So far, there is no study answering the question of which type of surgical technique is practically the most useful in the treatment of adult patients with ischemic type moyamoya disease (MMD). We evaluated the efficacy of single barrel superficial temporal artery (STA)-middle cerebral artery (MCA) bypass in the treatment of adult patients with ischemic type MMD by retrospectively collecting clinical and radiological data.
A retrospective review identified 31 adult patients who underwent 43 single barrel STA-MCA bypass procedures performed for treatment of ischemic-type MMD between 2006 and 2014. The male to female ratio was 17:14 and the mean age was 41 years (range, 21-65 years). Peri-operative complications, angiographic and clinical outcomes were analyzed retrospectively.
The permanent neurological morbidity and mortality rates were 2.3% and 0%, respectively. During the observation period of a mean of 35 months (range, 12-73 months), 29 patients (93.5%) had no further cerebrovascular events and transient ischemic attack occurred in two patients (6.5%), resulting in an annual stroke risk of 2.2%. Follow-up computed tomography perfusion (CTP) (mean, 18.4 months after surgery) documented improved cerebral hemodynamics in the revascularized hemispheres (
Our results suggest that single barrel STA-MCA bypass with wide dural opening is safe and durable method of cerebral revascularization in adult patients with ischemic type MMD and can be considered as a potential treatment option for adult patients with ischemic type MMD.
The symptoms and signs of moyamoya disease (MMD) can be classified into 2 major etiological categories: those caused by brain ischemia (ischemic type) and those caused by the deleterious consequences of the compensatory fragile collateral vessels (hemorrhagic type). Clinically, symptoms of brain ischemia are usually found in MMD children, while transient or permanent brain infarction and intracranial hemorrhage are noted in MMD adults.
Between 2006 and 2014, a total of 43 single barrel STA-MCA bypass procedures in 43 surgical sessions were performed in 31 adult patients for treatment of ischemic type MMD by two surgeons (S.W.L., J.K.K.). Medical data were collected according to our protocol and reviewed retrospectively under approval of the institutional review board. The inclusion criteria were as follows: 1) patients treated by single barrel STA-MCA bypass surgery, aged ≥ 20 years; 2) diagnosis of definite or probable MMD via digital subtraction angiography (DSA)
All surgically treated patients underwent direct bypass only, without the addition of an indirect revascularization procedure, on the affected side after confirmation of hemodynamic impairment by SPECT and/or CTP. Unless the hemodynamic insufficiency was clearly verified on the opposite side, surgery was done only on the affected side. In the 28 patients presented with ischemic symptoms, bypass surgery was performed between three weeks and three months after a stroke or TIA (mean, 8.3 weeks). Patients who require treatments to both hemispheres are managed with staged operations, with an interval of 8-12 weeks between the two surgeries. Single barrel STA-MCA anastomosis with wide dural opening was performed in all cases. In case of bilateral bypass procedures, surgery was performed on the more symptomatic hemisphere first. Bilateral bypass procedures were performed in twelve patients with one surgical session per side.
Following a linear or curvilinear skin incision of the temporalis muscle, the parietal or frontal branch of the STA was carefully dissected for approximately 10 cm, starting from the external auditory meatus. A large craniotomy was performed more than 10 cm in diameter for wide dural opening. The arachnoid membrane was minimally dissected to expose suitable-sized cortical branches of the MCA as the recipient artery. End-to-side anastomosis of donor and recipient arteries used interrupted 10-0 sutures under an operating microscope. Patency of the anastomosis was confirmed intra-operatively using a hand-held Doppler probe. What kind of an indirect revascularization procedure did not add any more in addition to STA-MCA anastomosis. All patients received 325 mg of acetylsalicylic acid once per day post-operatively. After discharge, dual antiplatelet therapy of clopidogrel and acetylsalicylic acid was maintained for at least three months.
