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Comparison of Direct and Indirect Bypass for Moyamoya Disease

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1 Comparison of Direct and Indirect Bypass for Moyamoya Disease
Jared Pisapia MGH Neurosurgery Grand Rounds September 23, 2010 My name is Jared Pisapia and I am visiting medical student from the University of Pennsylvania. Today I would like to present a comparison of direct and indirect bypass methods for patients with moyamoya disease.

2 Overview Moyamoya disease (MMD) Case presentation Clinical course
Surgical approach (EDAS) Revascularization options Indirect Direct Evidence supporting revascularization techniques As an overview, I will briefly review moyamoya disease (MMD) and then present the case of a patient undergoing an encephaloduroarteriosynangiosis (or EDAS). Although evidence suggests that surgical intervention improves patient outcomes in moyamoya disease, the most appropriate revascularization procedure is unclear. In the second half of the presentation, I will discuss alternative revascularization strategies, which can broadly be divided into indirect or direct procedures, and the evidence supporting their use.

3 MMD is a chronic cerebrovascular disorder characterized by progressive occlusion of the intracranial vessels, beginning in the intracranial carotid as shown by the red arrow and moving to the anterior, middle, and posterior cerebral arteries. As the arteries gradually stenose, a collateral network of capillaries develops at the base of the brain (blue arrowheads) to bypass the blockage, producing the characteristic reticulate appearance (“puff of smoke”) on cerebral angiography (red circle). Additional collateral vessels (green arrows) make their way into the brain from the surface.

4 Moyamoya Disease (MMD)
More common in Asian populations Incidence: < 1/100,000 Bimodal age of presentation Pediatric (Ischemia) Adults (Hemorrhage) Treatment – Revascularization Although more common in Asian populations, the incidence is still rare, and is less than 1 per 100,000. The disease has a bimodal age of presentation, with ischemia developing in children (first decade) because of inadequate collateral vessels and adults (fourth decade) presenting with intracranial hemorrhage due to the rupture of fragile collateral vessels. Revascularization is the primary treatment, as in the following case report.

5 Case Report JB is a 32 year old RH woman with PMH of congenital rubella syndrome referred by PCP to MGH ED for evaluation of R MCA stenosis Intermittent numbness: L facial (V2 and V3), R finger/toe x 1 month Episodes increased in frequency over prior year; lasting less than 20 min and resolving spontaneously JB is a 32 y/o RH woman with h/o congenital rubella syndrome c/b pulmonic stenosis and L-sided blindness/deafness referred to MGH by her PCP for evaluation of R MCA stenosis. PTA the patient c/o L facial numbness (V2 and V3 distribution) and R finger/toe numbness intermittently over the preceding month. Worsening complaints prompted PCP to obtain outpatient brain MRI.

6 Case Report Outpatient MRI
multifocal stenoses in anterior and posterior circulation PMH/PSH: as above Meds: OCP FH: Ischemic stroke, 72 year old father SH: clerk, non-smoker An outpatient MRI revealed multifocal stenoses in the anterior and posterior circulation. Her PMH/PSH primarily relates to congenital rubella syndrome and only medication was an oral contraceptive. Neurological exam only significant for L horizontal nystagmus. Vasculitis w/u negative.

7 CTA Multiple intracranial stenoses
Bilateral involvement of the supraclinoid ICAs and ICA terminus Near-occlusion of right M1 segment with intact flow distally The patient was admitted to MGH and a CTA was performed, which revealed, multiple intracranial stenoses, especially bilateral involvement of the supraclinoid ICAs and ICA terminus, and near occlusion of the R M1 segment with intact distal flow.

8 Brain MRI > 3 small DWI and T2- hyperintense lesions
Recent infarcts Embolic or low-flow infarcts No evidence of ICH Brain MRI was repeated and showed at least three small DWI and T2 hyper-intense lesions in the right cerebral hemisphere, at the watershed region of the R ACA and MCA. No evidence of intracranial hemorrhage.

9 Hospital course She was placed on ASA 81 mg daily and her OCP was discontinued She was discharged without further symptoms Follow-up in Neurosurgery Clinic; scheduled for EDAS for revascularization The patient was placed on baby aspirin and her OCP was discontinued. She was discharged without symptoms and asked to follow-up in Neurosurgery Clinic, at which time she was scheduled for EDAS for revascularization.

10 Encephaloduroarteriosynangiosis (EDAS)
Transposition of a segment of superficial temporal artery (STA) to surface of brain Formation of spontaneous anastomoses between the arteries of the cerebral cortex, dura mater, and the scalp Encephaloduroarteriosynangiosis (EDAS) involves the transposition of a segment of a scalp artery onto the surface of the brain, with the objective of improving collateral blood flow by the formation of spontaneous anastomoses between the arteries of the cerebral cortex, dura mater, and scalp.

11 For surgery, the patient was placed supine in a Mayfield with the right side exposed as shown in this reconstruction. A Doppler probe was used to map out the course of the superficial temporal artery (STA). Under the microscope, the location of the STA was again confirmed and an incision was made along its course.

