Mario Teo, Jeremiah N. Johnson, and Gary K. Steinberg
Abstract
When the parietal and frontal superficial temporal arteries are not available as a direct donor to the middle cerebral artery (MCA) territory, the occipital artery (OA) can often be utilized. Additionally, due to significant leptomeningeal collateralization from the posterior circulation to the anterior circulation, progressive steno- occlusion of the posterior cerebral artery (PCA) in advanced moyamoya disease (MMD) can result in inadequate collateralization of the MCA or PCA territory. The OA is also an appealing donor choice for revascularization of these territories due to its close proximity to the target recipient vessels; however, there are challenges associated with this strategy, such as tortuosity, multiple branches, and thick adherent investing tissue, which can result in inadvertent OA injury during vessel harvest. In this chapter, we highlight the steps and nuances in performing the challenging OA-MCA or OA-PCA bypass, the techniques used to troubleshoot inadvertent OA occlusion or injury, and illustrate with appropriate case examples. We also include the preoperative workup, intraoperative patient positioning, a step-by-step description of key procedures, and the long-term clinical and radiological postoperative care and surveillance, all of which contribute to achieving maximal benefits of direct bypass to the posterior MCA or PCA in select patients with MMD vasculopathy.
Keywords: OA-PCA or MCA bypass, occipital artery, posterior circulation MMD, inadvertent vessel injury, troubleshooting principles
Moyamoya disease (MMD) is a progressive angiopathy that, over time, can involve the posterior circulation. Because the posterior circulation provides significant collateralization, especially to the anterior circulation, stenosis or occlusion of the posterior cerebral artery (PCA) can also affect the anterior parts of the brain. When the target recipient vessel for bypass is the posterior middle cerebral artery (MCA), or posterior circulation, the occipital artery (OA) is a particularly appealing donor choice.
22.1.1 History
• 1970—Yasargil and colleagues reported the first successful extracranial to intracranial (ECIC) bypass.
• 1976—Khodadad reported the first successful OA- posterior interior cerebellar artery (PICA) bypass for a 58-year-old man with posterior circulation ischemic symptoms and a postoperative angiogram confirming bypass graft patency.
• Apart from ischemic neurological disease involving the posterior circulation, OA grafts are frequently used for PICA bypasses in the cases of PICA aneurysms that required parent vessel sacrifice.
• Recently, OA grafts have increasingly been used for posterior MCA or PCA revascularization in MMD.
• Repeat or initial revascularization for MMD patients with inadequate collateralization of the MCA or PCA territory, when no suitable superficial temporal artery (STA) donor is available.
• The harvest of OA is challenging due to its tortuosity, multiple branches, and thick investing fascia.
• Harvest an adequate length of OA to reach the territory to be revascularized.
• Harvest the main OA trunk, as smaller secondary tributaries are not usually of adequate size for direct bypass.
22.4.1 Strength
• Good donor option in the absence of suitable STA, when posterior MCA or PCA territories are to be revascularized.
22.4.2 Weakness
• OA is tortuous, has multiple branches, and thick adherent investing tissue.
22.4.3 Opportunity
• Stereotactic CT angiography of OA to accurately locate and harvest the OA branch to be utilized.
22.4.4 Threat
• Inadvertent injury resulting in occlusion of OA donor during dissection.
• Poor patient medical or neurologic condition excluding patients as candidates for cranial bypass.
• OA with extensive preexisting ECIC collateralization.
22.5.1 Relative Contraindications
• Patients with recent cerebral infarct should undergo diffusion-weighted imaging (DWI) on magnetic resonance imaging (MRI) of brain (within 1-2 weeks), as the risk of perioperative strokes is significantly increased.
• On angiogram, carefully study the OA tributaries and sizes as well as determine the branch to be harvested.
• Assess existing ECIC collateralization provided by OA on cerebral angiograms so as to determine if harvesting OA as a donor graft might lead to more ischemic brain injury.
• Optimize patient positioning for the brain territories to be revascularized, and the OA vessel to be harvested.
From 1991 to 2016 we have performed 1,440 ECIC bypasses for MMD, of which 1,252 (87%) were direct bypasses. OA-MCA or OA-PCA bypasses were used for repeat revascularization in eight cases.
Age of patients ranged from 8 to 60 years, with a mean follow-up of 6 years (range: 1 to 15 years).
