Moyamoya disease is a progressive cerebrovascular. Pial synangiosis in patients with moyamoya younger than 2 years of age.
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1 J Neurosurg Pediatrics 13: , 2014 AANS, 2014 Pial synangiosis in patients with moyamoya younger than 2 years of age Clinical article Eric M. Jackson, M.D., Ning Lin, M.D., Sunil Manjila, M.D., R. Michael Scott, M.D., and Edward R. Smith, M.D. Department of Neurosurgery, Children s Hospital Boston, Harvard Medical School, Boston, Massachusetts Object. Patients with moyamoya who are younger than 2 years of age represent a therapeutic challenge because of their frequent neurological instability and concomitant anesthetic risks. The authors report their experience with pial synangiosis revascularization in this population. Methods. The authors reviewed the clinical and radiographic records of all patients with moyamoya in a consecutive series of patients under 2 years of age, who underwent cerebral revascularization surgery using pial synangiosis at a single institution. Results. During a 12-year period ( ), 34 procedures (bilateral in 15 patients, unilateral in 4) were performed in 19 patients younger than 2 years (out of a total of 456 procedures in 240 patients). Eighteen of these patients presented with either stroke or transient ischemic attack. The average age of the 19 patients at first surgery was 1.4 years (range 6 months 1.9 years). Unanticipated staged operations occurred in 3 patients, due to persistent electroencephalographic changes during the initial surgery in 2 cases and due to brain swelling during the procedure requiring ventriculostomy in the other. There were 2 perioperative strokes; both patients had postoperative seizures but made clinical recoveries. The average follow-up was 7 years (range 1 14 years). Long term, at follow-up, 13 patients (68%) were clinically independent for their age, with 8 (42%) having no significant deficit. Late complications included subdural hygroma evacuation (1), additional revascularization procedures performed years later for frontal lobe ischemia (2), late infarction (1), and asymptomatic ischemic change on routine follow-up MRI studies (1). All patients who had both pre- and postoperative angiography demonstrated progression of disease. Conclusions. Despite the challenges inherent to this population, the majority of children with moyamoya under the age of 2 years have a good long-term prognosis. The data from this study support the use of pial synangiosis as a safe, effective, and durable method for treatment of moyamoya for most children in this potentially high-risk population. ( Key Words pial synangiosis moyamoya pediatric vascular disorders Abbreviations used in this paper: DSA = digital subtraction an giography; EDAS = encephaloduroarteriosynangiosis; EEG = electroencephalographic; IRB = institutional review board; mrs = modified Rankin Scale; STA = superficial temporal artery; TIA = transient ischemic attack. Moyamoya disease is a progressive cerebrovascular arteriopathy and a common cause of stroke in the pediatric population. 9,14 It is characterized by stenosis and occlusion of the distal internal carotid arteries and, less often, the proximal anterior cerebral and middle cerebral arteries. Associated with the stenosis is the development of collateral vessels from perforating arteries at the base of the brain, which gives the puff of smoke appearance. Surgical revascularization of the ischemic cerebral hemispheres, either with direct or indirect methods, significantly improves the long-term outcome for children with moyamoya. 3,5,6,10,13,15,16 Young children with moyamoya have been historically thought to be the most severely affected and most challenging to treat subgroup of all moyamoya patients. 5,8,12 The clinical course in these patients is frequently dynamic and rapidly progressing, leading to major strokes on presentation and poor eventual outcome. Furthermore, infants with moyamoya have severely compromised cerebrovascular reserve and are usually felt to have increased anesthetic risks. 17 Despite the fact that aggressive surgical management is usually warranted, moyamoya surgery This article contains some figures that are displayed in color on line but in black-and-white in the print edition. 420 J Neurosurg: Pediatrics / Volume 13 / April 2014
