Satoshi Kuroda
Abstract
General principles of indirect bypass surgery are very unique and specific for moyamoya disease. Previous studies have suggested that the elevated levels of angiogenic factors in the cerebrospinal fluid (CSF) may play an important role in aggressive neovascularization between the brain surface and vascularized donor tissues in moyamoya disease. Previously reported donor tissues include the dura mater, temporal muscle, galea aponeurotica, pericranium, and omentum. Surgical procedures are not difficult for well- trained neurosurgeons. However, the neurosurgeons should be aware of several important issues about indirect revascularization for moyamoya disease. First, indirect revascularization functions as effective collaterals in a majority of pediatric patients, but in only 50 to 70% of adult patients. Therefore, direct revascularization such as superficial temporal artery to middle cerebral artery (STA-MCA) anastomosis should simultaneously be indicated, especially in adult patients. Second, indirect revascularization requires 3 to 4 months to complete the development of effective collaterals, and thus carries the risk for ischemic stroke during and just after surgery, especially in patients with dense cerebral ischemia. Third, the extent of craniotomy and dural opening largely determines the extent of surgical collaterals development, which means that surgical design should be determined according to the extent of cerebral ischemia on blood flow measurements in each patient.
Keywords: moyamoya disease, indirect bypass, angiogenic factors, cerebrospinal fluid, craniotomy
General principles of indirect bypass surgery are very unique and specific for moyamoya disease. This surgical procedure only requires the attachment of the vascularized donor tissue onto the surface of brain. Gradual, but steady neovascularization occurs between these tissues in moyamoya disease. Nowadays, indirect bypass procedure is indicated almost only for moyamoya disease, although there are a small number of reports demonstrating that indirect bypass is also effective for other disorders, including atherosclerotic cerebrovascular diseases and spinal cord injury. In this chapter, the author describes history, pathophysiology, and concept of surgery of indirect bypass for moyamoya disease.
Fig. 3.1 demonstrates the history of main surgical procedures for indirect bypass. For these 40 years, various methods for indirect bypass have been reported for patients with moyamoya disease, including encephalo-duro-arteriosynangiosis (EDAS),1 encephalo-myo-synangiosis (EMS),2 encephalo-myo-arterio-synangiosis (EMAS),3 encephaloduro-arterio-myo-synangiosis (EDAMS),4 encephalo-galeo- synangiosis (EGS),5 and dural inversion.6 These procedures have been developed to provide collateral blood flow mainly to the territory of the middle cerebral artery (MCA) and useful to reduce or resolve ischemic attacks. However, it is well known that a certain subgroup of patients with moyamoya disease does not respond to these surgery and experiences ischemic attacks of the bilateral legs and/or cognitive dysfunction probably due to persistent ischemia in the territory of the anterior cerebral artery (ACA). Several procedures targeting the ACA territory have been reported later. Thus, Kinugasa et al inserted the pedicle of the galea on both sides into the interhemispheric fissure in addition to EDAMS (ribbon EDAMS). Kawaguchi et al developed multiple burr hole surgery to induce neovascularization through indirect bypass, using one to four burr holes.7 Yoshida et al inserted the dural pedicles into the epiarachnoid space to enlarge the revascularized area around craniotomy. For the same purpose, Kim et al also developed EDAS with bifrontal encephalogaleo(periosteal) synangiosis.8 Subsequently, Kamiyama and colleagues developed STA-MCA/ACA anastomosis and pan-synangiosis, which consists of EDMAS and EGS for the MCA and ACA territories through two different craniotomies, respectively.9 Kuroda et al further advanced indirect bypass procedure that can provide collateral blood flow to the whole territory of the internal carotid artery (ICA). For this purpose, a large frontal pericranial flap was employed to widely cover the frontal lobe through one craniotomy.10,11
Alternatively, the omentum has been employed as a donor tissue for indirect bypass and shown an aggressive neovascularization into the brain, but there are no reports on omental transplantation for these 20 years probably because of its invasiveness.12-16
As aforementioned, indirect bypass surgery induces spontaneous and aggressive neovascularization between the vascularized donor tissues and brain surface, which is almost specific for moyamoya disease. According to previous observations, the elevated levels of angiogenic factors in the cerebrospinal fluid (CSF) may play an important role in neovascularization between them. These angiogenic factors include basic fibroblast growth factor (bFGF) and hepatocyte growth factor (HGF). The concentrations of bFGF in the CSF significantly elevates in the CSF of patients with moyamoya disease, when compared with the controls.17
Interestingly, the concentration of bFGF is reported significantly higher in patients with good development of surgical collaterals via indirect bypass than in those without, strongly suggesting that bFGF are playing an important role in neovascularization after indirect bypass.18,19 However, the concentration of bFGF does not correlate with patients’ age, gender, and Suzuki’s angiographical stage. The elevation of bFGF concentration in the CSF may not be specific for moyamoya disease because it is confirmed in patients with Chiari malformation, arteriovenous malformation (AVM), brain tumor, and hydrocephalus.19 Pediatric patients with moyamoya syndrome also exhibit significantly elevated CSF levels of vascular cell adhesion molecule type 1 (VCAM-1), intercellular adhesion molecule type 1 (ICAM-1), E-selectin, and cellular retinoic acid-binding protein (CRABP)-1.20,21 However, the biological roles of these soluble factors are not known precisely. On the other hands, the concentration of HGF significantly elevates up to twofold of the controls in patients with moyamoya disease. Interestingly, HGF and its receptor, c-Met are highly expressed in the media and thickened intima of the involved carotid fork.22 Theses angiogenic factors may play a key role in not only disease onset but also the specific neovascularization after indirect bypass surgery.
Previously reported donor tissues include the dura mater, temporal muscle, galea aponeurotica, and pericranium. These tissues can easily be used as the vascularized donors for indirect bypass, because they are surrounding the cranium. Surgical procedures are not difficult for the well-trained neurosurgeons. Alternatively, the omentum has also been reported to supply efficient blood flow to the ischemic brain as a surgically anastomosed flap or long vascularized flap.
However, the neurosurgeons should be aware of several important issues about indirect revascularization for moyamoya disease. First, indirect revascularization functions as effective collaterals in a majority of pediatric patients, but in only 50 to 70% of adult patients.23,24 Therefore, direct revascularization such as STA-MCA anastomosis should simultaneously be indicated especially in adult patients. Second, indirect revascularization requires 3 to 4 months to complete the development of effective collaterals, and thus carries the risk for ischemic stroke during and just after surgery, especially in patients with dense cerebral ischemia.25 Therefore, proper anesthetic management is essential to prevent perioperative ischemic complications.26-28 Third, the extent of craniotomy and dural opening largely determines the extent of surgical collaterals development, which means that surgical design should be determined according to the extent of cerebral ischemia in each patient (Fig. 3.2).29-32
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