None of the eight patients experienced perioperative infarction. One patient developed a postoperative transient neurologic deficit (TND) that resolved within 10 days.
At last follow-up, all patients had preoperative symptom resolution, with follow-up cerebral angiogram confirming patent bypass grafts of all OA-MCA or OA-PCA revascularizations.
Preoperatively, patients underwent a thorough medical, cardiac, and anesthetic assessment with routine preoperative labs and the relevant diagnostic imaging, which includes 6-vessel cerebral angiogram, MRI brain, and cerebral perfusion imaging with and without Diamox (positron emission tomography, MR perfusion, TCDs). At our institution, we perform MR perfusion with and without Diamox and patients demonstrating poor cerebrovascular reserve or steal (indicating that the affected vascular territory is already maximally vasodilated to promote flow) are considered especially at high risk for ongoing ischemia without treatment. These patients are also at higher risk for perioperative ischemic complications, thus particular care is taken to avoid hypotension perioperatively and during the recovery period. Intraoperatively, the patient’s blood pressure is maintained at or above the preoperative baseline at all times.
22.8.1 Specific Consideration with Anticoagulation
• For patients with mechanical heart valves or recent venous thromboembolism, we restart anticoagulation at 2 to 4 weeks postoperatively after CT head confirms no significant hemorrhage.
• Aspirin is continued through the day before surgery, withheld on the day of surgery, and restarted on the first postoperative day.
22.9.1 Patient Position with Skin Incision
• Depending on the vascular territory to be revascularized, positioning options are: (1) prone (for occipital region, PCA territory; Fig. 22.1a) or (2) supine, head turned with the parietotemporal uppermost (posterior MCA territory).
• A Mayfield head holder secures the head position.
• A Doppler probe is used to map out the course of the OA(Fig. 22.1b)
• Skin incision options include: (1) horseshoe flap (Fig. 22.1b) or (2) linear incision over the vessel to be harvested.
22.10.1 Key Procedural Step 1: OA Harvest
• Use microscopic guidance.
• For a linear incision, make the superficial skin incision through the epidermis and partial thickness of the dermis starting above the suboccipital muscle over the vessel.
• To avoid damage to the OA, dissect through the remaining dermis and subcutaneous tissue using blunt- tip, fine curve scissors.
• Once the OA is visualized, carefully dissect along the main tributary with meticulous hemostasis to harvest enough length of the vessel to reach the recipient territory.
• For dissection of the OA using a horseshoe flap, the vessel is dissected from the underside of the scalp flap (Fig. 22.2a).
22.10.2 Key Procedural Step 2: Craniotomy and Dural Opening
• The OA is retracted laterally and protected with a vein retractor.
• The underlying occipitalis, fascia, and pericranium are incised in line with the long axis of the harvested OA.
• Perform subperiosteal dissection of the muscle and pericranial attachment to expose the underlying bone for craniotomy opening.
• Fashion burr holes in the supratentorial compartment, avoiding injury to the torcula, superior sagittal sinus, and transverse sinus.
• Perform the craniotomy over the parietotemporal or occipital region depending on whether the posterior MCA or PCA is being revascularized (Fig. 22.2b).
• Open the dura in a cruciate manner or with a flap that is based on the venous sinuses, and use dural tack-ups to obliterate the epidural space.
22.10.3 Key Procedural Step 3: Prepare Recipient Vessel
• Open the arachnoid for the recipient vessel with enough length (usually 7-10 mm) exposed to prepare for temporary clipping and anastomoses.
• Size measurement: the minimum diameter for the recipient vessel should be 0.8 mm, but ideally at least 1 mm.
• Measure flow using the Charbel Transonics ultrasonic flow probe.
• Select the position for temporary clip application.
• Choose the site for arteriotomy (parietotemporal or lateral occipital lobe for MCA territory, medial occipital or inferior temporal lobe for PCA territory).
22.10.4 Key Procedural Step 4: Prepare Donor Vessel
• Measure the size of the donor OA to ensure its diameter matches the recipient vessel, and is adequate for direct bypass (ideally 1 mm or larger, but at least 0.8 mm; Fig. 22.3a).
• Ensure patency of the donor graft with frequent handheld Doppler checks.
• Apply a temporary clip to the proximal OA, and divide the distal OA at a 45-degree angle (Fig. 22.3b). Flush the vessel lumen with heparinized saline to prevent thrombus formation (Fig. 22.3c).
