of C-1 is not necessary. Afterthe dura mater has been opened, the suboccipital surfaceof the cerebellum can be seen. Using careful retraction ofthe cerebellum laterally, the AICA in the petrous surface ismade visible (Fig. 5A). Anastomosis to the proximal por-tion of the AICA near the BA would require continuouscompression of the cerebellum, compromising the collat-eral branches between the AICA and PICA or the AICAand SCA. Therefore, the flocculonodular (Fig. 5B and C) orcortical (Fig. 5D and E) segment of the AICA, distal to thefacial–vestibulocochlear nerve complex, is selected for theanastomosis. The vessel is freed from the petrous surface ofthe cerebellum and is isolated. After the AICA has been ex-posed, the severed end of the OA is stripped of its fasciallayer and a 7- to 8-mm portion of the vessel is exposed. Thetip of the OA is cut into a shape that is suitable for the anas-tomotic site. The recipient vessel is prepared by placing

temporary clips across the vessel and performing a small ar-teriotomy that is equal in length to the one prepared on theAICA. After two stay sutures have been placed, anastomo-sis of the OA to the recipient vessel is performed using 10-0 nylon interrupted sutures. Generally, the anastomosis pro-cedure performed for the AICA is more difficult than thatfor the PICA because of the depth of the operative field andthe smaller diameter of the recipient vessel.

The OA–PICA Anastomosis. After dissection of the OAhas been completed, a suboccipital craniotomy is performedin the manner described for the OA–AICA anastomosis.The arch of C-1 is removed, if needed. After the dura materhas been opened, the caudal loop of the PICA is exposed.The vessel is freed from the arachnoid. After the PICA hasbeen exposed, the severed end of the OA is stripped of itsfascial layer, and a 7- to 8-mm portion of the vessel is ex-posed. The tip of the OA is cut into a shape that is suitablefor the anastomotic site. The recipient vessel is prepared byplacing temporary clips across the vessel and performing asmall arteriotomy equal in length to one prepared on thePICA. After two stay sutures have been placed, anastomo-sis of the OA to the recipient vessel is performed using 10-0 nylon interrupted sutures (Fig. 6A–C).

Short Arterial Interposition Graft Anastomosis. The STA orOA is used for an arterial graft. The OA–AICA, OA–PICA,or VA–PICA anastomosis can be performed using an inter-position graft. A section of STA or OA graft material, ap-proximately 8 cm long, is dissected from a skin flap andboth severed ends of the donor vessel are stripped of the fas-cial layer. For an OA–PICA anastomosis the graft is placedbetween the OA and the caudal loop of the PICA and at-tached using 10-0 nylon interrupted sutures (Fig. 6D and E).

Side-to-Side Anastomosis of the PICA. This procedure ischiefly used for cerebral revascularization of the distal por-tion of the PICA after occlusion of its proximal portion. Theproximity and parallel courses of the tonsillomedullary andthe telovelotonsillar segments of the PICAs permit side-to-side anastomosis. Arteriotomies, 4 mm in length, are madein both donor and recipient arteries. The most difficult pro-cedure is to make a tight suture on a back wall. After twostay sutures have been placed, the back wall is sutured in acontinuous running fashion from the intravascular side andthe anterior wall is closed with interrupted sutures (10-0 ny-lon). The distal portion of the artery beyond the occlusionsite is supplied by the adjacent artery (Fig. 7).

End-to-End Anastomosis of the PICA. The diseased PICAsegment that is involved with a tumor or aneurysm can beexcised, and the remaining portions of the vessel can bedirectly reattached in an end-to-end fashion. The proximaland distal stumps of the PICA are anastomosed using inter-rupted sutures (10-0 nylon), unless the difference betweenthe diameters of the stumps is greater than 10 mm.

