Surgical Techniques in Moyamoya Vasculopathy. Peter Vajkoczy

Chapter 20. Omental-Cranial Transposition

Mario Teo, Jeremiah N. Johnson, and Gary K. Steinberg


Selective moyamoya disease (MMD) patients have progressive neurological deterioration despite previous revascularization, and many have exhausted typical sources for bypass or have wide ischemic areas needing further revascularization. Omental-cranial transposition, a technique used sparingly, can be performed efficiently and safely. In this chapter, we highlight the steps and nuances in performing the laparoscopic omental harvest (which is better tolerated than laparotomy), the techniques used to ensure a thin, homogeneous, pedicled omental flap to provide wide cerebral hemispheric coverage, and illustrate with the appropriate case examples. We also include the preoperative workup, intraoperative strategies with step-by-step descriptions of key procedures, and postoperative management with long-term clinical and radiological outcome. With this method, we can achieve excellent angiographic revascularization and symptoms resolution for selective patients with resistant MMD.

Keywords: omental-cranial transposition, laparoscopic omental harvest, pedicled omental flap, resistant MMD, wide revascularization

20.1 Background

Revascularizations for moyamoya disease (MMD), either by direct or indirect procedures, are an accepted and effective treatment for the prevention of future ischemic events. However, small subsets of patients have persistent or new symptoms due to inadequate collateralization, hence, repeat revascularizations are performed. These repeat surgeries are technically more challenging due to scar tissue from the previous surgery, the meticulous attention required to avoid violating the previous bypass donor and its collateralization, and the lack of suitable local donor grafts. We describe the omental-cranial transposition as one of the rescue strategies that could be employed in these circumstances.

20.1.1 History

 1936—O’Shaughnessy sutured a pedicle of omentum to the heart.

 1962 to 1975—Vineberg explored clinical omental transposition to the heart.

 1973—Goldsmith et al described the first experimental omental-cranial flap in dogs to promote brain revascularization.

 1974 and 1977—Yasargil, Yonekawa, and their colleagues explored the use of omentum transplantation in animal models for the treatment of hydrocephalus and cerebral ischemia.

 1980—Karasawa et al described the first use of an omental flap in a patient with MMD who presented with ischemic symptoms. Anastomoses were made between the corresponding artery and vein of the superficial temporal and gastroepiploic vessels. The patient was free of ischemic attacks at 2 years follow-up.

20.2 Indications

 Revascularization of MMD in the absence of superficial temporal artery (STA), occipital artery or muscle donor.

 Large cortical surface areas to be revascularized, including bilateral hemispheres.

 Commonly employed strategy for repeat revascularization of MMD.

20.3 Key Principles

 Laparoscopic omental graft harvest in conjunction with the general surgeon.

 Preservation of gastroduodenal artery/vein and right gastroepiploic artery/vein blood supply.

 Careful delivery of the omentum to the cranial compartment.

20.4 SWOT Analysis

20.4.1 Strength

 Stretches and conforms easily to cover a large cortical area.

20.4.2 Weakness

 Technically challenging, potential associated morbidity with abdominal surgery.

20.4.3 Opportunity

 Stem cells in omentum produce angiogenesis-promoting cytokines, for example, vascular endothelial growth factor (VEGF) and basic fibroblast growth factor (bFGF).

20.4.4 Threat

 The viability of the omental graft could be compromised if the gastroepiploic artery is not preserved during harvest, or significant graft torsion occurs in the process of extraperitoneal omental delivery or tunneling to the cranial compartment.

20.5 Contraindications

 Previous complex abdominal surgery.

 Abdominal adhesion (peritonitis, peritoneal dialysis).

 Scarred down chest wall, difficulty with tunneling (relative contraindication).

20.6 Special Considerations

 History of previous major abdominal surgery should be carefully considered when contemplating omental- cranial harvest.

 Cortical areas to be revascularized: if located superior in the cerebral hemispheres (difficulty revascularizing using donor vessels due to inadequate length and small size of distal vessel), or a wide cortical surface area is to be reperfused (including bilateral hemispheres), the omental graft is a very good option.

20.7 Risk Assessment: Our Experience

At Stanford, we have performed 25 omental-cerebral transpositions for MMD (with 10 additional for non- MMD stroke patients).