• Perform “cut flow” measurement of the donor artery using Charbel Transonics ultrasonic flow probe.
• Fish mouth the donor vessel.
• Ensure well-visualized OA vessel walls.
Techniques used to troubleshoot inadvertent OA occlusion or injury:
• Flush with heparinized saline; regular papaverine or nicardipine drip on the vessel to prevent vasospasm.
• In the event of no blood flow after dividing the OA vessel, pass a 3F pediatric sheath or wire to dislodge any formed thrombus or to locate the area of occlusion (Fig. 22.3d).
• If an area of occlusion is identified that cannot be opened easily with the wire or pediatric sheath, excise the occluded segment, flush both proximal and distal cut end with heparinized saline (Fig. 22.3e), followed by primary anastomosis of the donor vessel (Fig. 22.3f) to restore donor graft patency (Fig. 22.3g).
22.10.5 Key Procedural Step 5: Microanastomosis
• Anesthetic optimization (hypothermia: 33 °C, CO2: 35 mm Hg, mean arterial pressure [MAP]: 80-90 mm Hg during exposure, MAP: 90-100 mm Hg) and burst suppression using propofol prior to recipient vessel occlusion.
• Apply temporary clips to M4/P4, followed by arteriotomy and flush the lumen with heparinized saline (Fig. 22.4a).
• The donor and recipient vessels are tinted with indigo carmine, methylene blue, or a sterile marking pen to better visualize the arteries during the microanastomosis (Fig. 22.4b).
• Use 10/0 Prolene for the anastomosis, toe stitch first, then heel stitch, three (sometimes four) interrupted stitches on each side, making sure to avoid incorporating the opposite vessel wall or stenosing the recipient vessel (Fig. 22.4b-f).
22.10.6 Key Procedural Step 6: Ensure Bypass Graft Patency
• Should observe some blood leakage at the anastomotic site on release of the temporary clips, which will mostly seal with time and irrigation.
• Occasionally, additional sutures are needed to control blood leakage at the anastomosis, but usually not necessary to reocclude the recipient artery.
• To confirm patency and function of the bypass graft we perform: (1) flow measurement (Transonics Charbel Flowmeter) of the OA, proximal, and distal recipient vessels, (2) Doppler probe for flow signal transduction, and (3) intraoperative indocyanine green (ICG) angiogram (Fig. 22.4g).
• Ensure hemostasis prior to closure; use Surgicel for the anastomosis site.
22.10.7 Key Procedural Step 7: Closure
• Ensure meticulous hemostasis.
• Dural opposition to not compromise the donor vessel.
• Dural graft overlying the brain: create a plane between brain and bone.
• Bone flap replacement: ensure adequate opening to accommodate the donor graft.
• Perform regular Doppler checks to ensure bypass graft patency.
• Multilayer the scalp closure to muscle, galea, skin.
• Perform meticulous dissection to follow the primary OA.
• Positioning depends on the areas being revascularized.
• Supine with head turned to revascularize posterior MCA, prone for PCA.
• Inadvertent occlusion or injury to the OA during dissection stage: use careful bipolar coagulation at low power of bleeding points.
• Dissection of the secondary OA branch instead of the primary OA.
• Stenosing recipient artery.
In case of inadvertent OA occlusion or injury:
• Identify the site of occlusion or injury.
• If the OA graft occluded due to thrombus, pass a 3F pediatric sheath or wire to dislodge the occlusion.
• If the OA graft was coagulated or injured during dissection, excision followed by primary anastomosis of the injured site is warranted.
22.14.1 Patient Surveillance
• First 24 hours postoperative:
о Intensive care unit with regular neuro checks.
о Close monitoring of hemodynamic status (fluid intake, output, and electrolytes).
о Thresholds for blood pressure MAP goals of 90110 mm Hg to prevent hypoperfusion, delayed TND, or hyperperfusion and postoperative hematoma.
о Analgesia, antiemetic.
• Day 2: mobilize, oral intake, transfer to regular ward care.
• Remain in hospital until deemed safe to be discharged by neurosurgical and general surgical team (average hospital stay 2-3 days).
• Post discharge, educate and inform about TND, wound care, and subsequent follow-up plans.