2 Moyamoya patients under 2 years of age in patients less than 2 years of age is performed infrequently, and there is limited literature that separates out this youngest age group of moyamoya patients. Here we present a single-center experience in treating moyamoya patients younger than 2 years with pial synangiosis. Methods Patient Selection A consecutive surgical series of patients with moyamoya arteriopathy who underwent pial synangiosis from 1994 through 2005 was reviewed to identify all patients who were younger than 2 years at the time of surgery. All patients who underwent surgery within this time period were included. In accordance with an institutional review board (IRB)-approved protocol, medical records were retrospectively reviewed to determine patient demographic information, age at presentation and initial surgery, symptoms at presentation, comorbid conditions, results of radiographic studies, perioperative and late complications, and long-term outcomes. The modified Rankin Scale (mrs) score at late follow-up and the Matsushima Scale score on postoperative digital subtraction angiography (DSA) were used to evaluate the outcome of this cohort. All these data are collected routinely as part of an IRBapproved protocol and longitudinal moyamoya database. Surgery and Perioperative Management The technique of pial synangiosis has been described previously. 1 Briefly, the superficial temporal artery (STA) is mapped with Doppler ultrasonography, and an STA graft is isolated and dissected free. A craniotomy is performed in the frontotemporal region, and the dura mater is opened into multiple flaps. The arachnoid membrane is dissected widely to expose the pial surface, and the STA graft is sewn to the pia mater with 10 0 monofilament nylon sutures. The dura mater is left open to prevent constriction of the arterial graft and to provide additional surface area for collateralization from meningeal vessels. Patients routinely are administered aspirin right up to the day of surgery and resume on postoperative Day 1. Patients who present with bilateral disease and require treatments to both hemispheres are usually operated bilaterally under a single anesthesia, assuming no operative or anesthetic complications or electroencephalographic (EEG) changes. Postoperative DSA is routinely performed 1 year after synangiosis surgery. Results Demographics A total of 240 patients were operated on for moyamoya during the study period. Nineteen (8%) of those patients were under 2 years of age at the time of their first operation and were included in the study. The demographic and clinical characteristics of the study cohort are summarized in Table 1. There were 11 female and 8 male patients in the group. Their average age at presentation was 1.1 years (range 2 months 1.7 years). Their average J Neurosurg: Pediatrics / Volume 13 / April 2014 age at the time of their first surgery was 1.4 years (range 6 months 1.9 years). A number of patients had associated diseases: 3 had neurofibromatosis Type 1, 2 had Noonan syndrome, and 1 had Alagille syndrome. Three patients had other vascular diseases 2 had cutaneous hemangiomas and 1 had a facial arteriovenous malformation. Moreover, there were familial associations in the study cohort 2 patients included were siblings and 1 patient had a mother with surgically treated moyamoya. Presentation Eighteen of the patients presented with evidence of cerebral ischemia (Table 2). Seventeen patients had clinical and imaging evidence of infarction. Four patients presented initially with seizures and were noted to have infarction on the imaging workup for the seizures. One patient had crescendo transient ischemic attacks (TIAs) with deep white matter changes on imaging. The remaining patient in the study group was worked up secondary to family history (2 siblings with moyamoya). She was noted to have significant asymptomatic disease and underwent prophylactic surgery. Operative Treatment All patients in the series underwent pial synangiosis as described above. 1 Thirty-four treated hemispheres were included in this analysis, out of a total of 456 surgically treated hemispheres in the entire series of 240 pedi- TABLE 1: Clinical and demographic characteristics of the study cohort* Characteristic Value no. of patients 19 age at presentation mean 1.1 yrs range 2 mos 1.7 yrs age at 1st op mean 1.4 yrs range 6 mos 1.9 yrs sex female 11 (57.9%) male 8 (42.1%) bilateral moyamoya yes 17 (88.9%) no 2 (11.1%) associated disease/condition NF1 3 Graves disease 2 Noonan syndrome 2 Alagille syndrome 1 facial AVM 1 hemangioma 2 * Values represent numbers of patients (%) unless otherwise indicated. AVM = arteriovenous malformation; NF1 = neurofibromatosis Type
3 E. M. Jackson et al. TABLE 2: Presenting symptoms in 19 patients with moyamoya disease younger than 2 years of age Presenting Symptom No. of Patients (%) TIA 18 (94.7) stroke 17 (89.5) seizure 4 (21.1) hemorrhage 0 (0.0) asymptomatic 1 (5.3) atric patients treated during this time period. Two operated hemispheres were excluded from the study. In one of these cases, the patient had a second hemisphere operated upon in a staged fashion after her second birthday. In the other. the patient had a myosynangiosis during the same anesthesia session on the opposite side due to the absence of a donor vessel following earlier treatment of a facial hemangioma. Twelve patients had bilateral procedures during a single session of anesthesia (including