Aim of Bypass

In cases of brain ischemia, bypass strategies aim to support a hemodynamically compromised watershed and to reverse ischemia or prevent its further progression (Fig. 10.1). Thus, the term blood flow augmentation is used to classify this type of bypass. ^{2 ,​ 3} In most cases of aneurysm trapping, the goal of bypass is to replace the preexisting normal blood flow through the parent artery and its distal branches; therefore, the term blood flow replacement is used. ⁴ Indications for flow replacement bypass are tumors (benign and malignant), vascular lesions (giant aneurysms and dural arteriovenous fistulas), and traumatic or iatrogenic vascular injuries. In complicated aneurysms, the preference between the terms blood flow augmentation and blood flow replacement is based on the estimated flow demand. Both low- and high-flow grafts are applicable, but the latter is preferable because it can carry almost the same blood flow as the internal carotid artery (ICA).

Volume of Blood Flow

The volume of blood flow is used to classify reconstructive bypass procedures (Fig. 10.2 ). Historically, bypasses have been classified as low flow or high flow, and this definition is still widely used. Low-flow bypasses usually use an STA-MCA bypass, and high-flow bypasses usually use bypasses from the carotid arteries in the neck to intracranial arteries using vascular grafts, such as radial artery grafts or saphenous vein grafts. ^{5 ,​ 6 ,​ 7} Technically, when describing a bypass, the terms low- and high-flow refer to the grafts: low-flow vessel grafts have a flow rate of 20 to 70 mL/min, ⁸ intermediate-flow vessels have a flow rate of 60 to 100 mL/min, and high-flow vessels have a flow rate of 100 mL/min or greater. ⁹ However, in many reported series, the flow was not measured directly. Mohit et al ¹⁰ classified patients as having high-flow bypass when a radial artery graft or saphenous vein graft was used; patients were classified as having low-flow bypass when they underwent other bypass procedures, including STA-MCA bypass, A3-A3 bypass, reimplantation, primary repair, posterior inferior cerebellar artery (PICA) to PICA bypass, occipital artery (OA) to posterior cerebral artery (PCA) bypass, OA to superior cerebellar artery (SCA) bypass, STA-SCA bypass, and PICA to anterior inferior cerebellar artery bypass. Kawashima et al ¹¹ described a low-flow bypass as one used to cover a relatively small area of vascular irrigation, whereas they described a high-flow bypass as one used for a larger area, such as the entire carotid territory. They also defined a pedicle graft as low flow and defined free interposition grafts (saphenous vein graft or radial artery graft) as high flow. ¹¹

A high-flow bypass allows a blood flow rate of between 100 and 200 mL/min. A high-flow bypass is used to replace the blood flow when a normal high-flow vessel must be sacrificed.

The term “intermediate flow” is used to describe bypasses with flow rates of approximately 60 to 100 mL/min, which is higher than that provided by a standard pedicled STA-MCA bypass but lower than that provided by a bypass using a saphenous vein graft. Usually intermediate flow is provided by bypasses from the maxillary artery or from the external carotid artery (ECA). ^{8 ,​ 12}

Anastomosing Arterial Basins

Bypasses can be characterized on the basis of the anastomosing arterial basins as EC-IC bypasses, intracranial-intracranial (IC-IC) bypasses, or in situ reconstructive procedures and extracranial-extracranial (EC-EC) bypasses (Fig. 10.3). EC-EC procedures in neurosurgical practice involve various reconstructive procedures performed on the carotid and vertebral arteries. In situ intracranial reconstruction techniques are a relatively recent innovation in neurosurgery and were developed after EC-IC anastomoses. IC-IC bypasses are technically more demanding than other bypasses because they require manipulations in a deep operative field.

IC-IC bypasses are most often used in aneurysm surgery (Fig. 10.4). Arterial aneurysms can be excised from the parent vessel with a consequent restoration of vessel integrity by different IC-IC bypass techniques that do not require harvesting a separate extracranial donor artery, such as by reimplantation or reanastomosis. The term reanastomosis means the creation of an end-to-end anastomosis, whereas reimplantation means the creation of an end-to-side anastomosis.

