microsurgical anatomy of cerebral revascularization. part ... et al.pdfthe microsurgical anatomy of...

HE number of cerebral revascularization proceduresperformed by neurosurgeons declined after the Co-operative Study of Extracranial–Intracranial Arterial

Anastomosis15 failed to demonstrate that this procedure re-duced the risk of stroke in patients with cerebral ischemia.Nevertheless, cerebral revascularization is now well rec-ognized as an important element in the treatment of com-plex intracranial aneurysms, cranial base tumors, and cer-tain kinds of ischemic diseases.

In this study we examined the microsurgical anatomyfor cerebral revascularization in the anterior circulation. Inthis paper we demonstrate various procedures for bypasssurgery.

Materials and MethodsThe focus of this paper is the microsurgical anatomy of cerebral

revascularization, including donor and recipient vessels, and thetechniques of revascularization, including STA–MCA, MMA–MCA, and side-to-side anastomoses; short arterial and venous inter-position grafting; and ECA/ICA–M2 and ICA–ICA bypasses. We ex-amined these vessels and techniques by using 25 adult cadavericspecimens and 3 to 40 magnification. Depending on the thickness ofthe vessel wall, 10-0, 8-0, 7-0, or 6-0 nylon thread (Ethicon, Inc.,Somerville, NJ) was used for suturing. The saphenous vein and theradial artery were used as grafts for bypass procedures. The arteriesand veins were perfused with colored silicone. The bone dissectionswere performed with the aid of a Midas Rex drill (Fort Worth, TX).

Results

Arterial Relationships

Table 1 shows the mean diameters of arteries frequentlyused for cerebral revascularization procedures.

J Neurosurg 102:116–131, 2005

116

Microsurgical anatomy of cerebral revascularization. Part I:Anterior 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 that require parent vessel oc-clusion, skull base tumors that involve major vessels, and certain ischemic diseases. In this study, the authors examinedthe microsurgical anatomy of cerebral revascularization in the anterior circulation by demonstrating various procedures forbypass surgery.

Methods. Twenty-five adult cadaveric specimens were studied, using 3 to 40 magnification, after the arteries and veinshad been perfused with colored silicone. The microsurgical anatomy of cerebral revascularization in the anterior circula-tion was examined with the focus on the donor, recipient, and graft vessels. The techniques discussed in this paper includethe superficial temporal artery (STA)–middle cerebral artery (MCA), middle meningeal artery (MMA)–MCA, and side-to-side anastomoses; short arterial and venous interposition grafting; and external carotid artery/internal carotid artery(ICA)–M2 and ICA–ICA bypasses. Bypass procedures for cerebral revascularization are divided into two categoriesdepending on their flow volume: low-flow and high-flow bypasses. A low-flow bypass, such as the STA–MCA anasto-mosis, is used to cover a relatively small area, whereas a high-flow bypass, such as the ICA–ICA anastomosis, is used forlarger areas. Cerebral revascularization techniques are also divided into two types depending on the graft materials: pedi-cled arterial grafts, such as STA and occipital artery grafts, and free venous or arterial grafts, which are usually saphenousvein and radial artery grafts. Pedicled arterial grafts are mainly used for low-flow bypasses, whereas venous or arterialgrafts are used for high-flow bypasses.

Conclusions. It is important to understand the methods of bypass procedures and to consider indications in which cere-bral revascularization is needed.

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

T

J. Neurosurg. / Volume 102 / January, 2005

Abbreviations used in this paper: ACA = anterior cerebral artery;AChA = anterior choroidal artery; CA = carotid artery; CCA = com-mon CA; ECA = external CA; EC–IC = extracranial–intracranial;ICA = internal CA; MCA = middle cerebral artery; MMA = middlemeningeal artery; OphA = ophthalmic artery; PCA = posterior cere-bellar artery; PCoA = posterior communicating artery; RA = radialartery; STA = superficial temporal artery.

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Internal Carotid Artery

The CCA divides into the ICA and ECA at the C2–3 lev-el, below the mandibular angle. The cervical, petrous, andsupraclinoid ICAs are sites of cerebral revascularizationprocedures and in this study their mean diameters were8.57, 5.42, and 3.95 mm, respectively (Table 1). The cervi-cal portion of the ICA is covered by the skin, superficialcervical fascia, platysma, deep fascia, anterior margin of thesternocleidomastoid muscle, and internal jugular vein. Dis-section of these anatomical structures exposes the carotidtriangle, which is formed by the posterior belly of the digas-tric, omohyoid, and sternocleidomastoid muscles. In the ca-rotid triangle, the ICA begins at the bifurcation of the CCA,opposite the upper border of the thyroid cartilage, and runsperpendicularly upward, in front of the transverse process-es of the upper three cervical vertebrae, to the carotid canalin the petrous portion of the temporal bone (Fig. 1A and B).

The petrous portion of the ICA courses within the carotidcanal and ends at the point at which the artery enters thecavernous sinus. At the site where it enters the carotid canal,the CA is surrounded by a strong layer of connective tissuethat makes it difficult to mobilize the artery. The roof of thecarotid canal opens below the trigeminal ganglion near thedistal end of the carotid canal. The greater petrosal nerveruns beneath the dura mater of the middle fossa, immediate-ly superior and anterolateral to the horizontal segment of thepetrous CA. The cochlea lies below the floor of the middlefossa, just posterosuperior to the lateral genu of the petrousCA. The Eustachian tube and the tensor tympani muscle arelocated parallel to and along the anterior margin of the hor-izontal segment, where they are separated from the arteryby a thin layer of bone (Fig. 1C).

The supraclinoid segment of the ICA begins at the sitewhere the artery emerges from the dura mater and enters thecranial cavity by passing along the medial side of the ante-rior clinoid process and below the optic nerve. It reaches thelateral side of the optic chiasm and bifurcates below theanterior perforated substance at the medial end of the syl-vian fissure to give rise to the ACA and MCA. The supra-clinoid segment of the ICA gives rise to three branches: theOphA, PCoA, and AChA. In addition, this segment has per-forating branches including the superior hypophyseal artery(Fig. 1D).