dural synangiosis in 1 patient without donor vessel). Three patients had staged bilateral procedures (one procedure was performed after 1 patient s second birthday). Four patients had unilateral procedures. Perioperative Complications Three patients underwent unanticipated staged procedures. Two patients had the second hemisphere treated in a staged procedure because of persistent EEG changes during the initial surgery. The third patient had significant brain swelling after the first operation requiring the placement of an external ventriculostomy drain (Table 3). Two patients developed perioperative infarcts, both of whom presented with seizures 12 hours postoperatively in one case and 36 hours postoperatively in the other. Both patients had immediate CT scans that demonstrated infarction. At the time of the operation, the first patient was noted to have an area of white, devascularized brain that was larger than the preoperative scans had suggested; the exact cause of the new event could not be determined. The second patient who suffered a stroke was undergoing the staged second-side procedure following an initial synangiosis that was complicated by EEG changes and brain swelling, suggesting that this patient had marked cerebrovascular instability under anesthesia. TABLE 3: Perioperative and delayed complications after pial synangiosis in 19 patients with moyamoya disease younger than 2 years of age Variable No. of Patients (%) perioperative complications persistent EEG change 2 brain swelling 1 seizures 2* infarction 2 delayed complications during follow-up hematoma evacuation 1 repeat synangiosis 2 infarction 1 asymptomatic MRI change 1 death 0 long-term outcome favorable (mrs 0 2) 13 (68.4%) unfavorable (mrs 3 6) 6 (31.6%) * In both cases, workup demonstrated infarction. Radiographic Outcome After Hospital Discharge Complete pre- and postoperative angiographic data with Suzuki grades 18 were available for 6 patients (11 hemispheres). All 6 patients (10 of 11 hemispheres) demonstrated progression of disease on postoperative DSA at 1 year after synangiosis surgery (Fig. 1). The 1 hemisphere that did not demonstrate progression had been graded 4 5 preoperatively. While we recommended postoperative DSA to all patients, some parents declined the procedure. As a result, data on 19 hemispheres in 10 patients were available to assess the development of collaterals following synangiosis surgery (Fig. 1). Eleven hemispheres were considered Matsushima A (57.9%); 6 were considered B (31.6%); and 2 were considered C (10.5%). 11 Clinical Outcome at Long-Term Follow-Up Outcomes (clinical and radiological) were reviewed with an average follow-up period of 7 years (range 1 14 years). Patients had an mrs score 15 calculated based on their most recent clinic note. Of the 19 patients, 8 had a score of either 0 or 1, 5 had a score of 2, 3 had a score of 3, 4 had a score of 4, and 0 had a score of 5 or 6 (Fig. 2). Thirteen patients (68.4%) were clinically independent for their age, with 8 (42.1%) having no significant deficit. Overall, 18 patients (94.7%) had improved or stable neurological status at follow-up compared with that prior to surgery. Delayed complications during follow-up are summarized in Table 3. No patient died during the followup period (mortality 0%). Of the 19 patients, 3 had additional neurosurgical procedures. One patient who had initially presented with significant bilateral infarcts and had undergone surgery on an urgent basis returned to the operating room 1 year later for drainage of subdural fluid collections, which were found to be under low pressure. Two other patients underwent repeat synangiosis for persistent TIA symptoms in the anterior cerebral artery territory. One patient had a right frontal pericranial synangiosis performed 4 years later. Of note, this hemisphere had been treated in a nonstandard fashion because of the absence of a donor vessel due to a facial hemangioma. The other patient returned to the operating room twice, for right frontal pericranial synangiosis 5 years after the original surgery and for right frontotemporal and parietotemporal dural synangiosis 8 years after the original surgery. One patient had a late infarct, presenting with right foot weakness 4 years postoperatively with evidence of 422 J Neurosurg: Pediatrics / Volume 13 / April 2014