Quiñones-Hinojosa and Lawton ¹³ analyzed a series of in situ vascular reconstructions, including A3-A3, MCA-MCA, and PICA-PICA anastomoses. The authors concluded that in situ reconstructions are less vulnerable to injury or occlusion. ¹³ Another technique for restoring collateral blood flow is the creation of a side-to-side anastomosis (Fig. 10.5). It is performed between arteries from different sides of the cerebral circulation that lie close to the midline, such as in PICA-PICA and A3-A3 bypasses, ^{13 ,​ 14} or between any arteries that run parallel to one another. ¹⁵

Length of the Graft

Another important bypass characteristic is the length of the vascular graft (Fig. 10.6 ). Bypasses can be classified on the basis of the length of the graft used: short IC-IC grafts (Fig. 10.7), short EC-IC grafts (Fig. 10.8), standard-length grafts (Fig. 10.9), and long grafts (Fig. 10.10).

Liu and Couldwell ⁵ stated that short grafts have better patency, and they proposed a cervical ICA to supraclinoid ICA saphenous vein bypass via a submandibular pathway. They performed a proximal end-to-end ICA graft anastomosis maximally distal on the neck and made a shorter graft with a more direct route. ⁵ In 1987, Sato and Kadoya ¹⁶ presented three cases in which a long saphenous vein graft was reconstructed after it had been occluded, and the vessels remained patent at the 4-year follow-up. Generally, by long-graft bypass procedures, surgeons mean either a bonnet bypass or a procedure in which grafts are joined to or are proximal to the carotid bifurcation. ¹⁷ A tandem bypass is a long-graft procedure using more than one graft to bypass multiple vascular lesions or to lengthen the graft. ^{18 ,​ 19} Short-graft bypasses are those that anastomose arteries from the extracranial surface (STA or OA) to the intracranial vessels using a graft (STA to saphenous vein graft to MCA ¹⁸ ), intracranial interposition grafts, or relatively shorter skull base bypasses (distal cervical ICA to intracranial ICA ⁵ or internal maxillary artery [IMA] to MCA ²⁰ ). The current recommendation is to use shorter grafts whenever possible. A number of alternative bypasses with shorter grafts have recently been proposed that aim to increase the long-term patency of the grafts compared with the standard ECA to graft to MCA bypass.

Laterality of Bypass Procedure

Another bypass characteristic is laterality (Fig. 10.11). For direct in situ bypasses, the donor artery is usually located on the same side as the recipient artery (Fig. 10.12a). However, when no suitable donor artery is available on the ipsilateral side, other options are possible, including a bonnet bypass in which blood flow is shunted from the donor artery to the contralateral side (Fig. 10.12b), a tandem bypass, or a long-graft bypass. ^{21 ,​ 22} A bilateral bypass may also be used. The term “bilateral” can refer to several variants of bypass. For example, a bilateral bypass can supply blood flow to both anterior cerebral arteries (ACAs) using a Y-shaped or double-barrel graft (Fig. 10.12c). ²³ A bilateral bypass can also be performed to revascularize bilateral MCA territories with donor arteries from both sides, usually STA-MCA bypasses in cases of moyamoya disease (Fig. 10.12d). ²⁴

Site of Distal Anastomosis

The spectrum of common sites for distal anastomosis is shown in Fig. 10.13. Intracranial anastomosis should support blood flow in the distal branches of the sacrificed vessel. The recipient vessel, which is examined preoperatively, should be of appropriate diameter. The diameter of the M1 segment of the MCA is usually 2.4 to 4.6 mm, the diameter of the M2 segment is 1.8 to 3.0 mm, and the diameter of the M4 segment is 0.8 to 1.6 mm. ²⁵ To prevent ischemia during transient occlusion, the recipient vessel should not have a significant number of perforators (most M1 segments have perforators ²⁵ ). When the supraclinoid ICA is determined as the recipient vessel, the flow in its distal branches should be supported, which requires a consistent communicant vessel distal to the site of occlusion—either the anterior communicating artery or posterior communicating artery. Revascularization of the posterior circulation deserves special attention, but the bypass strategy and anastomosis principles are the same. The most commonly used recipient vessels are the horizontal segment of the vertebral artery (VA), P2 segment of the PCA, SCA, or PICA. ¹⁰

Site of Proximal Anastomosis

The spectrum of common sites for proximal anastomosis or donor arteries is shown in Fig. 10.14. In the region of the carotid bifurcation, the common carotid artery, ECA, or ICA can be used as donor vessels. The advantage of an end-to-end anastomosis to the ECA is that the ICA is not occluded during anastomosis, whereas ECA occlusion is well-tolerated. Potential disadvantages include the inability to preserve the STA for bypass. A potential advantage when using the cervical ECA for end-to-side anastomosis is STA preservation without transient ICA occlusion, whereas the blood flow through the ICA is transiently discontinued during the creation of an end-to-side anastomosis on the ICA or common carotid artery.

