Moyamoya disease classification

Moyamoya disease classification

The ischemic and hemorrhagic subtypes are difficult to diagnose prior to disease onset.

The intralateral and perilateral ventricular arteries on the original axial Time of flight magnetic resonance angiography images might suggest the hemorrhagic type of moyamoya disease prior to onset 1).

Unilateral and bilateral moyamoya disease (MMD).

Quasi Moyamoya disease

Asymptomatic Moyamoya Disease

Ischemic-type Moyamoya Disease

Suzuki and Kodoma classified the severity of moyamoya disease by progression of an occlusive process and the eventual appearance of collaterals based on serial cerebral angiographic evaluations and staged them, known as ‘Suzuki stages of Moyamoya disease’ which are mentioned under staging.

see Suzuki staging.


Traditional moyamoya disease (MMD) classification relies on morphological digital subtraction angiography (DSA) assessment, which do not reflect hemodynamic status, clinical symptoms, or surgical treatment outcome.

The Berlin MMD grading system is able to stratify preoperative hemispheric symptomatology. Furthermore, it correlated with postoperative new ischemic changes on MRI, and showed a strong trend in predicting clinical postoperative stroke. 2)


Ladner et al performed digital subtraction angiography and noninvasive structural and hemodynamic MRI, and they outline a new classification system for patients with moyamoya that they have named Prior Infarcts, Reactivity, and Angiography in Moyamoya Disease (PIRAMD).

Healthy control volunteers (n = 11; age 46 ± 12 years [mean ± SD]) and patients (n = 25; 42 ± 13.5 years) with angiographically confirmed moyamoya provided informed consent and underwent structural (T1-weighted, T2-weighted, FLAIR, MR angiography) and hemodynamic (T2*- and cerebral blood flow-weighted) 3-T MRI. Cerebrovascular reactivity (CVR) in the internal carotid artery territory was assessed using susceptibility-weighted MRI during a hypercapnic stimulus. Only hemispheres without prior revascularization were assessed. Each hemisphere was considered symptomatic if localizing signs were present on neurological examination and/or there was a history of transient ischemic attack with symptoms referable to that hemisphere. The PIRAMD factor weighting versus symptomatology was optimized using binary logistic regression and receiver operating characteristic curve analysis with bootstrapping. The PIRAMD finding was scored from 0 to 10. For each hemisphere, 1 point was assigned for prior infarct, 3 points for reduced CVR, 3 points for a modified Suzuki Score ≥ Grade II, and 3 points for flow impairment in ≥ 2 of 7 predefined vascular territories. Hemispheres were divided into 3 severity grades based on total PIRAMD score, as follows: Grade 1, 0-5 points; Grade 2, 6-9 points; and Grade 3, 10 points.

In 28 of 46 (60.9%) hemispheres the findings met clinical symptomatic criteria. With decreased CVR, the odds ratio of having a symptomatic hemisphere was 13 (95% CI 1.1-22.6, p = 0.002). The area under the curve for individual PIRAMD factors was 0.67-0.72, and for the PIRAMD grade it was 0.845. There were 0/8 (0%), 10/18 (55.6%), and 18/20 (90%) symptomatic PIRAMD Grade 1, 2, and 3 hemispheres, respectively.

A scoring system for total impairment is proposed that uses noninvasive MRI parameters. This scoring system correlates with symptomatology and may provide a measure of hemodynamic severity in moyamoya, which could be used for guiding management decisions and evaluating intervention response 3).


In 2014 Hung et al. proposed a quantitative method using color-coded parametric quantitative DSA (QDSA) to improve prediction of the severity of MMD. The Td significantly correlated with conventional angiographic grading and with the status of hemodynamic impairment in patients with MMD. QDSA and Td measurements can provide a simple and quantitative angiographic grading system for patients with MMD. 4).


1)

Ishikawa M, Terao S, Kagami H, Inaba M, Naritaka H. Intralateral and Perilateral Ventricular Arteries on Original Axial Magnetic Resonance Angiography in Adult Moyamoya Disease. Eur Neurol. 2021 Mar 29:1-5. doi: 10.1159/000514429. Epub ahead of print. PMID: 33780954.
2)

Teo M, Furtado S, Kaneko OF, Azad TD, Madhugiri V, Do HM, Steinberg GK. Validation and Application for the Berlin Grading System of Moyamoya Disease in Adult Patients. Neurosurgery. 2020 Feb 1;86(2):203-212. doi: 10.1093/neuros/nyz025. PMID: 30864668.
3)