4 Moyamoya patients under 2 years of age Fig. 1. Illustrative case involving an 18-month-old boy with bilateral moyamoya treated with bilateral pial synangiosis. The patient presented with seizures, and brain MRI demonstrated infarction (arrow) on T2-weighted sequence (A) and slow cortical flow ( ivy sign, arrowheads) on FLAIR sequence (B). Preoperative DSA showed moyamoya arteriopathy in both hemispheres, with Suzuki Grade III on the right (C) and Grade II on the left (D). (The arrows indicate changes typical of the respective grades.) Postoperative injections from the external carotid arteries showed significant collaterals developed around the pial synangiosis, with Matsushima Grade A revascularization in both hemispheres (E and F). infarction on CT. These symptoms improved with time. An additional patient was noted to have new asymptomatic ischemic T2 signal changes on follow-up MRI. Discussion In this patient series, we chose a 2-year age cutoff to define a moyamoya patient population that we and others have noted to frequently have a fulminant clinical course and a poor long-term prognosis. Other measures to define this high-risk population, such as patient weight or radiographic measures of brain development, such as myelination status, might be equally useful Young children with moyamoya usually present with a severe ischemic burden and advanced arteriopathy and are frequently noted to have a poor prognosis. 5,6,8,12 Matsushima et al. 12 studied mental and cognitive outcomes following encephaloduroarteriosynangiosis (EDAS) in pa tients with onset of disease before 5 years of age. They found that children who presented at less than 2 years of age had a poor mental prognosis, with 7 of 8 patients having an IQ less than 80 (less than 61 in all 7 cases). Kim et al. 8 demonstrated that patients younger than 3 years had a higher rate of infarction at presentation (87%) and lower J Neurosurg: Pediatrics / Volume 13 / April 2014 rate of favorable outcome (58%) than older pediatric populations. Moreover, 39% of patients (9 of 23) in this age group (0 3 years of age) had additional infarctions while awaiting surgery, suggesting a rapidly progressive clinical course. 8 Our data were consistent with these prior reports and showed that children with moyamoya under 2 years of age presented with advanced disease. Eighteen (94.7%) Fig. 2. Modified Rankin Scale scores during long-term follow-up for patients who presented with moyamoya at less than 2 years of age. The x-axis indicates mrs scores; the y-axis percentages of patients. 423
5 E. M. Jackson et al. of the patients in the study presented with symptoms and imaging findings consistent with significant ischemia. The single patient without significant ischemia had been screened secondary to significant family history. Moyamoya disease in very young children (under 2 years of age) poses a significant challenge to the treating neurosurgeon. The small vascular caliber of donor vessels usually renders direct bypass technically challenging, and in these patients, indirect revascularization techniques are frequently used. Patients in this age group have markedly limited cerebrovascular reserve; as a result, it is essential to avoid hypotension, hypovolemia, and hyperthermia during induction and throughout the operation. Postoperatively, pain control is of vital importance to prevent persistent crying and hyperventilation. Additionally, we strongly believe that antiplatelet therapy should be given before and after surgery, and that intravenous fluid administration should be generous (1.5 times maintenance) postoperatively until the patient is able to tolerate good oral intake. Although our study cohort is small, the results suggest that pial synangiosis can be safely performed in children with moyamoya less than 2 years of age, although 2 patients in our series suffered perioperative strokes (rate of 10.5% per patient, 5.6% per treated hemisphere) despite careful attention to the perioperative treatment measures outlined above. There was no infectious complication or perioperative mortality. These results compare favorably to prior reports in the literature on moyamoya patients in a similar age group. In a large retrospective series, S. K. Kim et al. 8 divided 204 patients treated with EDAS into 3 age categories and reported a 17% perioperative stroke rate (4 of 23 cases) in patients under 3 years of age. S. H. Kim et al. 7 analyzed 90 children treated for moyamoya and found that age less than 3 years at time of operation was a significant factor associated with perioperative stroke (occurring in 5 [27.8%] of 18 cases). Postoperative angiography demonstrated Matsushima A-B revascularization in 89.5% of treated hemispheres in our series, which was similar to reports from our institution 15 and others 2 on children with moyamoya of all age groups. In the long-term follow-up, despite young age and advanced disease at presentation, most patients (13 [68.4%] of 19) had favorable outcomes and were functionally independent. These results, compared with the natural history of 65% 82% stroke risk over 5 years, 4,9 suggest that pial synangiosis can be an effective and durable method of treating moyamoya patients under 2 years of age. These clinical findings also support the notion that aggressive surgical management is necessary and essential to improve the outcome for moyamoya children in the very young age group. There are several limitations to be considered in interpreting