Discussion

In this study, we have shown various intracranial cere-bral revascularization procedures in the posterior circula-tion, which are considered to be routine neurosurgical tech-niques. We have also described the microsurgical anatomyof vessels related to these procedures. A variety of re-vascularization procedures associated with extracranial VA



139

hippocampal, anterior temporal, middle temporal, posterior tempo-ral, common temporal, and peduncular perforating arteries. Excessretraction of the temporal lobe should be avoided to protect the tem-poral lobe and the bridging veins. B and C: After the PCA hasbeen exposed, the severed end of the STA is stripped of its fasciallayer and a 7- to 8-mm portion of the vessel is exposed. The tip ofthe STA is then cut into a shape that is suitable for the anastomoticsite. The recipient vessel is prepared by placing temporary clipsacross the vessel and performing a small arteriotomy. After placingtwo stay sutures, anastomosis of the STA to the recipient vessel isperformed using 10-0 nylon interrupted sutures (arrowheads). D:Either a saphenous vein graft or an RA graft is used for this bypassprocedure. After a craniotomy was performed for the subtemporalapproach, the P2 segment of the PCA, which is thick and has theleast number of side branches, is chosen and mobilized for the anas-tomosis. The distal anastomosis between the P2 segment and thegraft is then performed in an end-to-side fashion by using inter-rupted sutures (upper inset, arrowhead). After completion of thedistal anastomosis, the graft is pulled down through the subcutane-ous tunnel. An arteriotomy, approximately 6 to 8 mm long, is madeon the ECA. The graft is anastomosed to the artery in an end-to-sidefashion (lower inset, arrowhead). E: The graft is anastomosed tothe P2 segment (arrowhead). Care should be taken to avoid damag-ing the perforating arteries. A.C.A. = anterior cerebral artery; Car.A. = carotid artery; Ext. = external; S.T.A. = superficial temporal ar-tery; Temp. = temporal.

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reconstruction were excluded from this study. Extracrani-al VA reconstruction techniques include VA–carotid arterytransposition;9,10,15 transposition of the subclavian artery tothe CCA;12,18 anastomosis of a branch or the trunk of theECA to the second portion of the VA;14,43 anastomosis of theOA to the third portion of the VA;14,43 saphenous vein by-pass grafting from the subclavian artery to the VA or fromthe CCA to the VA distal to the area of stenosis;36,51,55 verte-bral endarterectomy;1,49 a patch graft of the VA;44 and angio-plastic reconstruction of the VA,35 most of which are relatedto vertebrobasilar insufficiency caused by stenosis or occlu-sion of extracranial VA.

A cerebral revascularization procedure in the posteriorcirculation differs from one in the anterior circulation inseveral ways. First, indications for bypass surgery in theposterior circulation are more ambiguous than those in the

anterior circulation. This may be due to a lack of experienceor to the unique hemodynamic system in the posterior fossa,where collateral flow is abundant. Second, in the posteriorcirculation a revascularization procedure usually deals withrelatively small but critical areas including the brainstemand the cerebellum. Third, recipient vessels generally havea small diameter, which is similar to that of the corticalbranch of the middle cerebral artery. A saphenous vein graftis rarely used in revascularization except for a bypass be-tween the PCA and ECA. Finally, surgical procedures areusually difficult to perform in the deep and narrow oper-ative space near critical vital structures such as the brain-stem and cranial nerves. The OA–PICA anastomosis is per-formed in a relatively shallow place, but the dissection ofthe OA is more difficult than that of the STA. The role ofintracranial bypass surgery for vertebrobasilar insufficien-



FIG. 4. Photographs of cadaveric specimens demonstrating an STA–SCA anastomosis on the left side. A: The anastomosis is performedvia a subtemporal route. After the dura mater has been opened, the tem-poral lobe is elevated until the tentorial edge is identified. Care shouldbe taken not to damage the vein of Labbé or the posterior temporalveins as they enter the transverse sinus. B and C: The tentorial edgehas been removed to expose the SCA and the fourth cranial nerve. Be-cause in this segment the SCA frequently divides into rostral and cau-dal branches, the larger of the two branches is used for the anastomosis.D and E: After the SCA has been exposed, the severed end of that ves-sel is stripped of its fascial layer and a 7- to 8-mm portion of the vesselis exposed. The tip of the STA is then cut into a shape that is suit-able for the anastomotic site. The recipient vessel is prepared by plac-ing temporary clips across the vessel and performing a small arterioto-my equal in length to that prepared on the SCA. After two stay sutureshave been placed, anastomosis of the STA to the recipient vessel is per-formed using 10-0 nylon interrupted sutures (arrowheads).

