Patterns of collateral distribution in adult moyamoya disease

Objective To study the patterns of collateral circulation in adults moyamoya disease(MMD). Methods One hundred and nineteen consecutive adult patients with MMD (ischemic or hemorrhagic type) were identified by digital cerebral angiography in Nanjing Stroke Registry Program of Jinling Hospital between August 2004 and January 2010. The extracranial and (or) intracranial collateral circulations ipsilateral to stroke hemisphere were regarded as the research objects, and furthermore, these collateral circulations were divided into three different grades: Grade 1 collateral (anterior cerebral artery （ACA） → meningeal arteries （MLA） → middle cerebral artery （MCA）), Grade 2 collateral (dilating and extensing anterior choroidal artery beyond choroid fissure, patent posterior communicating artery → posterior cerebral artery→MLA→ ACA and(or) MCA, posterior cerebral artery→MLA→ACA and (or) MCA and posterior choroidal artery → posterior pericallosal arteries →ACA) and Grade 3 collateral (collateral originating from the external carotid artery supplying to cerebral blood flow). The relationship between collateral distribution patterns in adult MMD and Suzuki’s classification was analyzed. Results In 117 assessed vessel units of the collateral circulation ipsilateral to stroke hemisphere, there were a total of 200 collateral circulations. The percentage of numbers in Grade 1, Grade 2 and Grade 3 collateral was 11.5% (23/200), 52.0% (104/200) and 36.5% (73/200), respectively. The distribution percentage of Grade 1 was gradually decreased from Suzuki’sⅠto Ⅵ, mainly distributed in the early stage of MMD (Suzuki’s Ⅰ—Ⅱ) and accounted for 91.3% (21/23; Z=-7.270, P<0.01). The distribution percentage of Grade 3 was gradually increased from Suzuki’sⅠto Ⅵ, especially in the late stage of MMD (Suzuki’s Ⅴ—Ⅵ) and accounted respectively for 37.0% (27/73) and 63.0% (46/73; Z=-7.270, P<0.01). Compared with the total distribution of Grade 1 and 3 collateral circulation, the distribution percentage of Grade 2 was 6.7% (7/104), 7.7% (8/104), 15.4% (16/104), 40.4% (42/104), 14.4% (15/104) and 15.4% (16/104) from Suzuki’s Ⅰto Ⅵ. Although there was not significant difference, Grade 2 mainly distributed in the medium stage of MMD (Suzuki’s Ⅲ—Ⅳ). Conclusions The patterns of collateral distribution is various, changing with the progression of MMD. Grade 2 collateral circulation accounts for a higher proportion, especially in the medium stage of the disease, which suggests that these collaterals play an important compensatory role of blood flow. Key words: Moyamoya disease; Cerebrovascular circulation; Collateral circulation;  Angiography;  digital subtraction