Neurosurg Rev (2009) 32:245–249 DOI 10.1007/s10143-009-0184-6 CASE REPORT Cerebral ischemia owing to compression of the brain by swollen temporal muscle used for encephalo-myo-synangiosis in moyamoya disease Miki Fujimura & Tomohiro Kaneta & Hiroaki Shimizu & Teiji Tominaga Received: 17 June 2008 / Revised: 8 December 2008 / Accepted: 18 December 2008 / Published online: 22 January 2009 # Springer-Verlag 2009 Abstract Compression of the brain by swollen temporal muscle used for indirect pial synangiosis is a rare complication after the revascularization surgery for moyamoya disease, and its mechanism and clinical presentation are undetermined. A 26-year-old woman, who had been suffering transient ischemic attack (TIA), underwent superficial temporal artery-middle cerebral artery anastomosis with encephalo-myo-synangiosis (EMS) on the affected hemisphere. The 123I-IMP-SPECT 1 day after surgery demonstrated an improvement of cerebral blood flow (CBF) on the operated hemisphere. Two days later, however, she suffered fluctuating aphasia when computed tomography scan revealed marked swelling of the temporal muscle used for EMS. The 123I-IMP-SPECT 4 days after surgery showed significant decrease in CBF by the compression of the brain. Then, we performed revision of EMS. The base of the temporal muscle was markedly compressed by the edge of the free bone flap, which resulted in swelling of the entire temporal muscle used for EMS. We drilled out the edge of the free bone flap for decompression. Her aphasia disappeared postoperatively, and CBF normalized 7 days after the initial surgery. Her M. Fujimura (*) : T. Tominaga Department of Neurosurgery, Tohoku University Graduate School of Medicine, 1-1 Seiryo-machi, Aoba-ku, Sendai 980-8574, Japan e-mail: fujimur@nsg.med.tohoku.ac.jp T. Kaneta Department of Radiology, Tohoku University School of Medicine, Sendai, Japan M. Fujimura : H. Shimizu Department of Neurosurgery, Kohnan Hospital, Sendai, Japan TIA disappeared, and there was no deterioration during the follow-up period. The STA-MCA bypass has been patent since the initial surgery. Surgical revascularization including EMS has a substantial risk for cerebral ischemia owing to compression of the brain by temporal muscle swelling. Relative wide bone window for temporal muscle insertion is necessary to avoid this rare complication. Once the flow compromise is confirmed, we recommend early decompression by the revision of EMS. Keywords Moyamoya disease . Cerebral ischemia . Compression . Surgical complication . Indirect bypass Introduction Moyamoya disease is a chronic, occlusive cerebrovascular disease with unknown etiology characterized by bilateral steno-occlusive changes at the terminal portion of the internal carotid artery and an abnormal vascular network at the base of the brain [7, 11]. Surgical revascularization for moyamoya disease prevents cerebral ischemic attack by improving cerebral blood flow (CBF), and both direct bypass and indirect pial synangiosis are known as the standard surgical procedures for moyamoya disease [1, 3, 5, 8, 10]. Despite the favorable outcome of revascularization surgery for moyamoya disease, it is also reported to result in transient neurologic deterioration due to cerebral hyperperfusion or cerebral ischemia during the acute stage after surgery [1–5, 10]. Since indirect pial synangiosis such as encephalo-myo-synangiosis (EMS) requires the insertion of temporal muscle under the bone flap [8], it has a substantial risk for compression of the brain if it gets swollen [12, 13]. However, the detail of such complication has not been reported except for the limited cases including the chronic stage after 246 Neurosurg Rev (2009) 32:245–249 A 26-year-old woman, who had been suffering from transient ischemic attack (TIA) during the past 10 years, was admitted to our service. Neurological examination found no abnormality, and initial magnetic resonance angiography (MRA) demonstrated steno-occlusive changes at the terminal portion of the bilateral internal carotid arteries (Fig. 1a). Fluid attenuated inversion recovery (FLAIR) by magnetic resonance imaging (MRI) found “ivy sign” predominantly on the left hemisphere, while there was no cerebral infarction (Fig. 1b). Preoperative 123IIMP-SPECT found that her CBF and cerebrovascular reactivity were markedly compromised on the left hemisphere (Fig. 1c). Digital subtraction angiography confirmed the diagnosis of moyamoya disease (data not shown). Based on the diagnosis of moyamoya disease with apparent flow compromise and ischemic symptoms, she underwent superficial temporal artery-middle cerebral artery (STAMCA) anastomosis with EMS on the left hemisphere [1]. The patency of the STA-MCA bypass was confirmed by IRIS-V infrared imaging system during