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141

FIG. 5. Photographs of cadaveric specimens depicting an OA–AICA anastomosis on the right side. A: The OA can be dissected from itspoint of penetration through the occipital muscle to its most distal location. The OA is gently retracted off the field, and a lateral suboccipitalcraniotomy is completed. After the dura mater has been opened, the suboccipital surface of the cerebellum can be seen. With careful retractionof the cerebellum laterally, the AICA in the petrous surface is made visible. The flocculonodular (B and C) and cortical (D and E) segmentsof the AICAs located distal to the facial–vestibulocochlear nerve complex are selected for the anastomoses. The vessel is freed from the pe-trous surface of the cerebellum and is isolated. After the AICA has been exposed, the severed end of the OA is stripped of its fascial layer, anda 7- to 8-mm portion of the vessel is exposed. The tip of the OA is then cut into a shape that is suitable for the anastomotic site. The recipientvessel is prepared by placing temporary clips across the vessel and performing a small arteriotomy equal in length to one prepared on the AICA.After two stay sutures have been placed, anastomosis of the OA to the recipient vessel is performed using 10-0 nylon interrupted sutures (ar-rowheads). Generally, the anastomosis procedure for the AICA is more difficult than that for the PICA because of the depth of the operativefield and the smaller diameter of the recipient vessel. Sig. = sigmoid.

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cy caused by atherosclerotic disease of an extracranial or in-tracranial VA remains unclear. Nevertheless, cerebral revas-cularization in the posterior circulation is well recognized asan important component in the treatment of complex andgiant intracranial aneurysms and tumors, especially whenthese lesions involve major vessels in the posterior circu-lation.

Bypass Procedures

Four arteries—PCA, SCA, AICA, and PICA—are used

as recipient vessels; all of these vessels are more or less re-lated to perfusion of the brainstem. On the other hand, thereare two types of donor graft materials: pedicled arterialgrafts, such as the STA and OA, and free venous or arterialgrafts, such as the saphenous vein and the STA. Selection ofan anastomotic site and a graft material depends on severalfactors, including the patient’s symptoms (ischemic region),the site of the lesion, the collateral circulation, and the re-quired surgical skill.

Ausman and colleagues8 performed the first intracranial



FIG. 6. Photographs of cadaveric specimens demonstrating OA–PICA anastomoses performed using a pedicled graft on the right side (A–C)and a short arterial interposition graft on the left side (D and E). A–C: After dissection of the OA has been completed, the suboccipital duramater is opened to expose the caudal loop of the PICA. The vessel is then freed from the arachnoid. After the PICA has been exposed, the sev-ered end of the OA is stripped of its fascial layer and a 7- to 8-mm portion of the vessel is exposed. The tip of the OA is then cut into a shapethat is suitable for the anastomotic site. The recipient vessel is prepared by placing temporary clips across the vessel and performing a smallarteriotomy equal in length to one prepared on the PICA. After two stay sutures have been placed, anastomosis of the OA to the recipientvessel is performed using 10-0 nylon interrupted sutures. D and E: The free STA or OA is used for an arterial graft. A section of STA orOA graft material, approximately 8 cm long, is dissected from a skin flap, and both severed ends of the donor vessel are stripped of their fas-cial layers. The graft is anastomosed between the OA and the caudal loop of the PICA by using 10-0 nylon interrupted sutures (arrowheads).Cond. = condyle or condylar.