External Carotid Artery

The ECA begins at the bifurcation of the CCA, in frontof the ICA, and ascends backward to the space behind theneck of the mandible, where it divides into the STA andthe maxillary artery. The mean diameter of the ECA was5.75 mm (Table 1) in this study. The ECA is crossed by thehypoglossal nerve, the common facial and superior thyroidveins, and the digastric and stylohyoid muscles. The superi-or thyroid artery arises from the ECA just below the level ofthe greater cornu of the hyoid bone and ends in the thyroidgland. Because of its direction the STA—the smaller of thetwo terminal branches of the ECA—appears to be a contin-uation of that vessel. The STA plays an important role as adonor vessel in cerebral revascularization. This artery hasits origin in the substance of the parotid gland, behind theneck of the mandible, and crosses over the posterior root ofthe zygomatic process of the temporal bone. The mean di-ameter of the STA at the level of the zygoma was 1.93 mm

in this study (Table 1). The STA divides into two branches:one frontal and the other parietal. The frontal branch (an-terior temporal) runs tortuously upward and forward to theforehead, where it supplies the muscles, integument, andpericranium in this region, and anastomoses with the supra-orbital and frontal arteries. The parietal branch (posteriortemporal) is larger than the frontal branch; it curves upwardand backward on the side of the head, lying superficial tothe temporal fascia. This artery anastomoses with its coun-terpart on the opposite side and with the posterior auricularand occipital arteries (Fig. 1B).

Middle Cerebral Artery

The M2 and M4 segments of the MCA are sites of cere-bral revascularization procedures. The M2 segment includesthe trunks that lie on and supply the insula. This segmentbegins at the genu, where the MCA trunk passes over thelimen insulae and terminates at the circular sulcus of the in-sula. The greatest branching of the MCA occurs distal to thegenu at the site at which these trunks cross the anterior partof the insula. The M2 branches are used for bypass proce-dures, especially for high-flow bypasses. Important factorsto consider in selecting an artery for a procedure are its di-ameter, the length of artery available on the cortical surface,and the perforating arteries that arise from this segment andlead to the basal ganglia. The average diameter of the larg-est branch near the central sulcus of the insula was 1.76 mm(Table 1).

The M4 segment is composed of branches leading to thelateral convexity. These branches begin at the surface of thesylvian fissure and extend over the cortical surface of thecerebral hemisphere. The largest cortical artery is the tem-porooccipital artery. Nearly two thirds of these vessels are1.5 mm or larger in diameter and 90% are 1 mm or wider.The smallest cortical artery is the orbitofrontal artery; ap-proximately one quarter of these vessels are 1 mm or largerin diameter.17,39 In the present study the mean diameters of


Cerebral revascularization: anterior circulation

117

TABLE 1Diameters of arteries frequently used for cerebral

revascularization procedures in the anterior circulation*

Artery Mean Diameter (mm)

ICAcervical segment 8.57 6 1.34petrous segment 5.42 6 0.68supraclinoid segment 3.95 6 0.56

ECAcervical portion 5.75 6 0.94

STAat level of zygoma 1.93 6 0.48

MCAM2 segment (largest branch near central sulcus) 1.76 6 0.36M4 segment (largest branch in area)

frontal branch 1.19 6 0.32temporal branch 1.22 6 0.23parietal branch 1.36 6 0.24

ACAA2 segment 2.35 6 0.60A3 segment 1.98 6 0.35A4 segment 1.94 6 0.40A5 segment 1.55 6 0.12

* Values are expressed as means 6 standard deviations.

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the largest M4 in the parietal, temporal, and frontal areaswere 1.36, 1.22, and 1.19 mm, respectively (Table 1). Thecentral sulcal artery is the largest branch leading to the fron-tal lobe, and the angular artery is the largest branch leading

to the parietal lobe. The temporooccipital and posterior tem-poral arteries are the largest branches extending to the tem-poral lobe. The minimum length of a cortical artery need-ed to complete a bypass is 4 mm. The angular, posteriorparietal, and temporooccipital arteries have the longest seg-ments on the cortical surface, and the orbitofrontal andtemporopolar arteries have the shortest cortical segments(Fig. 1E and F).

Anterior Cerebral Artery

At the ACoA the ACA divides into two parts, proximal(A1 segment) and distal (A2–A5 segments). The A3 segmentof the ACA is the dominant site of cerebral revascular-ization procedures, including side-to-side anastomosis andshort arterial and venous interposition grafting. The averagediameters of the A2, A3, A4, and A5 segments in this studywere 2.35, 1.98, 1.94, and 1.55 mm, respectively (Table 1).The pericallosal artery is the portion of the ACA that liesdistal to the ACoA and is constantly present. The perical-losal artery ascends in front of the lamina terminalis to passinto the interhemispheric fissure (A2 segment). Above thelamina terminalis, the artery makes a smooth curve aroundthe genu of the corpus callosum (A3 segment) and thencourses backward above the corpus callosum in the perical-losal cistern (A4 and A5 segments).

The callosomarginal artery is defined as the artery thatcourses in or near the cingulate sulcus and gives rise to twoor more major cortical branches.38 When the callosomargin-al artery is well formed, it lies in the cingulate sulcus abovethe cingulate gyrus and follows a course roughly parallelto that of the pericallosal artery. Its origin varies from justdistal to the ACoA to the level of the genu of the corpus cal-losum. Its origin frequently is found at the A3 segment, fol-lowed by the A2 segment and the ACoA. The size of thepericallosal artery distal to the origin of the callosomargin-al artery varies inversely with the size of the callosomargin-al artery (Fig. 1G and H).

Types of Grafts

Artery Graft: Radial Artery. The RA appears, from its di-rection, to be the continuation of the brachial artery, but it issmaller in caliber than the ulnar artery. Beginning at the bi-furcation of the brachial artery, just below the bend of theelbow, the RA passes along the radial side of the forearm tothe wrist and then winds backward around the lateral sideof the carpus, beneath the tendons of the abductor pollicislongus and extensor pollicis longus muscles. In the upperthird of its course in the forearm, the RA lies between thebrachioradialis and pronator teres muscles and, in the lowertwo thirds of its course, it lies between the tendons of thebrachioradialis and flexor carpi radialis muscles. The super-ficial branch of the radial nerve is close to the lateral side ofthe artery in the middle third of its course.