surgery [9], and the postoperative 123I-IMP-SPECT showed increase in CBF on the operated hemisphere (Fig. 2b) compared to the preoperative finding (Fig. 1c). The patient did not suffer neurologic deficit immediately after surgery. Postoperative MRA showed the apparently patent STA-MCA bypass as a thick high signal intensity sign and diffusion weighted image showed no evidence of ischemic change (data not shown). Two days later, however, she suffered from fluctuating aphasia. The computed tomography (CT) scan revealed marked swelling of the temporal muscle used for indirect pial synangiosis which compressed the surface of the left brain (Fig. 2c). The 123I-IMP-SPECT 4 days after surgery showed significant decrease in CBF by the compression of the brain (arrows in Fig. 2d). Based on these findings, we considered that her aphasia was due to cerebral ischemia owing to compression of the brain by swollen temporal muscle used for EMS. Then, we performed revision of indirect bypass 4 days after initial surgery. The base of the temporal muscle was markedly compressed by the edge of the free bone flap, which resulted in swelling of the entire temporal muscle flap used for EMS. We drilled out the edge of the free bone flap and designed relatively wide bone window. We also drilled out the inner layer of the free bone flap for further decompres- Fig. 1 Preoperative MRA (a), FLAIR of MRI (b), and 123I-IMPSPECT at rest (c); steno-occlusive changes at the terminal portion of the internal carotid artery were evident bilaterally (a). FLAIR demonstrated “ivy sign” predominantly on the left hemisphere, while there was no cerebral infarction (b). CBF was decreased in the MCA and ACA territories on the left hemisphere surgery [12, 13]. Here, we report a case of moyamoya disease which manifested as cerebral ischemia owing to compression of the brain by swollen temporal muscle used for EMS during the acute stage after direct–indirect revascularization surgery. Time sequential performance of N-isopropyl-p-[123I] iodoamphetamine single-photon emission computed tomography (123I-IMP-SPECT) allowed us to reveal the cerebral hemodynamics during and after this rare complication and provided important information to decide the timing for the revision of EMS. Case report Neurosurg Rev (2009) 32:245–249 Fig. 2 Temporal profile of CT (a, c, e) and 123I-IMP-SPECT (b, d, f) at 1 day (a, b), 4 days (c, d), and 1 week (e, f) after left STA-MCA anastomosis with indirect pial synangiosis; CBF was increased on the operated hemisphere as early as 1 day after surgery (b), but it markedly reduced 4 days after surgery (arrows in d) when 247 compression of the brain by swollen temporal muscle was apparent by CT (arrows in c). Revision of indirect bypass with bone flap drilling relieved the compression (e), and CBF was significantly increased after decompression (f) Fig. 3 Postoperative MRA (a) and MRI (FLAIR) (b) 3 months after revascularization surgery demonstrating that left STA-MCA bypass and the branches of left MCA were well visualized (arrow in a) and that ivy sign on the left hemisphere was disappeared 248 sion. Her aphasia was relieved postoperatively and CBF normalized 7 days after initial surgery (Fig. 2f). Her TIA completely disappeared after surgery, and there was no cerebrovascular event during the follow-up period. The MRA 3 months after surgery demonstrated STA-MCA bypass as a thick high signal (Fig. 3a) There was no brain damage on the operated hemisphere, and the ivy sign disappeared by FLAIR (Fig. 3b), suggesting the improvement of cerebral ischemia. Discussion The present case indicated that the indirect revascularization procedure for moyamoya disease has a substantial risk for cerebral ischemia owing to compression of the brain by temporal muscle used for EMS during the acute stage after surgery, even when it is performed in combination with direct revascularization procedure. Since recent evidence suggests that surgical revascularization for moyamoya disease could result in temporary neurologic deterioration due to cerebral hyperperfusion during the acute stage after surgery [1–4, 10], it is clinically important to make accurate diagnosis of cerebral hyperperfusion and cerebral ischemia [1], especially when the compression of the brain was suspected by CT or MRI. Clinical presentation of cerebral hyperperfusion in moyamoya disease mimics that of cerebral ischemia, while the management of hyperperfusion is contradictory to that of ischemia [1, 4]. Based on these observations, we have stressed the importance of routine postoperative CBF measurement during the acute stage after revascularization surgery for moyamoya disease [1–3]. In the present case, time sequential 123I-IMP-SPECT allowed us to monitor the alteration of cerebral