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posterior circulation revascularization procedure for verte-brobasilar insufficiency in the form of an OA–PICA anas-tomosis in 1976. Sundt and Piepgras52 and Khodadad30 re-ported additional experiences with this operation. Sincethen, OA–PICA anastomosis has played an important rolein cerebral revascularization in the posterior circulation.6,32,

38,45 This procedure has several advantages. 1) A recipientvessel, usually the caudal loop of the PICA, has a ratherlarge diameter (mean diameter 1.68 mm), thus making ananastomosis easier. 2) The lumen caliber of the donor ves-sel, usually the OA (mean diameter at the level of the supe-rior nuchal line 2.01 mm), closely approximates that of the

recipient vessel. 3) Bypass surgery can be performed in ashallow and wide operative field, making the procedure eas-ier. The important technical point is to preserve perforatingbranches from the PICA. The disadvantage of this surgeryis the dissection of the OA. This dissection is generally dif-ficult because the OA is tortuous and runs deeply in the oc-cipital muscles. It is important to dissect a sufficiently longpiece of the OA to be able to reach the cerebellar arteries;therefore, the dissection may need to be extended to the lev-el of the mastoid process. The mean length of the OA fromthe exit of the digastric groove to the level of the superiornuchal line in this study was 81.9 mm. Hamada and asso-



143

FIG. 7. Posterior view of a side-to-side anastomosis of PICAs in cadaveric specimens. This procedure is mainly used for cerebral revascular-ization of the distal portion of the PICA after occlusion of its proximal portion. The proximity and parallel courses of the tonsillomedullary andthe telovelotonsillar segments of the PICAs permit their side-to-side anastomosis. Arteriotomies, 4 mm in length, are made on both donor andrecipient arteries. After placement of two stay sutures, the back wall is sutured in a continuous running fashion from the intravascular side andthe anterior wall is closed with interrupted sutures (arrowheads). The distal portion of the artery beyond the occlusion site (arrow) is suppliedby the adjacent artery (dotted arrows).

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ciates22,23 reported on VA–PICA bypasses in which STA in-terposition grafts were used to avoid time-consuming OAdissection. Other revascularization procedures for the PICAare side-to-end,5 end-to-end,34,58 and side-to-side31,56 PICA–PICA anastomoses without graft vessels. The proximityand parallel course of the bilateral tonsillomedullary and thetelovelotonsillar segments of the PICAs greatly facilitatetheir mobilization and anastomosis to one another.

The OA–AICA anastomosis is rarely performed. Fewcases have been reported in the literature.2,59 There are tworeasons for the infrequency of this procedure. One reasonis that the caliber of the lumen of the distal portion of theAICA is relatively smaller than those of other cerebellarvessels. Based on this study the mean diameter of the corti-cal segment of the AICA is 1.07 mm, causing it to be mis-matched with the donor vessel and preventing it from sup-plying a large area. The other reason is a narrow and deepoperative field. To perform the OA–AICA anastomosis asproximally as possible, it is necessary to compress the cer-ebellum with compromise of the collateral branch in thecerebellopontine angle.

Cerebral revascularization procedures were first per-formed in the lower intracranial portion of the posterior cir-culation and later in the upper intracranial portion, includ-ing STA–SCA and STA–PCA anastomoses. Ausman andcolleagues7 reported the first anastomosis between an STAand the cortical segment of an SCA in 1979. After that, thetechnique was modified and became an anastomosis be-tween the STA and the lateral pontomesencephalic segmentof the SCA, which is now well recognized as a standardSTA–SCA anastomosis procedure for cerebral revascular-ization in the posterior circulation.3,4,6,28,41 This procedure ismost commonly used to treat rostral brainstem ischemia.The site of anastomosis of the SCA is located in the antero-lateral margin of the brainstem. The SCA frequently dipscaudally onto the lateral side of the pons. To identify theSCA near the pons, it may be necessary to cut the tentoriumuntil the fourth cranial nerve is completely exposed. In addi-tion, the SCA often gives rise to rostral and caudal branch-es in this area. The larger branch should be selected as arecipient vessel. In the present study we found the mean di-ameters of the rostral and caudal trunks in this segment tobe 1.25 and 1.15 mm, respectively. In cadavers in which theSCA was a single trunk, the mean diameter was 1.51 mm.In this procedure, care should be taken to avoid damag-ing the temporal lobe by retraction, cranial nerves by dis-section in the basal cistern, and perforating arteries aris-ing from the SCA and PCA toward the brainstem.24 TheSTA–PCA anastomosis can be performed in the same oper-ative window used to perform the STA–SCA anastomosis.It may not be necessary to cut the tentorium to exposethe PCA because that vessel courses above the tentoriumin the incisural space. Nevertheless, the highly positionedPCA sometimes makes an anastomotic procedure difficult.To identify the P2A segment of the PCA, which is usuallythought to be a site for anastomosis, excessive retraction ofthe temporal lobe may be needed. A frequently seen seriouscomplication is hematoma and/or edema caused by tempo-ral lobe retraction.26 As a recipient vessel the PCA is advan-tageous because it can be anastomosed to the ECA by us-ing saphenous vein or RA grafts.53,57,60 The mean caliber ofthe lumen of the P2A segment was 2.13 mm in our study, thusmaking it possible to anastomose the graft to the PCA. The