these results. The study was a retrospective case series and sample size was small. Postoperative angiography was declined by some patients families, which could introduce additional selection bias. Nevertheless, our findings confirm that young children with moyamoya less than 2 years of age present with significant disease burden and ischemia. Conclusions Pial synangiosis is a safe, effective, and durable treatment for moyamoya patients under 2 years of age with a relatively low perioperative complication rate. Following synangiosis surgery, the majority of these patients have a favorable outcome and functional independence. Disclosure The authors report no conflict of interest concerning the materials or methods used in this study or the findings specified in this paper. Author contributions to the study and manuscript preparation include the following. Conception and design: Smith, Jackson, Lin, Scott. Acquisition of data: Smith, Jackson, Lin, Scott. Analysis and interpretation of data: Smith, Jackson, Lin, Scott. Drafting the article: Smith, Jackson, Lin, Scott. Critically revising the article: all authors. Reviewed submitted version of manuscript: all authors. Approved the final version of the manuscript on behalf of all authors: Smith. Administrative/technical/material support: Smith. Study supervision: Smith, Scott. References 1. Adelson PD, Scott RM: Pial synangiosis for moyamoya syndrome in children. Pediatr Neurosurg 23:26 33, Golby AJ, Marks MP, Thompson RC, Steinberg GK: Direct and combined revascularization in pediatric moyamoya disease. Neurosurgery 45:50 60, Guzman R, Lee M, Achrol A, Bell-Stephens T, Kelly M, Do HM, et al: Clinical outcome after 450 revascularization procedures for moyamoya disease. Clinical article. J Neurosurg 111: , Hallemeier CL, Rich KM, Grubb RL Jr, Chicoine MR, Moran CJ, Cross DT III, et al: Clinical features and outcome in North American adults with moyamoya phenomenon. Stroke 37: , Imaizumi T, Hayashi K, Saito K, Osawa M, Fukuyama Y: Long-term outcomes of pediatric moyamoya disease monitored to adulthood. Pediatr Neurol 18: , Isono M, Ishii K, Kamida T, Inoue R, Fujiki M, Kobayashi H: Long-term outcomes of pediatric moyamoya disease treated by encephalo-duro-arterio-synangiosis. Pediatr Neurosurg 36:14 21, Kim SH, Choi JU, Yang KH, Kim TG, Kim DS: Risk factors for postoperative ischemic complications in patients with moyamoya disease. J Neurosurg 103 (5 Suppl): , Kim SK, Seol HJ, Cho BK, Hwang YS, Lee DS, Wang KC: Moyamoya disease among young patients: its aggressive clinical course and the role of active surgical treatment. Neurosurgery 54: , Kuroda S, Houkin K: Moyamoya disease: current concepts and future perspectives. Lancet Neurol 7: , Lin N, Baird L, Koss M, Kopecky KE, Gone E, Ullrich NJ, et al: Discovery of asymptomatic moyamoya arteriopathy in pediatric syndromic populations: radiographic and clinical progression. Neurosurg Focus 31(6):E6, Matsushima T, Inoue T, Suzuki SO, Fujii K, Fukui M, Hasuo K: Surgical treatment of moyamoya disease in pediatric patients comparison between the results of indirect and direct revascularization procedures. Neurosurgery 31: , Matsushima Y, Aoyagi M, Masaoka H, Suzuki R, Ohno K: Mental outcome following encephaloduroarteriosynangiosis in children with moyamoya disease with the onset earlier than 5 years of age. 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6 Moyamoya patients under 2 years of age ber G, et al: Management of stroke in infants and children: a scientific statement from a Special Writing Group of the American Heart Association Stroke Council and the Council on Cardiovascular Disease in the Young. Stroke 39: , Scott RM, Smith ER: Moyamoya disease and moyamoya syndrome. N Engl J Med 360: , Scott RM, Smith JL, Robertson RL, Madsen JR, Soriano SG, Rockoff MA: Long-term outcome in children with moyamoya syndrome after cranial revascularization by pial synangiosis. J Neurosurg 100 (2 Suppl Pediatrics): , Smith ER, Scott RM: Surgical management of moyamoya syndrome. Skull Base 15:15 26, Soriano SG, Sethna NF, Scott RM: Anesthetic management of children with moyamoya syndrome. Anesth Analg 77: , Suzuki J, Takaku A: Cerebrovascular moyamoya disease. Disease showing abnormal net-like vessels in base of brain. Arch Neurol 20: , 1969 Manuscript submitted May 17, Accepted January 10, The data reported in this manuscript were presented at the International Stroke Conference in New Orleans, Louisiana, February 1 3, Current affiliation for Dr. Jackson: Johns Hopkins University, Baltimore, Maryland. Please include this information when citing this paper: published online February 14, 2014; DOI: / PEDS Address correspondence to: Edward R. Smith, M.D., Department of Neurosurgery, Hunnewell 2, 300 Longwood Ave., Boston, MA edward.smith@childrens.harvard.edu. J Neurosurg: Pediatrics / Volume 13 / April
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