 1991 to 2000: 9 cases with laparotomy for omental graft harvest (3 pedicled and 6 free grafts).

 2011 to 2016:16caseswith laparoscopic harvesting of pedicled omental grafts.

 In our laparoscopic omental-cranial transposition experience, 17 hemispheres in 16 patients were revascularized.

 Ages ranged from 5 to 45 years old, mean follow-up of 10.8 years (range: 1-27 years).

 Three patients had small postoperative diffusion weighted imaging (DWI) plus infarcts on MRI of the brain associated with contralateral arm and/or hand weakness, which recovered to preoperative baseline over 2 to 3 months. Two additional patients developed transient neurological deficits (TNDs) in the 30-day postoperative period that resolved.

 At the last follow-up, angiographic and MR findings of all cases showed patent grafts as well as viable omentum, and all patients experienced preoperative symptom resolution or improvement.

20.8 Preoperative Workup

Preoperatively, patients undergo a thorough medical, cardiac, and anesthetic assessment with routine preoperative labs and the relevant diagnostic imaging, including five-vessel cerebral angiogram, MRI of the brain, and cerebral perfusion imaging with and without Diamox (positron emission tomography, MR perfusion, CT perfusion, single-photon emission computed tomography [SPECT], transcranial Doppler). At our institution, we perform MR perfusion with and without Diamox, and patients who demonstrate poor cerebrovascular reserve (CVR) with steal phenomenon (indicating that the affected vascular territory is already maximally vasodilated to promote flow) are considered, especially patients of 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, each patient’s blood pressure is maintained at or above the preoperative baseline at all times.

20.8.1 Specific Consideration with Anticoagulation

 For patients with mechanical heart valves or recent venous thromboembolism, we would restart anticoagulation at 2 to 4 weeks postoperatively after a head CT confirmed no significant hemorrhage.

 Aspirin is continued through the preoperative day and restarted on postoperative day 1.

20.9 Patient Preparation

20.9.1 Patient Position with Skin Incision (Fig. 20.1)

 The laparoscopic surgical and neurosurgical teams work simultaneously.

 The patient is positioned supine.

 The head is positioned on a doughnut headrest to bring the cortical area to be revascularized uppermost.

 A transverse lower neck incision is made for tunneling of the omental graft from the peritoneal cavity to the cervical region over the chest wall. A retroauricular pocket is also created to connect the craniotomy site to the cervical incision.

 A lithotomy position is used.

 Laparoscopic port site insertion (three times), a subxiphoid incision is made to deliver the omentum after harvest.

20.10 Surgical Steps

20.10.1 Key Procedural Step 1: Omental Harvest (Fig. 20.2)

 Fig. 20.2a-c illustrates the key anatomical landmarks of the omental harvest stage. Fig. 20.2d-f shows the senior author’s early technique with open omental harvest.

 Laparoscopic omental harvest through working ports.

 Omentum dissected off the transverse colon, then splenic flexure (avoiding splenic vessel injury), and hepatic flexure.

 Dissection is along the greater curve of the stomach, preserving the right gastroepiploic artery and vein; the left gastroepiploic is cut.

 The pedicle is preserved at the pylorus.

20.10.2 Key Procedural Step 2: Delivery and Tunneling (Fig. 20.3)

 Subxiphoid incision (3-4cm) for omental delivery under direct vision, once the omentum is maximally mobilized.

 Omentum is inspected to identify its vascular supply and confirm patency of the arterial anastomotic arch of Barkow.

 To create a thin, homogeneous omental flap, the omentum is carefully divided between the epiploic arcades with step cuts.

 Subcutaneous tunnel from subxiphoid incision to a lower cervical incision is created using long lighted retractors and dissectors.

 Copious lubrication is used to facilitate the delivery of the omental graft to the low cervical area, then to the craniotomy site in step wise fashion.

 The subxiphoid incision is closed in multiple layers: abdominal fascia, subcutaneous tissue, and skin. The remaining abdominal port site incisions are closed in a subcuticular fashion.

20.10.3 Key Procedural Step 3: Craniotomy (Fig. 20.4)

 The incision and craniotomy should be designed to avoid damage to previous revascularization.