22.14.2 Bypass Function Assessment
• Intraoperative OA-PCA or OA-MCA bypass graft assessment using ICG angiogram, Transonic Charbel flow probe, and Doppler probe. Six-month postoperative digital subtraction angiogram (DSA) including a 5-vessel cerebral angiogram, MRI brain including fluid-attenuated inversion recovery (FLAIR)/ DWI sequence, MRI perfusion with/without Diamox (to assess cerebrovascular reserve), and neuropsychological testing.
• Long-term follow-up at 3,10,20, and 30 years with clinical and radiological surveillance (investigations as listed at the 6-month check).
22.15.1 Case 1: OA-PCA Bypass
A 10-year-old girl initially presented at age 7 with mild left arm neglect, and was diagnosed with bilateral MMD. She had bilateral indirect encephaloduroarteriosynangiosis (EDAS) revascularizations at an outside institution that was complicated by a postoperative stroke, requiring a right frontal decompression and lobectomy. After extensive rehabilitation she was left with complete left visual field loss, a spastic left-sided weakness (four out of five weakness), and attended school with a special visual aid due to her poor vision. When seen in our clinic, she was experiencing new episodes of transient blindness, which was worrisome for compromise in the cerebral blood flow in the left occipital region. Cerebral angiogram showed bilateral ICA occlusion with moyamoya vessels (Fig. 22.5a—d), and good revascularization of the MCA territories from the bilateral indirect bypass grafts (Fig. 22.5e—h). She also had bilateral PCA occlusion with poor filling of both occipital lobes (Fig. 22.5i, j). MRI brain showed a large stroke in the right MCA and PCA territory with a smaller left PCA stroke (Fig. 22.5k—n). She underwent an uneventful left OA-PCA direct bypass to revascularize her left occipital lobe.
Her 6-month and 3-year angiogram showed a patent left OA-PCA bypass supplying the parietooccipital and calcarine areas (Fig. 22.5o, p). MRI brain showed no new infarcts, and a nuclear medicine Diamox study showed fixed defects in the known areas of infarct and no Diamox-induced perfusion defect. At her latest follow-up 8 years after left OA-PCA bypass, she remained well and no longer complained of visual disturbance.
22.15.2 Case 2: OA-MCA Bypass
A 36-year-old female patient with transient ischemic attacks (TIAs) affecting her right hemisphere was diagnosed with right unilateral MMD (cerebral angiogram [► Fig. 22.6a, b], showed right-sided high-grade preocclusive stenosis involving the ICA and MCA with ACA occlusion), and underwent right EDAS. Her symptoms recurred 1 year later, with headache, intermittent left-sided weakness and numbness. Repeat cerebral angiogram showed poor filling of the rightsided indirect bypass graft with little collateralization of the right MCA territory (Fig. 22.6c). MRI brain showed no new infarcts, but reduced perfusion on the right watershed region (Fig. 22.6d). Xenon CT showed suboptimal augmentation of the same region involving the posterior MCA.
She then underwent right OA to posterior MCA direct bypass, with symptom reduction postoperatively. Her 6-month cerebral angiogram showed stable underlying ICA and MCA high-grade stenoses, and a patent right OA- MCA bypass graft supplying the posterior MCA portion (Fig. 22.6e, f). MRI brain showed no new infarcts, and MR perfusion showed improved cerebral blood flow to the right posterior watershed area in comparison to preoperative findings. At 3-year follow-up, she was asymptomatic, with cerebral angiogram (Fig. 22.6g-i) still showing a patent OA-MCA bypass graft, and MR perfusion showing appropriate augmentation in all vascular territories after Diamox challenge.
OA is a particularly appealing choice for posterior MCA or posterior circulation bypass procedures due to its proximity to the target recipient vessels. Despite the challenges encountered in harvesting the tortuous, highly branched OA, it remains a very good option as a donor graft to achieve the maximal benefit of direct bypass to the posterior MCA or PCA in select patients with MMD vasculopathy.
Suggested Readings
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Hayashi T, Shirane R, Tominaga T. Additional surgery for postoperative ischemic symptoms in patients with moyamoya disease: the effectiveness of occipital artery-posterior cerebral artery bypass with an indirect procedure: technical case report. Neurosurgery. 2009; 64(1):E195-E196, discussion E196
Khodadad G. Occipital artery-posterior inferior cerebellar artery anastomosis. Surg Neurol. 1976; 5(4):225-227
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