Before the dissection of the RA, an Allen test1 is neces-sary to check the circulation of collateral blood to the ter-ritory of this vessel. The RA is exposed at the wrist, whereit is located beneath the skin. One can trace the artery prox-imally in the forearm, between the brachioradialis and thepronator teres muscles, up to the bifurcation of the bra-chial artery. Branches joining the artery are subjected to li-gation or bipolar cautery. Heparinized saline solution isused to wash out blood inside the vessel and to check for



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FIG. 1. Photographs of cadaveric specimens showing the arterialrelationships between donor and recipient vessels. A and B: Ante-rolateral views of the cervical ICA and ECA. The cervical portionsof the ICA and ECA are covered by the skin, superficial cervicalfascia, platysma, deep fascia, anterior margin of the sternocleido-mastoid muscle, and internal jugular vein (A). Dissection of theseanatomical structures exposes the carotid triangle (dotted line),which is formed by the posterior belly of the digastric, omohyoid,and sternocleidomastoid muscles. In the carotid triangle, the ICAand ECA have their origins at the bifurcation of the CCA and runperpendicularly upward. C: Superior view of the petrous segmentof the ICA. The petrous portion of the ICA courses within the ca-rotid canal and ends at the point at which the artery enters thecavernous sinus. The roof of the carotid canal opens below the tri-geminal ganglion near the distal end of the carotid canal. The thirddivision of the trigeminal nerve, the greater petrosal nerve, cochlea,Eustachian tube, and tensor tympani muscle are located near thehorizontal segment of the petrous CA. D: Supraclinoid segment ofthe ICA viewed from the left pterional approach. The anterior cli-noid process has been removed. The supraclinoid segment of theICA begins at the site where the artery emerges from the dura materand enters the cranial cavity by passing along the medial side of theanterior clinoid process and below the optic nerve. It reaches the lat-eral side of the optic chiasm and bifurcates into the ACA and MCA.The supraclinoid segment of the ICA gives rise to three branches:the OphA, the PCoA, and the AChA. E: The M4 segment of theMCA viewed from the left pterional approach. The M4 segment iscomposed of branches leading to the lateral convexity, which areused for a low-flow bypass. These branches begin at the surface ofthe sylvian fissure and extend over the cortical surface of the cere-bral hemisphere. The largest cortical artery is the temporooccipitalartery. The central sulcal artery is the largest branch to the frontallobe, and the angular artery is the largest branch to the parietal lobe.The temporooccipital and posterior temporal arteries are the largestbranches leading to the temporal lobe. F: The M2 segment of theMCA viewed from the left pterional approach. The M2 segment in-cludes the trunks that lie on and supply the insula. This segment be-gins at the genu, where the MCA trunks pass over the limen insulaeand terminate at the circular sulcus of the insula. The M2 branchesare used for bypass procedures, especially for a high-flow bypass.Important factors for selecting an artery for the procedure are itsdiameter, the length of artery available on the cortical surface, andperforating arteries to the basal ganglia. G and H: The ACA, ante-rior and lateral views. The ACA is divided at the ACoA into twoparts, proximal (A1 segment) and distal (A2–A5 segments). The A3

segment is the dominant site of cerebral revascularization proce-dures, including side-to-side anastomosis and short arterial and ve-nous interposition grafting. The callosomarginal artery, the largestbranch of the pericallosal artery, generally arises at the A3 segment.A. = artery; A.C.A. = anterior cerebral artery; A.Ch.A. = anteriorchoroidal artery; A.Co.A. = anterior communicating artery; Ang. =angular; Ant. = anterior; Aur. = auricular; A1, A2, A3, A4, A5 =segments of the ACA; Call. Marg. = callosomarginal; Car. = carot-id; Cav. = cavernous; Cing. = cingulate; CN = cranial nerve; Ext. =external; Fiss. = fissure; Front. = frontal; Gr. = greater; Inf. = in-ferior; Int. = internal; Jug. = jugular; Lat. = lateral; Lt = left; M. =muscle; M1, M2, M3, M4 = segments of the MCA; N. = nerve; Oc-cip. = occipital; P.C.A. = posterior cerebral artery; P.Co.A. = poste-rior communicating artery; Par. = parietal; Pericall. = pericallosal;Pet. = petrosal; Post. = posterior; Sternocleidomast. = sternocleido-mastoid; Sup. = superior; Temp. = temporal; Tens. = tensor; Tr. =trunk; Tymp. = tympani; Vent. = ventricle; V. = vein; V1, V2,V3 = divisions of the trigeminal nerve.

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leaks. The harvested RA graft is placed in heparinizedsaline (Fig. 2A–C).

Vein Graft: Great Saphenous Vein. In the superficial veinsof the lower extremity, the great saphenous vein has beenused as a graft for cerebral revascularization. The greatsaphenous vein, the longest vein in the body, has its originin the medial marginal vein of the dorsum of the foot andends in the femoral vein approximately 3 cm below the in-guinal ligament. The vein ascends along the medial side of

the leg in relation to the saphenous nerve. The vein runs up-ward behind the medial condyles of the tibia and femur andalong the medial side of the thigh; passing through the fos-sa ovalis, the saphenous vein ends in the femoral vein. Thevessel usually becomes somewhat smaller at the level of theknee. This reduction in size helps lessen the discrepancy be-tween the caliber of the vein graft and that of the intracra-nial artery recipient. The valves in the great saphenous veinvary in number from 10 to 20; they are more numerous inthe leg than in the thigh.