 A horseshoe cranial flap is performed for a large craniotomy.

 Dura is opened widely followed by wide opening of the arachnoid, and thin omental flap is placed over the entire exposed cortical surface area and secured to the dural edges using 4-0 sutures.

 If the contralateral hemisphere also undergoes revascularization, the remaining omental flap can be mobilized subcutaneously, and the same procedure repeated.

 Omental flow is demonstrated using a Doppler probe and indocyanine green (ICG) angiogram.

 The craniotomy bone flap is trimmed on the inferior aspects, and thinned on the inner table to avoid strangulation of the vasculature and mass effect over the cortex.

 The bone flap is secured using titanium miniplates, and the scalp closure is performed in multiple layers.

20.11 Tips, Pearls, and Lessons Learned

 Omentum is excellent for secondary revascularization in difficult MMD cases.

 Work with an experienced laparoscopic surgeon to ensure a safe omental harvest.

 A thin omental covering of cortex is best in order to avoid mass effect on the brain parenchyma; drill off the inner table of the skull plate to be replaced during closure.

 A postoperative angiogram should include gastroduodenal or celiac artery injection to assess graft patency. However, sometimes the omental graft parasitizes blood supply from chest or cervical arteries, decreasing the filling from the gastroepiploic artery.

20.12 Pitfalls

 An inadequate omental harvest due to injury to gastroepiploic or gastroduodenal arteries.

 Possible pedicle twisting during extraperitoneal delivery or the tunneling stage to the cranial compartment.

 Omentum that is too thick to place on the cerebral cortex, which could result in mass effect on the brain parenchyma when replacing the bone flap. We routinely thin the inner table of the skull flap, leaving only the outer table.

 Challenge of preserving the omental blood supply when trimming the omental flap for smaller cortical placement.

20.13 Bailout, Rescue, and Salvage Maneuvers

 Work with an experienced laparoscopic surgeon.

 Deliver and tunnel omental pedicle under direct vision to avoid twisting.

 Irrigate frequently to avoid dehydration and shrinkage of the omental flap.

20.14 Postoperative Care

20.14.1 Patient Surveillance

• First 24 hours after surgery:

∙ Patient is in the intensive care unit with regular neuro checks.

∙ Closely monitor hemodynamic status (fluid intake, output, electrolyte, and gastrointestinal function).

∙ Maintain thresholds for blood pressure (mean arterial pressure goals 90-110 to prevent hypoperfusion, TND, and hyperperfusion with potential postoperative hematoma).

• Analgesia and antiemetic.

 Day 2: Mobilize, observe oral intake, and transfer to regular ward care.

 Discharge from hospital when deemed to be safe by the neurosurgical and general surgical team (4-day average hospital stay).

 Post discharge: Educate and inform about TND, wound care, and subsequent follow-up plans.

20.14.2 Bypass Function Assessment

 Intraoperative omental bypass graft assessment using ICG angiogram and Doppler probe.

 Six-month postoperative digital subtraction angiogram including injection of celiac trunk, gastroduodenal artery and five-vessel cerebral angiograms, MRI brain including fluid-attenuated inversion recovery/DWI sequence, MRI perfusion without/with Diamox (to assess CVR), and neuropsychological testing.

 Long-term follow-up at 3,10, 20, and 30 years with clinical and radiological surveillance (investigations performed as listed at 6 month check).

20.15 Case Illustrations

20.15.1 Case 1

A 7-year-old girl had bilateral direct STA-middle cerebral artery (MCA) bypasses, after initially presenting with a left hemispheric stroke manifested by aphasia and right hemiparesis, and became asymptomatic for 5 years. She subsequently developed new-onset, left-body transient weakness with intermittent choreiform movements affecting her left arm and foot. MRI of the brain showed no new strokes but significantly reduced perfusion in the right MCA territory, posterior and superior to the region of her previous STA-MCA bypass. Her SPECT cerebral blood flow studies showed impaired perfusion and poor augmentation of the right hemisphere, including basal ganglia, consistent with impaired hemodynamic reserve after Diamox study. Cerebral angiography showed excellent revascularization of her left hemisphere with a patent bypass graft, and a right hemisphere mainly supplied by meningeal collateral vessels, with poor revascularization in the areas posterior and superior to the prior bypass graft (Fig. 20.5a, b). She underwent an uneventful right craniotomy and laparoscopic omental-cranial transposition to revascularize her right parietal region.