hemodynamics and provided important information to decide the timing for the revision of EMS. In fact, CBF normalized after the revision of EMS, and the patients was discharged without neurologic deficit. Thus, we recommend CBF analysis during the acute stage after revascularization surgery for moyamoya disease, when the patients manifest as neurologic sign after surgery. A variety of techniques of indirect revascularization procedure such as EMS [1, 13], encephalo-duro-arteriosynangiosis [8], and multiple burr holes surgery [6] has been reported previously. The combination surgery of direct and indirect revascularization procedures has been getting more standard [1, 3, 5, 9] in light of the observation that the indirect techniques may further improve the postoperative cerebral hemodynamics by additional revascularization form meddle meningeal artery and/or deep temporal artery in wider territory on the ischemic hemisphere [5, 8]. Since we employed EMS in combination with STA-MCA anastomosis, which is one of the most common and Neurosurg Rev (2009) 32:245–249 minimally invasive indirect bypass techniques, we consider that the most of the indirect revascularization procedures have a substantial risk for the similar complication. Alternatively, multiple-burr-holes surgery could be a treatment of choice to avoid such complication [6] when it is employed without direct procedure. The exact mechanism by which the temporal muscle swelling occurred in the present case is undetermined. Venous congestion caused not only by the mechanical compression of the temporal muscle at the site of the insertion but also by the coagulation of the venous system of the temporal muscle during the manipulation may play a critical role in the pathophysiology of the temporal muscle swelling. Thus, it would be particularly important to preserve venous structure on the temporal muscle as well as to construct wider bone window at the site of temporal muscle insertion during this procedure for avoiding this rare complication. Indirect revascularization procedure including EMS was reported to be effective especially in patients with childhood moyamoya disease [8], but this procedure has not been well discussed from the cosmetic viewpoint. Bone window for the insertion of temporal muscle used as EMS could result in linear indentation and thus cause aesthetic complaint especially in children and young women with moyamoya disease. The present case was a 26-year-old woman who had just married, and we do not rule out the possibility that minimization of the bone window for temporal muscle insertion in the present case might cause, in part, the compression of the temporal muscle base and, thus, result in marked swelling of the entire temporal muscle flap. Based on our findings, we recommend to drill out the inner layer of bone flap as well as to keep thorough bone window to avoid the risk for this rare complication, as long as the bone window is located behind the hair line. This issue remained to be solved in the future modification of surgical procedure for moyamoya disease also from the aesthetic viewpoint. References 1. Fujimura M, Kaneta T, Mugikura S, Shimizu H, Tominaga T (2007) Temporary neurologic deterioration due to cerebral hyperperfusion after superficial temporal artery-middle cerebral artery anastomosis in patients with adult-onset moyamoya disease. Surg Neurol 67:273–282 2. Fujimura M, Kaneta T, Shimizu H, Tominaga T (2007) Symptomatic hyperperfusion after superficial temporal artery-middle cerebral artery anastomosis in a child with moyamoya disease. Childs Nerv Syst 23:1195–1198 3. Fujimura M, Kaneta T, Tominaga T (2008) Efficacy of superficial temporal artery-middle cerebral artery anastomosis with routine postoperative cerebral blood flow measurement during the acute stage in childhood moyamoya disease. Childs Nerv Syst 24:827– 832 Neurosurg Rev (2009) 32:245–249 4. Furuya K, Kawahara N, Morita A, Momose T, Aoki S, Kirino T (2004) Focal hyperperfusion after superficial temporal arterymiddle cerebral artery anastomosis in a patient with moyamoya disease. Case report. J Neurosurg 100:128–132 5. Houkin K, Ishikawa T, Yoshimoto T, Abe H (1997) Direct and indirect revascularization for moyamoya disease: surgical techniques and peri-operative complications. Clin Neurol Neurosurg 99 (Suppl 2):S142–S145 6. Kawaguchi T, Fujita S, Hosoda K, Shose Y, Hamano S, Iwakura M, Tamaki N (1996) Multiple burr-hole operation for adult moyamoya disease. J Neurosurg 84:468–476 7. Kuriyama S, Kusaka Y, Fujimura M, Wakai K, Tamakoshi A, Hashimoto S, Tsuji I, Inaba Y, Yoshimoto T (2008) Prevalence and clinicopathological features of moyamoya disease. Findings from nationwide epidemiological survey. Stroke 39:42–47 8. Matsushima T Inoue T, Suzuki SO, Fujii