FIG. 2. Photographs of cadaveric specimens showing graft extraction. A–C: Radial artery in the left forearm. The RA begins at the bifur-cation of the brachial artery, just below the bend of the elbow, and passes along the radial side of the forearm to the wrist, where it then windsbackward around the lateral side of the carpus, beneath the tendons of the abductor pollicis longus and extensor pollicis longus muscles. In theupper third of its course in the forearm, the RA lies between the brachioradialis and pronator teres muscles; in the lower two thirds, betweenthe tendons of the brachioradialis and flexor carpi radialis. D–F: Great saphenous vein in the right lower extremity. The great saphenous vein,the longest vein in the body, begins in the medial marginal vein of the dorsum of the foot and ends in the femoral vein approximately 3 cm be-low the inguinal ligament. It runs upward behind the medial condyles of the tibia and femur and along the medial side of the thigh; passingthrough the fossa ovalis, the vein ends in the femoral vein. The vein is harvested from the leg or thigh, depending on the caliber of the graft re-quired, with care taken to avoid vascular injury and potential thrombosis. The incision is begun 1 cm anterior and 1 cm rostral to the medialmalleolus (dotted circle in D), and the vein is located in the subcutaneous tissue. Brachiorad. = brachioradialis; Car. = carpi; Flex. = flexor;Gr. = great; Rad. = radialis; Uln. = ulnar.

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The vein is harvested from the leg or thigh, depending onthe caliber of the graft required, by using care to avoid vas-cular injury and potential thrombosis. The incision is begun1 cm anterior and 1 cm rostral to the medial malleolus, andthe vein is located in the subcutaneous tissue. The vein istraced superiorly toward the medial side of the knee for 15to 20 cm as needed. Branches joining the vein are eitherligated or occluded using small clips. Before the saphe-nous vein is dissected, it is marked superficially with a skinmarker to avoid later kinking. After complete dissection ofthe saphenous vein, the vessel is ligated proximally and dis-tally, sectioned, and removed. Heparinized saline solution isused to wash out the blood inside the vessel and to check forleaks. The harvested saphenous graft is placed in heparin-ized saline (Fig. 2D–F).

Procedures for Cerebral Revascularization

The STA–MCA Anastomosis. An STA–MCA anastomosisis the most frequently performed anastomotic procedure inthe anterior circulation. The patient is positioned supine,with the head turned so that the side of the bypass is eas-ily accessible. The STA courses in the subcutaneous tissueabove the galea (Fig. 3A). The outline of the STA is deter-mined either by palpation or by using a portable Dopplerdevice. The severed end of the STA is stripped of its fasciallayer, and a 7- to 8-mm portion of the vessel is exposed(Fig. 3B). Once dissection of the STA has been completed,the temporal muscle and fascia are incised at the site of thecraniotomy (Fig. 3C and D). Removal of the bone flap anddura mater exposes the cerebral cortex, where the anas-tomosis is performed. The frontal branch of the STA cours-es above the frontotemporal region, whereas the parietalbranch of the STA passes above the parietotemporal region(Fig. 3E). The recipient artery, which is wider than 1 mmand has a segment measuring at least 6- to 8-mm long formicroanastomosis, is chosen according to its supply area.One or two small branches from the recipient vessel mayneed to be coagulated and sacrificed. A colored backgroundmaterial is placed beneath the recipient artery. The tip ofthe STA is then cut, making a fish-mouth incision suitablefor the anastomosis site. The recipient vessel is prepared byplacing temporary clips across it and performing a small ar-teriotomy. After two stay sutures have been placed, anasto-mosis of the STA to the recipient vessel is performed usinginterrupted 10-0 nylon sutures (Fig. 3F and G).

The MMA–MCA Anastomosis. The MMA is anastomosedto the MCA in this procedure. After a frontotemporal crani-otomy has been performed, the MMA is dissected from be-tween the dural leaves. Anastomosis is accomplished usinginterrupted 10-0 nylon sutures (Fig. 4A–D).

The Side-to-Side (MCA–MCA and ACA–ACA) Anastomo-sis. This procedure is mainly used for cerebral revascular-ization of MCA branches and the distal ACA (A3 segment),combined with occlusion of their proximal branch vessels.Arteriotomies, 4 mm in length, are made in both donor andrecipient arteries. The most difficult procedure is to make atight suture on a back wall. After two stay sutures have beenplaced in the distal and caudal edges of the arteriotomies,the back wall is sutured in a continuous running fashionfrom the intravascular side. The anterior wall is subsequent-ly closed using interrupted sutures (10-0 nylon). Occlusionof the proximal vessel is then completed. The distal portion

of the artery that lies beyond the occlusion site is suppliedby the adjacent artery (Fig. 5A–F).

Short Arterial Interposition Graft Anastomosis. The STA orthe occipital artery is used for an arterial graft. A section ofSTA graft approximately 4 cm long is dissected from a skinflap, and both severed ends of the STA are stripped of thefascial layer. The graft is anastomosed between the bilater-al A3 segments by using interrupted sutures (10-0 nylon).Then, the right pericallosal and callosomarginal junction isoccluded. The distal portion of the right pericallosal arteryis supplied by the left pericallosal artery (Fig. 6A and B).

Short Venous Interposition Graft Anastomosis. In this tech-nique, a short vein graft is used to connect the donor andrecipient arteries. Cerebral revascularization is performedusing a short saphenous vein graft or a superior temporalvein graft, between 5 and 10 cm in length, which extendsfrom the STA trunk anterior to the ear to the M2 or M4 seg-ment. An end-to-side anastomosis of the vein to the recipi-ent artery is performed using 10-0 nylon interrupted sutures.After completion of the anastomosis at the distal end, anend-to-end anastomosis of the vein to the STA trunk imme-diately above the zygoma is performed using 8-0 nylon in-terrupted sutures (Fig. 6C and D).