At 3 months after surgery she was free of transient ischemic attacks (TIAs) with resolution of the choreiform movements. A 6-month angiogram showed a gastroepiploic arterial supply along the course of the subcutaneous tunnel and excellent collateralization of the high right parietal area (Fig. 20.5c, d). An MRI of the brain at 6 months also showed reduced thickness of the omental flap compared to the immediate postoperative scan (Fig. 20.5e, f). A postoperative SPECT study at 6 months showed more symmetrical augmentation bilaterally after Diamox administration (Fig. 20.5g). She remained symptom free at the latest follow-up, and a delayed angiogram at 4 years showed that the underlying right STA-MCA bypass graft (Fig. 20.5h) and the omental-cranial transposition graft remained patent (Fig. 20.5i-k).

20.15.2 Case 2

A 5-year-old girl presented with progressive neurological deterioration 6 months after bilateral direct STA-MCA/ encephalo-duro-arterio-myo-synangioses (EDAMS) that were performed at an outside institution. Despite her previous treatment, she had persistent headaches with worsening motor and sensory (TIAs involving bilateral hemispheres). MRI and SPECT studies showed new bilateral ischemic lesions and reduced perfusion in the watershed areas, worse on the left. A cerebral angiogram showed progression of bilateral MMD, limited MCA collateralizations from previous bypasses, and lack of revascularization in bilateral high frontoparietal regions (Fig. 20.6a-d). She continued to deteriorate despite efforts to optimize her fluid status and blood pressure, and underwent bilateral omental-cranial transposition using a single pedicled, laparoscopic-harvested, vascularized omental flap.

She made an uneventful recovery, and was discharged on day 4 postoperatively. Her TIAs markedly reduced in frequency and severity 2 months after the omental-cranial transposition, and her 6-month angiogram showed excellent revascularization from the omental flap supplying bilateral superior MCA territories, and the gastroepiploic artery along the subcutaneous tunnel (Fig. 20.6e, f). Robust collateralization between the external carotid systems and the omental graft’s arterial supply was also seen.

She was symptom free at her 3.5 year follow-up with hypertrophy of the gastroepiploic artery supplying the brain parenchyma (Fig. 20.6g-j), and a thin layer of omental graft visible on an MRI of the brain (Fig. 20.6k).

20.16 Conclusion

Omental-cranial transposition as a rescue strategy for MMD patients with persistent or new symptoms after previous revascularizations is a versatile option with very good clinical outcome. Laparoscopic harvest of the omentum reduces the abdominal morbidity associated with the procedure, and the omental graft provides coverage for a large surface area of the brain hemisphere to be revascularized.

Suggested Readings

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Karasawa J, Kikuchi H, Kawamura J, Sakai T. Intracranial transplantation of the omentum for cerebrovascular moyamoya disease: a two-year followup study. Surg Neurol. 1980; 14(6):444-449

Karasawa J, Touho H, Ohnishi H, Miyamoto S, Kikuchi H. Cerebral revascularization using omental transplantation for childhood moyamoya disease. J Neurosurg. 1993; 79(2):192-196

Lee J, Steinberg GK. Omental to cerebral transposition for the treatment of cerebral ischemia. In: Goldsmith HS, ed. The Omentum. Woodbury, CT: Cine-Med, Inc.; 2010:137-149

Navarro R, Chao K, Gooderham PA, Bruzoni M, Dutta S, Steinberg GK. Less invasive pedicled omental-cranial transposition in pediatric patients with moyamoya disease and failed prior revascularization. Neurosurgery. 2014; 10(1) Suppl 1:1-14

Ya§argil MG, Yonekawa Y, Denton I, Piroth D, Benes I. Experimental intracranial transplantation of autogenic omentum majus. J Neurosurg. 1974; 40 (2):213-217

YonekawaY, Ya^argil MG. Brain vascularization by transplanted omentum: a possible treatment of cerebral ischemia. Neurosurgery. 1977; 1(3):256- 259

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