6.1 Key Learning Points

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  The IMax bypass is a safe and effective method to provide an extracranial-intracranial anastomosis without the need for a long conduit.

  
  
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  The IMax bypass may be utilized to provide a mid- to high-flow alternative donor vessel if superficial temporal artery is not available.

  
  
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  Detailed study of the IMax anatomy on the preoperative imaging, in particular its relationship with both heads of the lateral pterygoid muscle, is necessary.

  
  
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  To obtain a longer segment of the IMax, initial localization can be based on the pterygomaxillary fissure as a landmark and drilling performed more posteriorly in the middle fossa toward foramen spinosum.

  
  
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  Other alternative bypass techniques including intracranial-intracranial and bonnet bypass may also be considered based on surgeon’s preference.

6.2 Indications

Invasive skull base tumors often become closely involved with the cerebral vasculature. In particular, in scenarios where gross total resection of the tumor is deemed to be clinically necessary, but the encasement of major vessels precludes its complete resection, arterial bypass may be required.

Tissue biopsy of the offending neoplasm may be necessary prior to the decision for an extensive skull base surgery, as certain tumors may be treated appropriately with aggressive chemoradiation therapy. Neoplasms that have demonstrated poor response to chemoradiation and have involvement of the vessel adventitia should be considered for aggressive resection to improve prognosis. ¹ However, many tumors, when noninvasive and soft in consistency, may be dissected away and taken out microsurgically despite close proximity to the carotid artery. ^{2 ,​ 3}

Careful consideration of the patient’s overall functional status, disease burden, as well as the ability to obtain gross total resection should be evaluated prior to committing a patient for surgery. ^{2 ,​ 4 ,​ 5} Preoperative neuroradiologic imaging should be carefully evaluated to delineate the extent of neoplasm involvement of the skull base and cerebral vasculature. Noninvasive modalities such as computed tomography (CT) angiography or magnetic resonance (MR) angiography (MRA) may be useful in demonstrating spatial relationships, but definitive delineation of the vasculature by digital subtraction angiography (DSA) is recommended to understand the dynamic relationship between the tumor, surrounding cerebral vasculature, and collateral flow. Furthermore, understanding the anatomy of the internal maxillary artery is vital.

6.3 Determination of Cerebrovascular Reserve

Given the significantly increased risk of developing ischemia following carotid or middle cerebral artery (MCA) ligation, it is necessary to clearly delineate the presence of collateral flow from the posterior and contralateral circulation. MRI/MRA and most importantly a noninvasive optimal vessel analysis (NOVA) MRA can be utilized for this purpose and followed by formal angiography. ⁶ The NOVA MRA gives accurate quantitative measurement of flow inside cranial vessels, which could be helpful for planning of a cerebral revascularization.

More invasive procedures can be utilized to assess patient’s tolerance to carotid occlusion, such as the temporary balloon test occlusion (BTO) (see Chapter 2). During this test, the carotid is temporarily occluded using an inflatable balloon positioned via endovascular access. Mean arterial pressure is then decreased by about 20%. The patient is then assessed clinically to see if there is a change in the neurologic examination. A single photon emission computed tomography (SPECT) scan, computed tomography perfusion (CTP), or transcranial Doppler (TCD) may be performed in conjunction with a BTO to further evaluate blood flow. However, the team must be prudent in interpreting the results from a normal BTO, as the risk of future cerebrovascular event may still be possible due to complications arising from thromboembolic events or revascularization injury. ^{7 ,​ 8 ,​ 9 ,​ 10} In addition, skull base resections can often remove external carotid collateral supply.