Cervical ECA/ICA–M2 Anastomosis. Either a saphenousvein graft or an RA graft is used for this bypass procedure.The CCA, ICA, and ECA are exposed in the carotid trian-gle by making a cervical incision along the anterior aspectof the sternocleidomastoid muscle. The zygomatic arch isdrilled to fashion a conduit for the graft when it is placed ina preauricular position. After the craniotomy, a wide dis-section of the sylvian fissure is performed. The MCA trunkis identified and the secondary branches are dissected attheir origin. The secondary vessel, which is thick and hasthe least number of side branches, is chosen and mobilizedfor the anastomosis. The diameter of the vessels in the insu-lar area is normally larger than 1 mm. Care should be takento avoid damaging the lenticulostriate perforating vesselsthat extend from the M2 branches. The main trunk of theMCA is occluded distal to the lenticulostriate perforatingvessels, and its branches are also occluded. The distal anas-tomosis between the M2 segment and the graft is then per-formed in an end-to-side fashion by using interrupted 10-0nylon sutures. After completion of the distal anastomosis,the cervical ECA is occluded proximally and distally. Thegraft is pulled down through the subcutaneous tunnel. Anarteriotomy, approximately 6 to 8 mm in length, is made onthe ECA. The graft is anastomosed to the artery in an end-to-side fashion by using 7-0 nylon sutures (Fig. 7A–C).

Petrous ICA–Supraclinoid ICA Anastomosis. After thepterional craniotomy, the sylvian fissure is opened wide-ly. The sphenoid ridge, anterior clinoid, and proximal opticcanal are drilled away. The distal dural ring is cut to provideroom to place a clip on the ICA proximal to the OphA. Asufficiently long piece of the ICA is then available betweenthe OphA and the PCoA for use in anastomosing a saphe-nous vein graft. Exposure of the petrous segment of the ICAis performed extradurally under the middle fossa dura ma-ter. The dura is elevated along the course of the MMA to theforamen spinosum. The MMA is divided and exposure iscontinued medially and anteriorly to the foramen ovale.A small area of bone posterior to the third branch of thetrigeminal nerve and medial to the foramen spinosum is



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FIG. 3. Photographs of cadaveric specimens demonstrating an example of a low-flow bypass, an STA–MCA anastomosis. A and B: AnSTA–MCA anastomosis is the most common operative procedure performed to create a low-flow bypass. The outline of the STA is determinedeither by palpation or by using a portable Doppler device. The severed end of the STA is stripped of its fascial layer and a 7- to 8-mm portionof the vessel is exposed. C and D: The STA divides into two branches, frontal and parietal. Once dissection of the STA is completed, thetemporal muscle and fascia are incised at the site of the craniotomy. E: Removal of the bone flap and the dura mater exposes the cerebral cor-tex, where the anastomosis is performed. The anterior branch of the STA courses above the frontotemporal region, whereas the posterior branchof the STA passes above the parietotemporal region. F and G: The recipient artery, whose diameter is larger than 1 mm and has a segmentat least 6 to 8 mm long that can be used for microanastomosis, is chosen according to its supply area. One or two small branches from the recip-ient vessel may need to be coagulated and sacrificed. The tip of the STA is cut, making a fish-mouth incision suitable for the anastomosis site.The recipient vessel is prepared by placing temporary clips across the vessel and performing a small arteriotomy. After two stay sutures havebeen placed, anastomosis of the STA to the recipient vessel is performed using 10–0 nylon interrupted sutures (arrows in F). Sphen. = sphe-noid; STA = superficial temporal artery.

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drilled away to expose a portion of the petrous ICA that islonger than 1 cm. The Eustachian tube and the tensor tym-pani muscle are identified and preservation of these struc-tures is attempted. The saphenous vein is anastomosed tothe petrous segment of the ICA in an end-to-side or end-to-end fashion between temporary clips. Interrupted suturesare made using 8-0 nylon thread. The other end of the sa-phenous vein graft is then anastomosed to the ICA in anend-to-side or end-to-end fashion between the OphA andthe PCoA by using an 8-0 or a 10-0 suture, depending onthe wall thicknesses of the ICA and vein graft. Anastomosisat this site is often difficult because a sclerotic change in thearterial wall is frequently observed in the supraclinoid seg-ment of the ICA (Fig. 8A–D).

Cervical ICA–Petrous ICA Anastomosis. The cervical seg-ment of the ICA in the carotid triangle and the horizon-tal segment of the petrous ICA are exposed as previouslydescribed. An RA graft is passed from the cervical area be-neath the subcutaneous tissue on the zygomatic arch towardthe petrous ICA. The proximal end of the RA graft is anas-tomosed in an end-to-side or end-to-end fashion to the cer-vical ICA by using interrupted sutures (7-0 nylon). Thedistal end of the RA graft is then anastomosed in an end-to-side fashion to the petrous ICA by using interrupted sutures(8-0 or 6-0 nylon) (Fig. 8E).

Cervical ICA–Supraclinoid ICA Anastomosis. The supra-clinoid segment of the ICA can be used as the recipient ves-sel in cases in which the MCA is not suitable for anastomo-sis. The cervical and supraclinoid segments of the ICAs areexposed as previously described. The proximal end of the

saphenous vein graft is anastomosed in an end-to-side orend-to-end fashion to the cervical ICA by using interruptedsutures (7-0 nylon). The distal end of the saphenous veingraft is then anastomosed in an end-to-side fashion to thesupraclinoid ICA by using interrupted sutures (8-0 or 6-0nylon). Frequently, the intima of the supraclinoid portion ofthe ICA is atherosclerotic (Fig. 8F).

Bonnet Bypass. In the absence of an available ipsilateraldonor artery in a patient requiring cerebral revasculariza-tion, an anastomosis between the contralateral STA or ICA/ECA and a branch of the MCA (M2 or M4 segment) shouldbe performed using a saphenous vein or an RA graft. Aftera left frontotemporal craniotomy, the saphenous vein graftis anastomosed to the contralateral ICA. The graft is thenplaced over the skull through the subcutaneous tunnel andis anastomosed to the left M2 or M4 segment (Fig. 9A–D).

Discussion

Cerebral revascularization is an important procedure inthe treatment of complex intracranial aneurysms, cranialbase tumors, and certain ischemic diseases. In this study, weexamined microsurgical procedures for cerebral revascular-ization in the anterior circulation and demonstrated eachprocedure by using cadaveric specimens. This knowledge ishelpful not only for surgeons but also for neurologists, neu-roradiologists, and other physicians so that they may under-stand the methods of cerebral revascularization.