high-flow ECA–PCA bypass allows blood flow to cover alarge area, but there are several disadvantages, including asize discrepancy between the donor and recipient vessels,an anastomotic distortion, an inappropriate graft route, graftocclusion, cerebral hyperperfusion, and surgical manipula-tion during harvest and preparation of the vein segment.11,16,

42,46,50,54

Rationale of Bypass Procedures

Revascularization procedures in the posterior circulationare well recognized as important components in the treat-ment of complex and giant intracranial aneurysms.25,27,31,32,34,

47,53,57,60,61 At present, endovascular techniques, with or with-out combined bypass surgery, offer an alternative therapyfor the treatment of patients with complex and giant pos-terior circulation aneurysms.13,19,20 Nevertheless, there arecontraindications for endovascular treatment, including apartially thrombosed aneurysm and a wide aneurysm neck.Most of these aneurysms present treatment challenges withthe use of the direct clipping procedure. Cerebral revas-cularization procedures are then applied to the treatmentof these aneurysms. The dominant sites for saccular aneu-rysms in the posterior circulation are the VA–PICA junctionand the top of the BA. If a giant aneurysm involves thePICA and it is impossible to spare that vessel, a minimalpiece of the PICA may be removed, followed by repair ofthe stump vessels in an end-to-end fashion.34 If its remov-al is irreparable, consideration should be given to PICAtrapping proximal to the aneurysm and/or revasculariza-tion with the aid of an OA–PICA or PICA–PICA bypass. Inthese procedures, it is important to preserve all viable VAand PICA perforating branches. In a previous report, one ofthe authors (A.L.R.) examined the microsurgical anatomyof the PICA in detail.33 The anterior medullary segment ofthe PICA gives rise to none, one, or two (mean one) of theperforating branches, which usually are of the short circum-flex posterior type and supply the anterior, lateral, or pos-terior surface of the medulla oblongata. On the other hand,the tonsillomedullary segment gives rise to more perforat-ing branches than the other segment (range 0–11 branch-es; mean 3.3 branches), which are either of the direct orshort circumflex type, although the former is predominant.Therefore, revascularization of the distal PICA is neededunless the PICA is sacrificed at a site beyond the tonsil-lomedullary segment. In the case of a giant BA aneurysm,cerebral revascularization should be established, followedby ligation of the vessel proximal to the aneurysm.25,27,47,57,

60,61 The bypass procedure should be selected on the basis ofthe degree of collateral blood flow and aneurysm location.An STA–PCA or STA–SCA bypass can be an option forpatients with mild or moderate hemodynamic insufficiencyof the BA, whereas an ECA–PCA bypass with a high-flowbypass graft should be used for patients with severe he-modynamic insufficiency of the BA. Nevertheless, mattersconcerning the evaluation of the hemodynamic status of pa-tients, expectation of a hemodynamic change after the oper-ation, and potential complications of a graft material remainunclear, as previously described. On the other hand, cere-bral revascularization combined with endovascular tech-niques plays an important role in the treatment of patientswith dissecting aneurysms in the posterior circulation.29,38

Iihara, et al.,29 divided VA dissecting aneurysms into two



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types: those involving the PICA and those not involvingthe PICA. These authors demonstrated good outcomes inpatients with VA dissecting aneurysms that involve thePICA by using endovascular treatment combined with by-pass surgery.