The subclavian artery can be used as a donor if the carotid arteries are inappropriate. When the subclavian artery is used, the long graft length should be taken into account. ^{16 ,​ 26}

Other sources of arterial blood flow are the IMA, ²⁰ petrous ICA, ⁷ stumps of the STA and OA, ^{4 ,​ 27} middle meningeal artery (MMA), ²⁸ posterior auricular artery ²⁹ and different segments of the VA for bypass in the posterior fossa. ¹⁴ Several technical difficulties are associated with performing petrous ICA bypasses: exposing the petrous carotid artery is challenging, the greater petrosal nerve usually needs to be sacrificed, the anastomosis is technically difficult, the ICA blood flow is stopped for at least 30 minutes to 1 hour, and the ICA is occluded before the shunt patency is confirmed. ⁶ The recently described IMA bypass necessitates extensive skull base resection, including removal of the zygoma and temporalis muscle or middle fossa floor. ^{20 ,​ 30 ,​ 31} This bypass has the potential for injury to the temporomandibular joint, although less traumatic variations have been described. ³²

Options of Distal Anastomosis

A single distal anastomosis is the simplest and most frequently used option; however, complex reconstructions may be necessary (Fig. 10.15). The term double bypass, or double-barrel bypass, is used to describe different techniques. For example, the term is applied to the bypass procedure when both the frontal and parietal branches of STA are anastomosed with the M4 branches of MCA or the PCA and SCA. ^{33 ,​ 34} Another example includes the use of a Y-shaped graft with two distal barrels. This graft can be obtained by harvesting the thoracodorsal axis artery ²³ or by modifying a radial artery graft. ³⁵ The term combined is usually used for vascular anastomosis combined with indirect revascularization; this type of anastomosis is often used to treat moyamoya disease ²⁴ or is used in combination with an endovascular procedure. ³⁶ A supportive bypass is used for blood flow support to the distal branches during the temporary clipping of a proximal part of the vessel for the time needed to create a larger proximal anastomosis. Sequential bypass is a type of double bypass in which the recipient vessels are anastomosed to the side and to the end of the donor vessel. This procedure is predominantly used for myocardial revascularization ³⁷ and is an option for intracranial reconstructions. Another technique known as a double reimplantation is a type of sequential bypass in which several efferent recipient branches are implanted at multiple sites into the large caliber proximal vessel or donor graft. ³⁸

Graft Origin

Grafts can be reasonably classified as pedicled arteries, such as STA grafts and OA grafts, and free vessel grafts, such as radial artery grafts and saphenous vein grafts (Fig. 10.16). ¹¹ The reasons for choosing between radial artery graft and saphenous vein graft are disputable. Saphenous vein graft harvesting usually allows one to obtain a graft that is approximately 25 cm long, whereas radial artery graft harvesting (Fig. 10.17) requires a prolonged dissection, is more invasive, and usually allows one to obtain a graft that is approximately 20 cm long and 2 to 3 mm across. ¹⁰

Grafts are very delicate structures. The possible causes of failure of a saphenous vein graft include endothelial damage caused by venous spasm, overdistension, or direct trauma to the vessel wall during operative manipulation. Applying sutures too tightly to the branch base can cause stenosis at the branching points. Exposing the subendothelial layers to the arterial flow causes inadequate coaptation of the anastomosis. There are other causes of graft failure, such as adventitial tags carelessly left in the vessel lumen, too-vigorous removal of the adventitia, osseous extrinsic compression, and vessel twisting or kinking. Veins also contain valves and should be properly oriented. Saphenous vein grafts are considered to have larger diameter and higher blood flow than radial artery grafts. Radial artery grafts are also susceptible to early vasospasm and intimal hyperplasia. However, applying the pressure distension technique solves the problem of early vasospasm, and calcium channel blockers help in the treatment of intimal hyperplasia of radial artery grafts. ³⁹ The data from the Coronary Artery Surgery Study showed that the long-term patency rate of saphenous vein grafts decreased to 60% after 11 years, and that of radial artery grafts decreased to 91.9% in 5 years. ⁴⁰ Radial artery grafts seem to have a higher long-term patency and diameter closer to the intracranial arteries than saphenous vein grafts; therefore, they are preferred by many surgeons. A saphenous vein graft is used when the radial artery is not available, is small in diameter (e.g., in children), or when cosmetic considerations must be taken into account (e.g., to avoid dissection on the arm). Other choices for a free graft include a thoracic axis arterial graft, ²³ a lingual artery graft, ⁴¹ or a portion of STA used as a short vascular graft. ^{42 ,​ 43} Synthetic vascular grafts are widely used for large vessels, including the ICA, but they are not suitable for replacing vessels with a smaller diameter. A promising option for patients with no suitable autologous arteries or veins available for grafting is the development of tissue-engineered vascular grafts. ^{44 ,​ 45}