Bypass Procedures. Bypass procedures for cerebral revas-cularization are divided into two categories depending on



123

FIG. 4. Photographs of cadaveric specimens showing an example of a low-flow bypass, an MMA–MCA anastomosis. A–D: The MMAis anastomosed to the MCA. After a frontotemporal craniotomy, the MMA is dissected from between the dural leaves. The anastomosis is per-formed using interrupted 10-0 nylon sutures. M.M.A. = middle meningeal artery.

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their flow volume: low-flow and high-flow bypasses. Thelow-flow bypass includes the STA–MCA, MMA–MCA,side-to-side, and arterial and venous short interposition graftanastomoses. These techniques are normally used to cov-

er a relatively small area, where large volumes of bloodare not necessary because of the small caliber of the donorvessel and the low inflow from the terminal branch. Sincethe STA–MCA anastomosis was introduced for EC–IC



FIG. 5. Photographs of cadaveric specimens showing a low-flowbypass provided by side-to-side anastomosis. A–C: The M2 seg-ments of the MCA. A side-to-side anastomosis is performed betweendistal M2 segments (dotted area) in preparation for the proximal occlu-sion of the M2 segment. The side-to-side anastomosis between the dis-tal M2 segments has been completed (arrowhead in B), followed byocclusion of the proximal M2 segment performed using permanentclips (arrow in B). The distal portion of the M2, which lies beyond theocclusion site, is supplied by the adjacent M2 (dotted arrows in C)through the anastomotic site (arrowhead in C). D–F: The A3 seg-ments of the ACA. A side-to-side anastomosis is performed betweenthe A3 segments of the ACA (arrowhead in E), in preparation for theproximal occlusion of the right A2 segment. The distal portion of theright M2 segment, which lies beyond the occlusion site (solid arrow inF) is supplied by the left A3 segment (dotted arrows in F) through theanastomotic site (arrowhead in F).

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anastomotic procedures,14,56 it has played an important rolein cerebral revascularization. Some modifications of thistechnique, such as a double-barrel STA–MCA bypass con-nection28 and STA–M2 anastomosis,13 have been reported toincrease flow from the bypass. The site of an MCA anasto-mosis for an MCA branch or trunk should be selected onlyafter a careful review of the angiograms by considering thedesirable blood flow to supply the ischemic area. Other im-portant factors to consider in the selection of a cortical ar-tery for this procedure are its diameter and the length of ar-

tery available on the cortical surface. In a previous study thelargest cortical artery was found to be the temporooccipitalartery.17 In addition, Chater and associates9 found a corticalartery with a diameter larger than 1.4 mm in the angularzone in 100% of hemispheres. In the present study, we alsohad similar results regarding the diameter of the M4 seg-ment. Arteries over the tip of the temporal lobe and thefrontal lobe were considerably smaller. Side-to-side anasto-mosis is used when extracranial vessels are injured, athero-sclerotic, or very small in caliber. It eliminates the require-



125

FIG. 6. Photographs of cadaveric specimens showing a low-flow bypass provided by a short interposition graft anastomosis. A and B:Short arterial interposition graft anastomosis. A section of the STA approximately 5 cm long is dissected from a skin flap and both severedends of the piece of STA are stripped of the fascial layer. The graft (black arrowheads in B) is anastomosed between the bilateral A3 segmentsby using interrupted sutures (10-0 nylon). Following this, the right pericallosal and callosomarginal junction is occluded (arrow in B). The dis-tal portion of the right pericallosal artery is supplied by the left pericallosal artery through the anastomotic sites (white arrowheads in B). Cand D: Short venous interposition graft anastomosis. Cerebral revascularization is performed using a short saphenous vein graft or a superiortemporal vein graft 5 to 10 cm in length and extending from the STA trunk anterior to the ear to the M2 segment (arrows). An end-to-side anas-tomosis of the vein to the recipient artery is performed using 10-0 nylon interrupted sutures. After completion of the anastomosis at the distalend, an end-to-end anastomosis of the vein to the STA trunk immediately above the zygoma is performed using 8-0 nylon interrupted sutures.

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ment of an extra vessel to be harvested and the need to per-form two anastomoses. This procedure is especially suitablefor revascularization of the ACA (pericallosal artery) be-cause that artery is located deep inside the frontal interhemi-

spheric fissure, away from pedicled arteries such as the STAand the occipital artery.21,57 The MMA could be a potentialdonor artery for cerebral revascularization when the STA isunavailable because of atresia, surgery, injury, infection, or



FIG. 7. Photographs of cadaveric specimens showing an example of a high-flow bypass represented by a cervical ECA/ICA–M2 anastomo-sis. A–C: Either a saphenous vein graft or an RA graft is used for this procedure. The CCA, ICA, and ECA are exposed in the carotid trian-gle. The zygomatic arch is drilled to fashion a conduit for the graft when it is placed in the preauricular position. After the craniotomy, a widedissection of the sylvian fissure is performed. The MCA trunk is identified and its secondary branches are dissected at their origins. The second-ary vessel, which is thick and has the least number of side branches, is chosen and mobilized for the anastomosis. The main trunk of the MCAis occluded distal to the lenticulostriate perforating arteries, and its branches are also occluded. The distal anastomosis is then performed in anend-to-side fashion by using interrupted 10-0 nylon sutures (arrowhead in Fig. B). After completion of the distal anastomosis, the cervical ECAor ICA is occluded proximally and distally. An arteriotomy, approximately 6 to 8 mm long, is made on the arterial surface. The graft is anas-tomosed to the artery in an end-to-side fashion by using 7-0 nylon sutures.