For evaluation of clinical outcome, procedure-related complications including postoperative stroke and subsequent ipsilateral stroke beyond 30 days were checked. Postoperative stroke was defined as either infarction or intracerebral hemorrhage, intraventricular hemorrhage, and subarachnoid hemorrhage that developed during the surgery or within 30 days after the surgery. Brain MRI and computed tomography (CT) were performed in cases where the neurological status declined at any time. The preoperative angiographic stage was evaluated according to Suzuki grade.
Single barrel STA-MCA anastomosis with wide dural opening was technically successful in all 43 hemispheres.
During the observation period, with a mean of 35 months after surgery (range, 12-73 months), there were no further cerebrovascular events in 29 patients (93.5%). Two patients (6.5%) experienced a subsequent TIA. In these two patients, further evaluation did not reveal the exact cause and the TIA was an isolated event without further ischemic events. In sum, stroke recurrence occurred in two patients (6.5%), resulting in an annual stroke risk of 2.2%.
Digital subtraction angiography prior to surgery was available to review in all 31 patients. Six patients had probable MMD and underwent revascularization of the affected hemisphere only. Among 25 patients with bilateral MMD, bilateral bypass procedures were performed in 12 patients. Severity of MMD was quantified with Suzuki stage (I-VI, with Stage VI the most severe). The majority of the affected hemispheres (54/56, 96.4%) had Suzuki Stage III-V, and the average Suzuki stage of the study cohort was 4.1.
Follow-up imaging (DSA, MR angiography, or CT angiography) was performed in all 43 revascularized hemispheres to assess patency of the bypass. These studies were performed between two and 59 months after surgery (mean, 16.5 months). Post-operative patency was clearly verified in 38 bypasses (88.4%), while five bypasses (11.6%) were not patent or questionably patent. Post-operative strokes or TIAs did not occurred during the follow-up period in these five patients with occluded bypasses. Although bypasses were not patent or questionably patent in five cases, spontaneous anastomosis, as a result of indirect revascularization, appeared to be helpful in improvement of perfusion in four cases (80.0%).
In all 43 revascularized hemispheres, reduced regional CVR was proven by SPECT examinations using acetazolamide challenge preoperatively. In the current series, SPECT examinations were performed pre/post-operatively to evaluate cerebral hemodynamics and revealed improved cerebral hemodynamics after surgery in most cases. However, this result was excluded from the analysis because of the evaluation method of visual assessment, somewhat less objective. Complete sets of CTP results (pre-operative and follow-up) were obtained for 28 patients with 40 revascularized hemispheres in order to assess changes in CBF, CBV, time to peak (TTP), and mean transit time (MTT). If a patient had two or more CTP studies after bypass surgery, only the last post-operative study was included in this analysis. These radiological exams were performed between six and 42 months after surgery (mean, 18.4 months). The difference of CTP parameters between pre-operative and follow-up is summarized in
MMD presents with various cerebrovascular events, including TIAs, ischemic stroke, intracranial hemorrhage, headache, or seizures. In adult MMD, approximately half of the patients have intracranial hemorrhage, and the rest of the patients have TIA or cerebral infarct.
In previous reports, it is well recognized that surgical revascularization using direct and/or indirect bypass provides an improved outcome in patients presenting with the ischemic type,
Recently, the use of combined direct and indirect [encephaloduroarteriosynangiosis or encephalomyosynangiosis] bypass has been advocated as the optimal treatment in adult MMD.
After the trial and error to reduce postoperative morbidity, since January 2006, we have continued to perform single barrel STA-MCA bypass with wide dural opening, without the addition of an indirect revascularization procedure (wide dissecting of arachnoid membrane, inverting dura matter, suturing temporalis muscle to the dura, and the placement of the pericranial flap), as primary treatment for adult MMD. In present series, postoperative stroke was observed in three instances in 43 procedures (6.9%). A recent randomized trial (Carotid Occlusion Surgery Study) reported very high 30-day rates for ipsilateral ischemic stroke (14.4%) after STA-MCA bypass in patients with symptomatic atherosclerotic internal carotid artery occlusion.