6.4 Traditional High-Flow Cerebral Revascularization Methodology and Limitations

Standard high-flow bypass techniques were addressed in the previous chapter (see Chapter 5) and will only be described briefly here. In essence, the common carotid or external carotid artery in the neck is utilized as donor vessels and anastomosed via an autologous graft to the intracranial internal carotid or MCA. Typically, this graft is harvested from the saphenous vein or radial artery. ^{11 ,​ 12 ,​ 13} Complications may arise, however, when utilizing long grafts (approximately 20 cm), as they can be occluded along their course. ^{14 ,​ 15 ,​ 16} Three separate operative exposures must be created, including the intracranial exposure of the internal cerebral artery or MCA, the exposure in the neck of the common or external carotid, and the graft site (i.e., radial or saphenous), which requires constant change in surgical view. Often, an approximately 20 cm long graft must be tunneled in the neck to access the recipient site. These can contribute to patient morbidity and increased operative time. ^{1 ,​ 4 ,​ 12 ,​ 17}

6.5 Advantages of the Internal Maxillary (IMax) External Carotid-Internal Carotid (EC-IC) Bypass

First described in cadaveric study over two decades ago, the IMax artery was noted to be feasible as a donor graft for EC-IC bypass. ¹⁸ Subsequent to its described initial use, the technique has been continuously refined with emphasis on the safe utilization of the IMax artery as an intermediate/high-flow (20–120 mL/minute) bypass source.

The IMax EC-IC bypass may be favored over traditional methods due to its ability to utilize a solitary surgical field, shortening surgical time, the ability to use a shorter graft (7–10 cm), decreasing the risk of occlusion, the capacity to see the entire graft length in the surgical field, and its utility for use as a salvage procedure in patients with prior cervical procedures. ^{4 ,​ 19 ,​ 20 ,​ 21} A careful evaluation of required flow replacement is necessary prior to utilizing the IMax as the donor site.

6.6 IMax Artery—Importance of Preoperative Angiography

Prior to surgery, it is prudent to assess for differences in the course of the IMax artery to maximize the operative outcome and identify any abnormalities in the angiographic route of the IMax artery. ⁵ Furthermore, the possible anastomoses with intracranial circulation need to be identified. Attention should be paid to possible ophthalmic artery collaterals through the IMax and make sure the distal ligation of the IMax in its pterygoid segment does not interfere with intraocular blood supply if it is the solitary supply to the retina.

The utilization of noninvasive modalities like CT angiography and MR angiography are recommended initially and also very helpful as intraoperative imaging for IMax localization. Specifically, CT or MR angiography will help delineate the availability, size, and course of the donor segments of the IMax artery, including the mandibular, pterygoid, and pterygopalatine segments, ²² in particular with regard to relationship to the lateral pterygoid muscle. To best delineate the availability, size, collaterals, and location of the donor vessel, an invasive, formal, four-vessel DSA should be performed to aid in appropriate patient selection and check availability of IMax vessel donors. ^{23 ,​ 24 ,​ 25} Specifically, the distal pterygoid segment, which allows for the easiest anastomosis due to its more superficial location and its cross-sectional diameter of 2.3 to 3.2 mm, is a suitable donor for most revascularization purposes. The preoperative decision-making process should include collaboration and discussion with endovascular colleagues to delineate which patients may be selected for the IMax EC-IC bypass.

6.7 IMax Artery Anatomical Considerations

Following its bifurcation from the common carotid artery, the external carotid artery divides into the superficial temporal artery and IMax artery distally. The IMax arises deep to the mandibular neck where it courses anteriorly and trifurcates into three segments: (1) mandibular, (2) pterygoid, and (3) pterygopalatine. ²² The mandibular division continues dorsal to the mandible. The pterygoid division continues to the pterygomaxillary fissure, while the pterygopalatine division continues where it runs inferior to V2. ²⁶ Initially, the pterygopalatine division of the IMax was used as a intermediate- to high-flow bypass donor vessel. However, more recently, the pterygoid segment has been favored due to its wider operative exposure and more maneuverability, lower number of arterial side branches, and closer adjacent course to the floor of the middle fossa. The use of the pterygoid segment favors an end-to-end anastomosis to the graft as opposed to an end to side to the pterygopalatine segment. ^{27 ,​ 28 ,​ 29} Although there are variations in the diameter of the IMax, the average diameter of the pterygoid and pterygopalatine segments are similar (2.4–3.46 mm vs. 2.3–3.2 mm) which may theoretically translate into similar flow rates. ³⁰ This matches closely with the diameter of the M2 segment of the MCA, making adequate anastomosis technically feasible. ³¹