Ladner TR, Donahue MJ, Arteaga DF, Faraco CC, Roach BA, Davis LT, Jordan LC, Froehler MT, Strother MK. Prior Infarcts, Reactivity, and Angiography in Moyamoya Disease (PIRAMD): a scoring system for moyamoya severity based on multimodal hemodynamic imaging. J Neurosurg. 2016 Mar 11:1-9. [Epub ahead of print] PubMed PMID: 26967789.
4)

Hung SC, Liang ML, Lin CF, Lin CJ, Guo WY, Chang FC, Wong TT, Chang CY. New grading of moyamoya disease using color-coded parametric quantitative digital subtraction angiography. J Chin Med Assoc. 2014 Aug;77(8):437-42. doi: 10.1016/j.jcma.2014.05.007. Epub 2014 Jul 12. PMID: 25028291.

Moyamoya Disease Epidemiology outside of Asia

Moyamoya Disease Epidemiology outside of Asia

Studies from outside of Asia are rare. In Washington state and California, the incidence of MMD was reported to be 0.086/100,000 based on 298 patients. The incidence was the highest in Asians, followed by Blacks, Whites, and Hispanics. The incidence in Asian Americans was 4.6 times higher than that in Whites. Female preponderance was also noted 1).

African-Americans had an earlier disease onset with a median age of 18. However, a more recent study based on the Nationwide Inpatient Sample database reported that MMD appears to be distributed among the races according to their relative proportions in the USA population 2).

From 2005 to 2008, there were an estimated 7,473 (2,236 pediatric and 5,237 adult) patients admitted with a diagnosis of MMD in the USA. MMD patients were most frequently Caucasians. Overall, ischemic stroke was the most common reason for admission in both children and adults. Hemorrhagic stroke was more frequent in adults compared with children, and there was a bimodal age distribution with peaks in the first and fourth decades of life. Female-to-male ratio was 2.2. Thus, MMD in the USA does not seem to differ from East Asian MMD.


The incidence of Moyamoya disease (MMD) in Europe is not well known. In those affected, the risk of brain hemorrhage is considered low. A study of Birkeland et al. aimed to investigate the incidence and clinical presentation of MMD in the Danish population.

Eligible patients were identified in the Danish National Patient Register from 1994 to 2017. They collected clinical and radiological data from individual patient records from neurological, neurosurgical, and pediatric units across Denmark. The diagnosis was validated according to established criteria. They also extracted basic demographic data on the cohort from the Danish Civil Registration System.

A total of 52 patients fulfilled the diagnostic criteria for MMD. Most cases were native Danes and only 15% of cases had an East Asian background. The ratio of female to male patients was 1.8, and the incidence had two peaks: one in childhood and another in young middle age. Until 2007, MMD was only diagnosed sporadically. From 2008 onwards, the incidence rate was 0.07 per 100 000 person-years (95% confidence interval 0.05-0.09 per 100 000 person-years). The most common mode of presentation was ischemic stroke (33%), followed by hemorrhage (23%), headache (17%), and transient ischemic attack (14%).

MMD is rare in Denmark, but associated with a considerable risk of hemorrhage. Thus, MMD should be considered in the workup for ischemic as well as hemorrhagic stroke in children and middle-aged Caucasian3).

References

1)

Uchino K, Johnston SC, Becker KJ, Tirschwell DL. Moyamoya disease in Washington State and California. Neurology. 2005;65(6):956-958. doi:10.1212/01.wnl.0000176066.33797.82
2)

Kainth D, Chaudhry SA, Kainth H, Suri FK, Qureshi AI. Epidemiological and clinical features of moyamoya disease in the USA. Neuroepidemiology. 2013;40(4):282-287. doi:10.1159/000345957
3)

Birkeland P, Tharmabalan V, Lauritsen J, Ganesan V, Bjarkam CR, von Weitzel-Mudersbach P. Moyamoya disease in a european setting: A danish population-based study [published online ahead of print, 2020 Jul 15]. Eur J Neurol. 2020;10.1111/ene.14439. doi:10.1111/ene.14439

Moyamoya disease outcome

Moyamoya disease outcome

The disorder can lead to negative mood and stress, which, left unresolved, may increase adverse health outcomes. yang et al. conducted a cross-sectional survey to examine the stress and mood of adults with moyamoya disease. Participants were recruited at a university hospital in SeoulKorea. Data were collected through questionnaires and review of participants’ electronic medical records. A total of 109 adult patients participated. Significant correlations were found between perceived stress, anxiety, and depression. Adults with moyamoya disease experience anxiety, depression, and stress-related to the risk of cerebral hemorrhage or ischemia, similar to patients with other cerebrovascular diseases. If uncontrolled, negative mood and stress can cause adverse health outcomes. Health professionals caring for patients with moyamoya disease should carefully observe patients’ stress and mood and develop interventions tailored to stages of the disease to help patients manage stress and mood. The study results provide baseline information for understanding the level of and the factors associated with stress and mood 1).