FIG. 8. Photographs of cadaveric specimens demonstrating ICA–ICA high-flow bypasses. A–D: Petrous ICA–supraclinoid ICA anasto-mosis. The sphenoid ridge, anterior clinoid, and proximal optic canal are drilled away. The distal dural ring is cut to provide room to place aclip on the ICA proximal to the OphA. A sufficient portion of the ICA between the OphA and the PCoA is available for anastomosing a graft.Exposure of the petrous segment of the ICA is performed extradurally under the middle fossa dura. A small area of bone posterior to the thirdbranch of the trigeminal nerve and medial to the foramen spinosum is drilled away to expose a portion of the petrous ICA longer than 1 cm.The Eustachian tube and the tensor tympani muscle will be identified and their preservation will be attempted. The saphenous vein is anasto-mosed to the petrous segment of the ICA in an end-to-side or end-to-end fashion between temporary clips. Interrupted sutures are made using8-0 nylon thread. The other end of the saphenous vein graft is then anastomosed to the ICA in an end-to-side (on the right side) or an end-to-end (on the left side) fashion between the OphA and PCoA by using either an 8-0 or a 10-0 suture. Arrowheads in B, C, and D indicate anas-tomotic sites. E: Cervical ICA–petrous ICA anastomosis. The cervical segment of the ICA in the carotid triangle and the horizontal segmentof the petrous ICA are exposed. An RA graft is passed from the cervical area toward the petrous ICA. The proximal end of the saphenous veingraft is anastomosed in an end-to-side fashion to the cervical ICA by using interrupted sutures (7-0 nylon). The distal end of the saphenous veingraft is then anastomosed in an end-to-side fashion to the petrous ICA with interrupted sutures (8-0 nylon). F: Cervical ICA–supraclinoidICA anastomosis. The supraclinoid segment of the ICA can be used as the recipient vessel when the MCA is not suitable for anastomosis. Thecervical and supraclinoid segments of the ICAs are exposed. The proximal end of the saphenous vein graft is anastomosed in an end-to-side orend-to-end fashion to the cervical ICA by using interrupted sutures (7-0 nylon). The distal end of the saphenous vein graft is then anastomosedin an end-to-side fashion to the supraclinoid ICA by using interrupted sutures (8-0 or 6-0 nylon). Frequently, the intima of the ICA in the supra-clinoid portion is atherosclerotic. Arrowheads in E and F indicate anastomotic sites. Arrows in E and F indicate the site of inset. Ophth. = oph-thalmic; P1, P2 = segments of the PCA. (see p 127 ��

)

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embolization.31 If the MMA is dilated in a pathological stateto meet demand, the procedure would be easier than undernormal conditions. A side-to-side anastomosis is rarely per-formed by neurosurgeons, although it is a routine procedurein cardiovascular surgery. A narrow and deep operativefield and a difficult microsurgical procedure may preventneurosurgeons from using this technique easily. Usually, arunning suture is used for both far and near suture lines. Thesize of the orifice should be larger than twice the vesseldiameter.21 Bederson and Spetzler4 also reported a patientwith a giant proximal MCA aneurysm who was treated suc-cessfully by performing a side-to-side anastomosis of theanterior temporal artery to a secondary trunk of the MCA.Short arterial or venous interposition grafts are an alterna-tive to a long vein graft in cases in which a relatively smallarea needs to be supplied.20,23,30,53 This procedure should be

planned if a branch of the STA or the occipital artery dis-plays atherosclerotic changes and the proximal branch ofthe recipient vessel is not available for side-to-side anasto-mosis because of stenosis or occlusion. The pressure differ-ence between the donor and recipient vessels is not as greatas that afforded by saphenous vein or RA grafts. Therefore,to prevent later graft occlusion short interposition graftsshould not be long. The high-flow bypass includes theECA/ICA–MCA and ICA–ICA anastomoses, which aresuitable for supplying large areas when long saphenous veinor RA grafts are used.24,26–29,32,42–44,46,48,50,51 The high-flow by-pass supplies enough blood flow to cover the entire MCAand ACA territories supplied by the ICA. This procedureis usually more difficult than that of the low-flow bypassbecause it requires handling high-flow vessels in a narrowand deep operative field. Anastomotic sites include the cer-



FIG. 9. Photographs of cadaveric specimens demonstrating a high-flow bypass, the bonnet bypass. A and B: A saphenous vein graft isanastomosed to the left M2 segment in the sylvian fissure (white ar-rowhead in B). C and D: The graft is placed over the skull throughthe subcutaneous tunnel (black arrowheads) and anastomosed to theright ICA.

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vical ICA and ECA, the petrous ICA, the supraclinoid ICA,and the M2 segment. The M2 segment is located in the syl-vian fissure on the insular cortex; therefore, bypass surgeryis more easily performed at this site than at other sites in ahigh-flow bypass. The mean diameter of the largest M2 seg-ment near the central sulcus of the insula was 1.76 mm inthis study. Umansky, et al.,54 also reported that the diameterof the M2 in the insular area is larger than 1 mm and, in thecase of secondary trunks, it is usually larger than 2 mm, thusmaking it suitable for most cerebral revascularization pro-cedures. The ECA is used as a donor vessel if there is nocollateral circulation in the high-flow bypass, whereas theICA is used as a donor vessel if there is at least some col-lateral flow and the ICA can be safely occluded tempo-rarily.43 The bonnet bypass is performed either for a low-flow or high-flow bypass, depending on the donor artery.26,49

On the other hand, cerebral revascularization techniquesare also divided into two types, depending on whether thegraft materials are pedicled arterial grafts, such as STA andoccipital artery grafts, or free venous or arterial grafts,which are usually saphenous vein grafts. The pedicled arte-rial grafts are mainly used for low-flow bypasses, whereasthe free venous or arterial grafts are used for high-flow by-pass. For patients in whom both the STA and the occipitalartery are affected by atheromatous disease or in whom theanastomosis site is far from the pedicled graft, however, freevenous or arterial grafts are used in low-flow bypasses asdescribed previously.20,23,30,53 The long saphenous vein graftis usually used as an interposition graft in high-flow EC–ICbypass surgery. The flow through the saphenous vein graftis enough to prevent ischemia in patients with an isolatedICA and no collateral vessels. On average, the vein graftcarries as much as 110 ml/minute of blood supply to the an-terior circulation.52 Disadvantages of this method includedonor–recipient size discrepancy, anastomotic distortion,inappropriate graft route, graft occlusion, cerebral hyper-perfusion, and surgical manipulation during harvest andpreparation of the vein segment.5,12,37,41,48,52 Okada, et al.,36 re-ported the application of a subcutaneous Dacron tube toreduce the incidence of complications such as twisting andcompression of vein grafts within the subcutaneous tunnel.The cervical-to-petrous ICA–saphenous vein in situ bypasstechnique, in which the cervical ICA is used as a tunnel fora vein graft, has also been reported to compensate for thedisadvantages of saphenous vein bypass grafting.6 The RAis another option for an interposition graft in high-flow EC–IC bypass surgery.24,35,42 There are several theoretical rea-sons for using RA grafts. The caliber of the lumen in thisgraft more closely approximates that of small recipientvessels, such as the M2 segment of the MCA. Also the RAhas a uniform intimal wall that lacks valves. Nevertheless,blood flow through the RA graft is much less than that car-ried by a saphenous vein graft (approximately one half ofthat provided by a saphenous vein graft of a typical size).44