Graft Pathway

For a bypass connecting a carotid artery in the neck and one of the intracranial arteries, a vascular graft is usually tunneled either suprazygomatically or subzygomatically (Fig. 10.18). Submandibular graft placement requires removal of the zygomatic arch with muscle retraction and creation of a trough in the middle fossa floor. This route of graft placement provides additional protection compared with a subcutaneous tunnel, and it provides good long-term patency. ^{5 ,​ 46} Short EC-IC bypasses from the IMA, distal cervical ICA, or petrous ICA require specific skull-base approaches. A common rule for any approach is that grafts should be aligned in a way to prevent kinking; sometimes a longer loop-graft trajectory is better than a short graft with a change of flow direction at a sharp angle. ^{42 ,​ 47}

STA-MCA Bypass

The basic techniques of low-flow bypass surgery can be demonstrated by the example of STA-MCA anastomosis, which is one of the standard bypass procedures for brain revascularization. ⁶⁶

Patient Positioning

The patient is placed in the supine position with the head fixed in a frame and turned to the contralateral side, and the ipsilateral shoulder is raised with a cushion. The head should be flat to tilted down to facilitate drainage from the operative field. Electrophysiology neuromonitoring probes are attached to the patient’s head. STA branches are marked on the skin with indelible marker under mini-Doppler navigation (Fig. 10.20). Then, the hair is shaved to a width of 1 to 2 cm along the planned incision line. The skin is prepared using standard aseptic protocol without skin infiltration or local anesthesia, which can cause vessel spasm or injury.

Skin Incision and Craniotomy

The type of skin incision used for bypass procedures varies between clinics and surgeons and according to the needs of the patient (Fig. 10.21). General considerations for the skin incision are STA course, hairline, and adequate approach to the recipient artery (the MCA). In general, an incision that follows the STA is most commonly used.

One of two types of craniotomy is usually used: a regular frontotemporal craniotomy or a small “keyhole” craniotomy. A targeted keyhole bypass can be performed through a small craniotomy using navigation. In this approach, the keyhole position is planned according to the recipient artery position and chosen preoperatively using brain metabolic, perfusion, and angiographic data obtained from MRA, positron emission tomography, and CT. ⁶⁵ The craniotomy should be large enough to allow selection between a number of surface vessels, as the imaging and exposed appearance do not always correspond perfectly.

A linear incision can be used for a single bypass through a small craniotomy. A J-shaped incision is usually used for a double bypass. A single incision can be used for the temporal STA branch, with a small supportive incision placed for additional dissection of the frontal STA branch for a double bypass through a small craniotomy as described by Yoshimura et al. ⁶⁷ A J-shaped incision is created as follows: the first, ascending part of the incision is performed in the projection of the temporal branch of the STA. After the STA is dissected, the incision is prolonged anteriorly, and a craniotomy is performed above the site where the MCA emerges from the sylvian fissure. The frontal branch of the STA can then be easily dissected from the inside of the scalp flap. A craniotomy with a 4 cm diameter is usually adequate for exposing the appropriate recipient artery. The center of the craniotomy is located on a line perpendicular to the orbitoauricular line, 6 cm above the external auditory meatus. This procedure consistently exposes the vessels around the angular gyrus (Fig. 10.21a). ⁶⁸

Meticulous hemostasis throughout the operation is necessary to prevent obstruction of the view by blood and cerebrospinal fluid during microsurgery suturing, to prevent postoperative hematomas, and to preserve hemoglobin with a hematocrit at 30 to 35% so that brain ischemia is avoided, especially in pediatric patients with low total blood volume. ⁶⁹

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