12 EDAS The STA was dissected free of surrounding soft tissue in the region of the superior temporal line. The artery was then dissected to the area just in front of the ear. A cuff of soft tissue was left adjacent to the vessel. HEAD

13 The needle tip Bovie was used to coagulate the soft tissue adjacent to the STA, so we were able to work underneath the artery to free it from its surrounding soft tissue.

14 Red vascular loops were passed and good mobilization of the STA was obtained.

15 We used a Bovie to incise the underlying fascia and muscle and used periosteal elevators to sweep muscle aside.

16 A burr hole was placed at the superior and inferior aspect of the exposed bone. The craniotome was used to create an ellipse shaped craniotomy.

17 The bone was then removed to expose the dura, and the dura was opened and reflected.

18 We then placed the artery on the pial surface and tacked it into position using 9-0 sutures.

19 We then used a pericranial graft to close the dura over the artery such that the dura held the artery to the pial surface. The bone flap was replaced and the wound was closed in layers.

20 Multiple Burr Holes Baaj et al., 2009
Next we created 2 separate incisions, one in the frontal region just behind the hairline and one in the high parietal region posteriorly. Burr holes were then drilled, and the dura was opened and left open to encourage collateral formation. The galea and skin were closed. The patient tolerated the procedure well, and she was discharged on POD #2 Baaj et al., 2009

21 Indirect Bypass: EDAS main trunk of the STA
posterior branch of the STA anterior branch of the STA galeal flap dura mater Several options exist for revascularization, and these techniques are broadly divided into the categories of indirect and direct. JB underwent an indirect procedure. As review, the posterior branch of the STA was laid on the brain surface, covered with galea and sutured to the pia.

22 Direct Bypass: STA-MCA bypass
STA-MCA bypass is an example of a direct bypass in which the superficial temporal artery and MCA are anastomosed. Baaj et al., 2009)

23 Direct and Indirect Bypass: STA-MCA Anastomosis + EMS.
Combination: b. posterior branch of the STA; c. anterior branch of the STA; f. temporal muscle; g. branch of the MCA; h. anastomosis The STA-MCA bypass may be combined with EMS, or encephalomyosynangiosis, in which a temporalis muscle flap (instead of dura) is laid over the anastomosis of the STA and MCA in the operative field. Over time, collateral vessels form between the blood-rich muscle and ischemic neural tissue. Matsushima et al., 1998

24 Additional Indirect Options
EMAS = EDAS + EMS EDAMS = EMAS + dura (includes middle meningeal artery) Multiple burr holes EMAS combines laying down vessel and laying down temporalis muscle. EDAMS combines both above aspects and also includes a galeal flap, which leads to middle meningeal artery involvement. Multiple burr holes may be used alone or in conjunction with other indirect options, as was performed in the case of JB. Whereas the above procedures lead to revascularization in the MCA territory, burr holes may be placed and encourage revascularization in the ACA or PCA territories. [Omental transposition requires midline abdominal laparotomy and preservation of the gastroepiploic vascular pedicle; an anastomosis is performed between the pedicle and STA, and the omentum is then spread over the cortical surface and under the edges of the exposed dura. Conservative management involves antiplatelet agents, anticoagulants, and calcium channel blockers; however, medical management does not appear to offer benefit.] Baaj et al., 2009; Chang SD, Steinber GK, 2010

25 Multiple Combined Indirect Bypass
Finally, multiple combined indirect bypass involves removal of the dura and covering of the dural defect with frontal muscle with the anterior branch of the STA (B) and an EDAS (laying the STA) and EMS (laying the temporalis) (C). Some consider STA-MCA bypass to be the optimal procedure for patients with moyamoya disease, but there is little evidence revealing the overall best treatment, which may be situation or patient specific. Next, I would like to discuss the evidence comparing direct and indirect approaches in terms of revascularization and outcome in various clinical settings. a. main trunk of the STA; b. posterior branch of the STA; c. anterior branch of the STA; d. galeal flap; e. dura mater; f. temporal muscle; Matsushima et al., 1998

26 Indirect vs. Combined vs. Direct Bypass
50 patients with pediatric MMD, 76 hemispheres, EDAS MCI STA-MCA N 12 22 16 Collateral vessel formation 44% 52% 74% Clinical improvement 56% 63% Complications 1 minor stroke 2 epidural hematomas 1 major & 1 minor stroke 50 MMD patients underwent indirect, combination, or direct revascularization with 3 postoperative outcome measures: Greater than two-thirds of postoperative collateral vessel formation was noted on the angiogram for 44, 52, and 74% in EDAS, MCI, and STA-MCA anastomosis patients, respectively. Symptoms resolved in 56, 63, and 74% of respective patients. Complications included: 1 minor stroke, 2 epidural hematomas, 1 major & 1 minor stroke, respectively The authors concluded that: Direct bypass (STA-MCA bypass) is associated with the highest postoperative collateral formation and clinical improvement. However, indirect bypass methods of EDAS and MCI were safer, and MCI led to the formation of collaterals in the ACA as well as the MCA distribution. Direct STA-MCA is associated with the greatest postoperative collateral formation and clinical improvement EDAS and MCI were safer, and MCI caused formation of collaterals in the ACA distribution and is best procedure in children Matsushima et al., 1998