The consistent surgical method of single barrel STA-MCA direct bypass only, without the addition of an indirect revascularization procedure, used in this study allowed us to demonstrate the effectiveness of surgical treatment in adult patients with ischemic-type MMD. In this study, we performed 43 surgeries in 31 adult MMD patients with hemodynamic impairment. There were two delayed TIAs (6.5%), and 93.5% (29/31) had no further ischemic or hemorrhagic events after a mean follow up period of 35 months, resulting in an annual risk of 2.2%. No deaths by stroke occurred in this series. Considering the fact that these two TIAs were an isolated event, all patients had a favorable outcome beyond one month after surgery. These midterm outcome in present study compare favorably with other reported series of combined revascularization surgery for adult patients with MMD, although the results should be interpreted with caution because the current study has the major flaws of its retrospective feature and the lack of a control group.
The current study has several limitations. First, this study examined a small number of patients. Second, it was a retrospective observational study. There may have been bias in patient selection and demographics. Third, the follow-up period was not sufficient. MMD is a gradually progressive lesion, and therefore much longer-term follow-up is necessary to investigate the progress of MMD after revascularization. Nonetheless, our findings suggest that single barrel STA-MCA bypass with wide dural opening appears to be a effective treatment strategy in adult patients with ischemic type MMD, given suitable levels of institutional and operator expertise, although these findings should be confirmed by a meta-analysis using large-scale retrospective studies that include a control group.
Our results suggest that single barrel STA-MCA bypass with wide dural opening is safe and durable method of cerebral revascularization in adult patients with ischemic type MMD and can be considered as a potential treatment option for adult patients with ischemic type MMD. Further studies with larger patient series and a longer follow up period will be helpful in elucidation of both the efficacy and the longevity of this treatment.
Characteristics | n = 31 |
---|---|
Age (years) | 41 ± 11 (21-65) |
Gender | |
Male | 17 (55) |
Female | 14 (45) |
Bilateral moyamoya | |
Yes | 25 (81) |
No | 6 (19) |
Initial presentations | |
TIA | 4 (13) |
ACI | 27 (87) |
Initial Suzuki angiographic stage | |
3 | 15 (35) |
4 | 22 (51) |
5 | 17 (39) |
6 | 2 (5) |
Bilateral bypasses | |
Yes | 12 (39) |
No | 19 (61) |
Values presented as the mean ± standard deviation (range) or the number of hemispheres (%).
N = number of patients; TIA = transient ischemic attack; ACI = acute cerebral infarction
Patient No. | Age/Sex | Symptom onset | Symptoms | Radiologic findings | Results |
---|---|---|---|---|---|
1 | 45/M | POD 5 | Dysarthria | ACI | Full recovered |
2 | 39/M | POD 11 | Motor aphasia | ACI | Full recovered |
3 | 51/F | POD 13 | Left hemiparesis | ACI | Partial recovered |
4 | 39/M | POD 5 | Motor aphasia, Seizure | EDH | Full recovered |
POD = postoperative day; ACI = acute cerebral infarction; EDH = epidural hematoma
Variable | Pre-operative | Follow-up | Ratio (Pre-operative/Follow-up) | |
---|---|---|---|---|
CBF | 48.29 ± 9.91 | 53.52 ± 10.76 | 1.11 | 0.019 |
CBV | 3.23 ± 3.23 | 3.24 ± 3.24 | 1.01 | 0.429 |
TTP | 12.18 ± 4.36 | 11.55 ± 2.36 | 0.95 | 0.006 |
MTT | 5.01 ± 1.31 | 4.47 ± 1.13 | 0.89 | 0.001 |
Values are presented as mean ± standard deviation.
CTP = computed tomography perfusion; CBF = cerebral blood flow; CBV = cerebral blood volume; TTP = time to peek; MTT = mean transit time