K, Fukui M, Hasuo K (1992) Surgical treatment of moyamoya disease in pediatric patients—comparison between the results of indirect and direct revascularization procedures. Neurosurgery 31:401–405 9. Nakagawa A, Fujimura M, Ohki T, Suzuki H, Takayama K, Tominaga T (2006) Intraoperative brain surface blood flow monitoring using IRIS V thermographicimaging system in patients with Moyamoya disease. No Shinkei Geka 34:1017–1025, (Jpn.) 10. Ohue S, Kumon Y, Kohno K, Watanabe H, Iwata S, Ohnishi T (2008) Postoperative temporary neurological deficits in adults with moyamoya disease. Surg Neurol 69:281–286 11. Suzuki J, Takaku A (1969) Cerebrovascular ‘moyamoya’ disease. Disease showing abnormal net-like vessels in base of brain. Arch Neurol 20:288–299 12. Takemura S, Sato S, Kuroki A, Sato S, Kayama T (1999) New ideas for indirect revascularization surgery for moyamoya disease. No to Shinkei 27:987–992 13. Touho H (2007) Cerebral ischemia due to compression of the brain by and hypertrophied muscle used for encephalomyosynangiosis in childhood moyamoya disease. Surg Neurol [Epub ahead of print] Comments Carlo Schaller, Geneva, Switzerland The authors report an unusual complication following otherwise uncomplicated left-sided STA-MCA bypass surgery with additional encephalo-myo-synangiosis (EMS) by subdural placement of the temporal muscle in a 26-year old patient who suffered from moyamoya disease: Two days after surgery and after initially documented improvement of CBF thanks to the functioning bypass, she developed aphasia. This was obviously due to considerable swelling of the temporal muscle which was compressed at the inferior 249 level of the bon flap. Thus, they took the patient to the OR again and drilled off the inferior edge and some part of the inner table of the bone flap. This has lead to clinical improvement of the patient’s condition that was then discharged without neurological deficits. In the discussion the authors highlight the differential diagnosis for postoperative deterioration in moyamoya patients, which should include not only the well-known complication of postoperative hyperperfusion but swelling of the temporal muscle as well if EMS has been performed. Having a lower incidence in Europe than in Japan, moyamoya disease is being seen at centers with dedicated teams for neurovascular treatment mainly. There is a regain of interest, however, in the performance of EC-IC bypasses, with more and more unruptured complex aneurysms detected, which are not all amenable to endovascular therapy and with more elaborate tests for the precise diagnostics of cerebrovascular insufficiency now available, which does also contribute to the increasing numbers of EC-IC bypasses performed recently. Although local compression of the bypass with consecutive muscular swelling is more likely to occur with EMS, it may as well occur due to venous stasis or subgaleal rebleeding in ECIC bypass surgery alone without additional EMS. Thus, I see the very practical aspect of this case description and on how the authors have successfully managed this unusual postoperative complication. This includes the knowledge of two important differential diagnoses for clinical deterioration following primarily successful bypass surgery with or without additional EMS: hyperperfusion or ischemia. They have successfully ruled out hyperperfusion by IMP-SPECT, which showed ischemia, whereas MRA revealed the patent STA-MCA bypass. We perform postoperative perfusion MRI and Duplex sonography in our bypass patients regularly, and I think the analogous problem might not have gone unnoticed as well. I think this report is a nice technical contribution and of interest for those of us who deal with neurovascular diseases. Masao Sugita, Hiroyuki Kinouchi, Yamanashi, Japan The authors provide a thoughtful analysis of a case with moyamoya disease suffered from rare postoperative complication. This study contains two kinds of essential information. First, they indicated the importance to evaluate the cerebral blood flow alteration in the acute stage following revascularization procedure especially when the symptoms appeared in order to differentiate ischemia from hyperperfusion since their clinical presentation is similar. Second, they successfully demonstrated that cerebral ischemia by muscle compression could be responsible for postoperative neurologic deterioration, which could be relieved by decompressive encephalo-myo-synangiosis (EMS) revision. The ischemic complications after direct and indirect anastomosis in this disease are commonly by technical failure; however, the mass effect of the swollen vascular supply materials, especially muscle for EMS, could be a cause for cerebral ischemia. Therefore, we should keep in mind of this rare complication.