Although few cases with complications such as aneu-rysms have been reported, revascularization procedures arethought to be important for the treatment of complex andgiant skull base tumors involving dominant vessels in theposterior circulation.48,58 Indications leading to cerebral re-vascularization for treatment of these tumors are almost thesame as those for aneurysms. Bypass surgery should be per-formed with the aim of maintaining blood flow to involvedterritories and preventing ischemic complications.

Vertebrobasilar insufficiency occurs frequently and ath-erosclerosis is the predominant cause of the disease. Symp-toms of vertebrobasilar stenoocclusive disease include thosecaused by ischemia of the brainstem and cerebellum. Diz-ziness, which is a common symptom in patients with ver-tebrobasilar disease, may be caused by ischemia of thevestibular nuclei that are fed by the most distal branch of thelong circumflex arteries. Different disease processes tendto involve different portions of the vertebrobasilar circula-tion, and intracranial lesions cause different symptoms fromextracranial lesions. The common sites of atherosclerosisin the vertebrobasilar circulation are the junction of the VAand the subclavian artery; the junction of the VA and thePICA; and the midportion of the BA.37,39 Anticoagulationtherapy has been recommended and is widely used in cas-es of vertebrobasilar ischemia.21 Many patients continueto have transient ischemic attacks in the posterior circula-tion, however, despite receiving anticoagulation therapy.62,63

Although no clear guideline has been established, surgicaltherapy provides an alternative treatment for vertebrobasi-lar stenoocclusive disease, which may be effective in manycases.6 Ogawa and colleagues40 reported a change in CBFand metabolism after STA–SCA bypass surgery, which wasperformed in patients with vertebrobasilar occlusive dis-ease by using positron emission tomography. In their study,CBF, which was low in the posterior fossa preoperatively,increased significantly after STA–SCA anastomosis. Theoxygen extraction fraction, which was high preoperative-ly, decreased significantly not only in the posterior circu-lation but also throughout the entire brain following theprocedure. Further evaluation of each revascularizationprocedure, including data on blood flow and metabolism,should be investigated to establish appropriate indicationsfor bypass surgery in a patient with vertebrobasilar stenooc-clusive disease.

The role of cerebral revascularization in the posterior cir-culation has been less frequently discussed than that in theanterior circulation. In particular, the role of revascular-ization as a treatment modality for patients with arterioscle-rotic disease in the vertebrobasilar tree has not been wellstudied. There has been no controlled randomized studyoffering a comparison of medically and surgically treatedpatients. On the other hand, cerebral revascularization pro-cedures combined with the endovascular technique provideanother opportunity for treatment of patients with complexaneurysms. Further investigations, including the natural his-tory of vertebrobasilar stenoocclusive disease and a changein CBF and cerebral metabolism before and after surgery,will help solve current problems related to choosing a spe-

cific therapy not only for patients with vertebrobasilar isch-emia but also for those harboring aneurysms or tumors inthe posterior circulation.

It is important to understand various microsurgical tech-niques and their related anatomical structures. It will helpsurgeons consider surgical indications for the treatment ofpatients who need cerebral revascularization.

Acknowledgments

We thank Ronald Smith, M.S., Director, and David Peace, M.S.,Medical Illustrator, of the Microneuroanatomy Laboratory, Depart-ment of Neurological Surgery, University of Florida, for constantsupport. We also thank Becky Norquist for reviewing the manu-script.

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Manuscript received April 21, 2004.Accepted in final form August 30, 2004.Address reprint requests to: Masatou Kawashima, M.D., Ph.D.,

Department of Neurosurgery, Kitasato University School of Medi-cine, Kanagawa, Japan. email: [email protected].



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