Pediatric Moyamoya disease patients have greater patency and a greater ability to establish good leptomeningeal collateral circulation (LMC) status than adult patients, and poor LMC status has a strong correlation with severe clinical symptoms and poor postoperative outcomes. LMC status may be an important factor in the differences in clinical characteristics and prognosis between pediatric and adult MMD patients 2).


Recurrent stroke after surgical revascularization is still a big issue for moyamoya disease (MMD).

Female, left-sided surgery and edematous lesion were independent risk factors for postoperative TNEs; the left-sided surgery and edematous lesion were also independently associated with the severity of TNE. Although patients with postoperative TNEs had worse neurological status during the perioperative period, postoperative TNEs had no associations with worse mRS score at the time of discharge 3).


The outcome following surgery is very difficult to judge, and there is no standardised measurement to assess it. It is therefore important to know which approach for such patient is adequate.

Comparing to patients with acute idiopathic primary intraventricular hemorrhage (PIVH), patients with acute MMD-related PIVH have younger age, lower blood pressure, and better renal function. Moreover, patients with acute MMD-related PIVH have lower short-term mortality 4).


Sundaram et al., compared the long-term outcome of moyamoya patients treated conservatively to those who underwent RS.

A study population included all patients with moyamoya disease/syndrome from 2002 to 2012. The demographic, clinical characteristic and imaging details were reviewed. The outcome was obtained prospectively.

Of the 36 patients, 26 (72.2%) had MMD and 10 (27.8%) had moyamoya syndrome. The median age at onset of symptoms was 17.5 years (range, 10 months-55 years). Fifteen patients belonged to pediatric group and 21 were adults. All the pediatric patients had ischemic events at onset and 10 (47.6%) of the adults presented with hemorrhage. Twenty (55.6%) patients received conservative treatment and 16 (44.4%) underwent revascularization procedures. The median duration of follow-up was 28 months (range, 3-90 months). Three (18%) of the surgically treated patients had recurrent ischemic events on follow-up, but none of the conservatively treated patients had events. An excellent outcome (Modified Rankin Scale of ≤2) was seen in 12 (75%) surgically treated and 16 (94%) conservatively treated patients (p=0.17).

Compared to East Asians, our patients had a lower stroke recurrence rate and good functional outcome even with conservative treatment. Future studies should focus on clinical and imaging predictors of progression to select moyamoya patients for RS 5).

References

1)

Yang YS, Ryu GW, Yeom I, Shim KW, Choi M. Stress and Mood of Adults with Moyamoya Disease: A Cross-Sectional Study. Nurs Health Sci. 2020 Apr 26. doi: 10.1111/nhs.12729. [Epub ahead of print] PubMed PMID: 32336006.
2)

Liu ZW, Han C, Wang H, Zhang Q, Li SJ, Bao XY, Zhang ZS, Duan L. Clinical characteristics and leptomeningeal collateral status in pediatric and adult patients with ischemic moyamoya disease. CNS Neurosci Ther. 2020 Jan;26(1):14-20. doi: 10.1111/cns.13130. Epub 2019 Apr 13. PubMed PMID: 31875482.
3)

Lu J, Zhao Y, Ma L, Chen Y, Li M, Chen X, Ye X, Wang R, Zhao Y. Predictors and clinical features of transient neurological events after combined bypass revascularization for moyamoya disease. Clin Neurol Neurosurg. 2019 Aug 29;186:105505. doi: 10.1016/j.clineuro.2019.105505. [Epub ahead of print] PubMed PMID: 31622898.
4)

Yu Z, Guo R, Zheng J, Li M, Wen D, Li H, You C, Ma L. Comparison of acute moyamoya disease-related and idiopathic primary intraventricular hemorrhage in adult patients. World Neurosurg. 2019 Jan 24. pii: S1878-8750(19)30167-6. doi: 10.1016/j.wneu.2019.01.070. [Epub ahead of print] PubMed PMID: 30685378.
5)

Sundaram S, Sylaja PN, Menon G, Sudhir J, Jayadevan ER, Sukumaran S, Sreedharan SE, Sarma S. Moyamoya disease: a comparison of long term outcome of conservative and surgical treatment in India. J Neurol Sci. 2014 Jan 15;336(1-2):99-102. doi: 10.1016/j.jns.2013.10.014. Epub 2013 Oct 16. PubMed PMID: 24183032.
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