6.8 Autograft Selection for High-Flow Bypass

Suitable graft determination must consider the hemodynamic outflow necessary to maintain the cerebrovasculature of the target areas supplied by the artery that is being subjected to bypass. The diameter of the donor and recipient arteries, the usability of graft locations and the maximum span of the graft must also be taken into account. ^{15 ,​ 32}

Typically, the graft types that are considered for high-flow carotid bypass (80–200 mL/minute) include the lower extremity saphenous, brachiocephalic veins, and radial artery. ^{33 ,​ 34} Flow rates between venous grafts (70–140 mL/minute) and arterial grafts (40–150 mL/minute) are relatively comparable. ^{4 ,​ 15 ,​ 35} Radial artery grafts are initially preferred as vascular dissection is relatively uncomplicated due to its superficial course. The radial artery diameter matches well with the donor and recipient sites making anastomosis easier. Rates of vessel occlusion have been reported to be low when utilizing radial artery grafts, with documented better graft patency rates than venous autografts. ^{16 ,​ 24 ,​ 29 ,​ 36} The risk of graft spasm remains the major downside of the radial artery graft and therefore a pressure distention technique ⁴ needs to be applied during the graft harvest to decrease the risk of spasm postoperatively. The pressure distention technique involves injecting saline into the vessel from either end (with the other end occluded) to forcibly inflate the vessel. ⁴ Other arterial graft options are anterior tibial artery, posterior tibial artery, lateral circumflex femoral artery, and internal mammary artery. In the event an arterial graft cannot be acquired, or it is not preferred due to risk of spasm, saphenous venous grafts may also be utilized. However, close postoperative monitoring is required as venous grafts have been shown to be susceptible to the formation of accelerated atherosclerosis following the procedure. ^{37 ,​ 38} Heparinization for a goal partial thromboplastin time (PTT) of 45 to 50 for vein grafts for up to 72 hours after surgery is recommended. Patients are routinely placed on ASA 81 mg on the morning of the surgery and subsequently kept on it indefinitely.

6.9 IMax Bypass Operative Technique

A frontotemporal skin flap is incised and reflected to anticipate the generous exposure of the sylvian fissure required for successful IMax bypass. We prefer the utilization of an interfascial dissection of the temporal muscle, with exposure of the frontal process of zygomatic bone.

Pterional craniotomy with addition of zygomatic or orbitozygomatic osteotomy are subsequently performed, allowing for access to the infratemporal fossa and inferior reflection of the temporalis muscle ³⁹ (Fig. 6.1). The pterygomaxillary fissure is identified by palpating the posterior wall of the maxilla and following it inferiorly. If the IMax is not immediately visible, then the superior head of lateral pterygoid muscle is partially detached from its insertion at the infratemporal crest for better visualization of infratemporal fossa contents. The IMax is identified between the lateral and medial pterygoid muscle entering the pterygo-maxillary fissure (PMF). A sufficient length of the vessel is dissected in a retrograde fashion in its pterygoid segment to increase the mobility of arterial stump. Deep temporal branches are identified, and usually a distal bifurcation in which the IMax size remains similar to the proximal segment is the limit of distal dissection and ligation of the IMax pterygoid segment. Following distal ligation (with hemoclips) and temporary occlusion of the proximal portion, the vessel is transected and mobilized superiorly for end-to-end anastomosis. ³⁹

Stereotactic navigation, with intraoperative merging of the preoperative CTA and MRI with contrast, is useful in all cases to help aid in determining the location of the IMax and confirming its position based on anatomical landmarks. With the use of navigation and Doppler, the IMax is identified medial (38%) or lateral (61.6%) to the lateral pterygoid muscle ⁴⁰ (Fig. 6.2).