Consequently, the RA should be reserved for cases in whichthere is some collateral circulation.42,43

Rationale of Bypass Procedures. The ideal treatment of in-tracranial aneurysms should eliminate the aneurysm fromthe circulation and preserve blood flow through the parentvessel onto branch vessels. This treatment is best accom-plished by direct clip placement across the aneurysm neck;however, aneurysms’ sizes, inaccessibility, lack of discrete

necks, or other technical difficulties sometimes prevent clipplacement. These aneurysms are sometimes unamenableto endovascular coil treatment. Alternative techniques fortreating these unclippable aneurysms, including proximalvessel occlusion, trapping, or excision of the aneurysm, re-quire neurosurgeons to establish cerebral revascularizationto reduce the risk of ischemic disease.26–29,50 Furthermore,recent reports have revealed that an alternation or reductionin blood flow to the aneurysm by cerebral revascularizationis an available option to reduce the risk of aneurysm growthand rupture without sacrificing vital vessels.7,19 This in-dicates that hemodynamics and direction of flow to aneu-rysms play critical roles in their rupture.

The involvement of the petrous or cervical ICA by a neo-plasm represents a difficult surgical problem. In general, themost important principle for approaching neoplastic in-volvement of the ICA is the maintenance of cerebral circu-lation. This usually involves an attempt to dissect the ICAfree from the neoplasm to preserve the artery. If a lacerationof the ICA occurs during dissection, it is repaired or a ve-nous patch graft is used. Only if the ICA is invaded by thetumor, cannot be dissected free from the tumor, or is dam-aged irreparably should consideration be given to ICA re-section and/or cerebral revascularization by providing ahigh-flow bypass between petrous and supraclinoid, cervi-cal and petrous, or cervical and supraclinoid segments ofthe ICA.32,43,47 These procedures require the exposure of thepetrous ICA, which is generally considered to be a compli-cated and difficult procedure. Exposure of the entire petrousICA was described by Fisch and colleagues16 with the sac-rifice of conductive hearing function and transposition ofthe facial nerve. Glasscock, et al.,18 used a similar approach,but one involving temporary division of the facial nerve totreat a petrous ICA aneurysm. Sekhar and associates45 useda preauricular infratemporal fossa approach for exposure ofthe cervical and petrous ICA. If exposure of the entire pe-trous ICA is not necessary, however, a portion of the hori-zontal segment of the petrous ICA can be exposed moreeasily for cerebral revascularization.

For treatment of patients with certain ischemic diseases,cerebral revascularization procedures still play an impor-tant role. Since the discouraging results of the Internation-al Cooperative Study of Extracranial–Intracranial ArterialAnastomosis,15 bypass surgery is rarely performed for thetreatment of arteriosclerotic cerebral ischemic disease. Nev-ertheless, one limitation of the EC–IC bypass trial was thatthere was no method available at the time of the trial to as-sess the status of cerebral hemodynamics in the distal ce-rebral circulation.2,3,10 Recent reports advocate the use ofpositron emission tomography or single-photon emissioncomputerized tomography scanning to predict the risk ofstroke.11,22 Derdeyn, et al.,11 reported that an EC–IC bypasswill be cost effective in patients with symptomatic CA dis-ease in whom the oxygen extraction fraction is increased. Itis important to evaluate the status of cerebral hemodynam-ics before bypass surgery. Current indications for bypassprocedures in patients with symptomatic cerebral ischemiainclude the following: patients are unresponsive to optimalmedial treatment; responsible lesions such as stenosis of thecarotid siphon, are inaccessible for direct surgery; and a re-gion of reduced perfusion has been documented either bydirect measurement of regional cerebral blood flow or bymetabolic studies.8 In addition, bypass surgery plays an im-



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portant role in the treatment of specific ischemic diseases,such as moyamoya disease and traumatic ICA injury.20,25,55

Moyamoya disease is characterized by spontaneous occlu-sion of the circle of Willis, which causes cerebral ischemiaand/or intracranial hemorrhage. To prevent an additionalischemic attack and to reduce hemodynamic stress on theso-called moyamoya vessels, which tend to rupture leadingto intracerebral hemorrhage, cerebral revascularization in-cluding STA–MCA anastomosis is performed. On the otherhand, traumatic ICA dissections are likely to occur in youn-ger patients. First-line therapy for traumatic ICA dissectionsroutinely consists of anticoagulation therapy; however, trau-matic ICA dissections tend to cause significant neurologicaldeficits and require surgical intervention.33,34,40 Vishteh, etal.,55 reported excellent outcomes after cerebral revascular-ization procedures had been performed for the treatment ofpatients with persistently symptomatic traumatic ICA dis-sections.

Cerebral revascularization techniques have been devel-oped in the last three to four decades. The field is still de-veloping with changes in technique and new indications foroperative intervention such as a combination with endo-vascular procedures. The value of cerebral revascularizationsurgery as an aid to improve cerebral ischemia differs notonly between neurosurgeon and physician, but also amongneurosurgeons. It is important to understand the mechanismof each bypass procedure. Careful consideration, includingthe hemodynamic status of patients and difficulties withtechniques, should be taken when a cerebral revasculariza-tion procedure is planned.

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 address: [email protected].



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