27 Rebleeding in Hemorrhagic MMD
STA-MCA bypass in prevention of future stroke, including rebleeding or ischemia Conservative EDAS STA-MCA N 11 5 6 Ischemic or rebleeding event 3 Stroke-free time (years) 8.1 +/- 1.5 4.0 +/- 1.5 8.5 +/- 1.3 In a second study, authors evaluated the effects of STA-MCA bypass in the prevention of future stroke, including rebleeding or an ischemic event, in patients suffering from hemorrhage MMD by comparing this method to indirect bypass and conservative treatment. The study population consisted of 22 patients with hemorrhagic MMD but no aneurysm (age mean 43; f/u mean 8 years). Patients undergoing revascularization were treated at least one month after initial presentation. 9 (22%) had ischemic or rebleeding events during the follow-up period: Incidence of future stroke events in patients with STA-MCA bypass (0%) was lower than that with conservative management or EDAS. Stroke-free times longer for STA-MCA bypass (8.5 +/- 1.3 yrs) over EDAS (4 +/- 1.5 years) and conservative treatment (6.1 +/- 1.5 yrs) Recurrent intracranial hemorrhage and ischemic deficits occurred less frequently in patients who underwent STA-MCA bypass than in those who underwent EDAS. Therefore, the authors recommend STA-MCA bypass over indirect bypass for patients presenting with intracranial hemorrhage. Recurrent ICH occurred less frequently in patients undergoing STA-MCA bypass than those who underwent EDAS Authors recommend STA-MCA bypass over indirect bypass for patients presenting with intracranial hemorrhage Kawaguchi et al., 2000)

28 Adults vs. Pediatric; Ischemia
23 patients underwent indirect bypass 16 adults (mean 35, years old) 7 children (mean 10, 3-16 years old) Good collaterals on postoperative angiography 7/7 pediatrics, 7/16 adults Advancing age decreases development of collaterals through indirect bypass Direct bypass is main treatment option for patients > 40 years Although it is known that excellent collateral circulation can be achieved through indirect bypass for pediatric patients, the same is not known for adult patients with ischemic symptoms. 16 adults and 7 children underwent postoperative angiography at a median of 6 months. All pediatric patients showed good or moderate development of collaterals through the indirect bypass. Among the adult group, seven patients aged 20 to 29 had angiographic results similar to those of the pediatric group. On the other hand, nine patients older than 30 had results contrary to those of pediatric patients Advancing age may affect the development of collateral formation through the indirect bypass. Consequently, direct bypass is thought to be the main treatment option for patients older than 40.

29 Comparison of Direct versus Indirect
Indirect (EDAS) Direct (STA-MCA bypass) Useful if inadequate donor artery grafts At least several weeks required to form collaterals Easier and safer in patients with serious medical comorbities Technically difficult; size and progressive MCA occlusion Immediate revascularization Symptomatic cerebral hyperperfusion, although transient The following columns provide a comparison of characteristics of each bypass technique.

30 Conclusions The most appropriate revascularization procedure for patients with MMD is not fully defined. Case series are limited by inadequate power, selection bias, and inherent differences in patient characteristics. Choice of procedure may depend on surgeon’s experience, nature of symptoms, and patient age. Although patients with MMD appear to benefit from surgical revascularization, the optimal bypass technique is unclear. There have been no randomized trials to assess the efficacy of a single surgical treatment, and case series suffer from inadequate power, selection bias, and inherent differences in patient characteristics. Each procedure, direct and indirect revascularization will continue to play a major role in the treatment of MMD. The choice of procedure appears to depend on the surgeon’s comfort level and skill as well as on the nature of the patient’s symptoms, and age. Randomized prospective clinical trials comparing the various procedures may better define the most appropriate indications and use of these procedures.

31 References Baaj AA, Agazzi S, Sayed ZA, Toledo M, Spetzler RF, van Loveren H: Surgical management of Moyamoya disease: a review. Neurosurg Focus 26(4):E7, 2009 Kawaguchi S, Okuno S, Sakaki T: Effect of direct arterial bypass on the prevention of future stroke in patients with the hemorrhagic variety of moyamoya disease. J Neurosurg 93: , 2000. Matsushima T, Inoue T, Ikezaki K, Matsukado K, Natori Y, Inamura T, et al: Multiple combined indirect procedure for the surgical treatment of children with moyamoya disease. A comparison with single indirect anastomosis with direct anastomosis. Neurosurg Focus 5(5):4, 1998 Mizoi K, Kayama T, Yoshimoto T, Nagamine Y.:Indirect revascularization for moyamoya disease: is there a beneficial effect for adult patients? Surg Neurol 45:541-9, 1996. Starke RM, Komotar RJ, Connolly ES: Optimal surgical treatment for moyamoya disease in adults: direct versus indirect bypass. Neurosurg Focus 26(4):E8, 2009.

32 Acknowledgements Christopher S. Ogilvy, M.D. Brian V. Nahed, M.D.
Brian P. Walcott, M.D. Robert L. Martuza, M.D. Neurosurgery Department

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