The dural opening is centered around the sylvian fissure with the dural flap reflected anteriorly. The sylvian fissure is split and dissected in standard fashion, until appropriately sized MCA (M2 vessels) are visualized (Fig. 6.3). We prefer to use the MCA as opposed to ICA for distal anastomoses. The recipient vessel is dissected free of arachnoid and off the pia of the underlying cortex in a segment devoid of side branches to a length of approximately 1 to 2 cm. Patency of the recipient vessel is assessed by micro-Doppler probe. A colored plastic background is placed underneath the vessel to increase contrast between the vessel and underlying brain.

Analogous to the preparation of the recipient vessel, the IMax is dissected free of any soft tissue. After the patency is checked with micro-Doppler, a temporary clip is placed proximal to the intended implantation site for proximal anastomoses and the very distal segment is ligated. The IMax is subsequently liberated from its muscular attachments, transected, and mobilized superiorly up to the level of the middle fossa floor. The lumen of the proximal IMax stump distal to the temporary clip is flushed clear of blood using heparinized saline. The adventitia of both the IMax and the proximal part of the graft is meticulously dissected.

The harvested interposition graft is sewn onto the proximal end of the IMax in end-to-end fashion with an 8–0 suture/cutting needle ⁴¹ (Fig. 6.4). The proximal temporary clip on the IMax is briefly opened to assess patency of the anastomosis. Once this is established, the proximal temporary clip on IMax is reapplied and the graft is flushed clear of blood with heparinized saline and is ready to be implanted onto the MCA vessel (Fig. 6.5). The distal end of the graft is fish-mouthed (if necessary, to match recipient size) and implanted in an end-to-side fashion to the MCA vessel. Naturally, the recipient MCA vessel is temporarily clipped around the site of anastomosis. Using 9–0 or 10–0 sutures, the heel and toe are sewn first, followed by interrupted sutures on the back wall and running sutures on the front wall. This particular technique has worked very efficiently. Heparin saline is used to flush the anastomosis site during the suturing.

Before tying the last stich, a temporary opening of clips on the IMax is conducted to observe flow across the implantation site. This helps to identify possible pitfalls with the anastomosis, including inadvertent suturing of both walls of MCA vessel together, occlusion of the recipient vessel resulting in thrombosis or the presence of an air leak. After this has been successfully accomplished, a temporary clip is placed back on IMax, the last knot of the anastomosis is tied, and all temporary clips removed. Clips are removed in sequence beginning first with distal MCA, then proximal MCA and last the IMax. Minor bleeding from the anastomosis site is expected and addressed by applying small Gelfoam pledgets to the suture line.

Intraoperative neuromonitoring should be utilized to monitor changes in motor or sensory evoked potentials, especially during occlusion time of the MCA. Papaverine may also be liberally used to prevent arterial vasospasm. Intraoperative indocyanine green, intraoperative flow assessment with Doppler flow probe as well as intraoperative angiography is advised to display adequate flow through the graft site. ⁴² If flow is maintained, subsequent ligation of the carotid artery or the relevant vessel may occur. In particular, dural, cranial, and skin closure should be completed with no compression or kinking of the graft. Patients typically receive 3,000 units of heparin during the temporary clipping and are placed on ASA 325 mg daily both pre- and postoperatively. For vein grafts, heparinization with a goal PTT of 45 to 50 for up to 72 hours after surgery is implemented.

6.10 Illustrative Case 1

A 64-year-old man presented with a large, 6-cm, left-sided parapharyngeal tumor extending proximally toward the skull base (Fig. 6.6). The extracranial ICA was encased by the tumor and was resected along with the tumor based on the stability of neuromonitoring during ICA clamping time. The patient presented with recurrent transient ischemic attack (TIA) and eventually evidence of watershed infarct on diffusion-weighted imaging (DWI) sequence MRI in the frontal lobe, specifically in the centrum semiovale and operculum a few days after surgery (Fig. 6.7). This presentation confirmed the need for cerebral revascularization. An IMax–MCA bypass was performed with robust filling through the graft evident on postoperative angiography (Fig. 6.8). The patient had significant improvement of his right-sided weakness at short-term follow-up.