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Open Access

Different aspects of cognitive function in adult patients with moyamoya disease and its clinical subtypes

Zhiyong Shi, Yu-Jie Wen, Zheng Huang, Le-Bao Yu, Dong Zhang
DOI: 10.1136/svn-2019-000309 Published 30 March 2020
Zhiyong Shi
1 Department of Neurosurgery, Beijing Tiantan Hospital, Capital Medical University, Beijing, China
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Yu-Jie Wen
2 The National Clinical Research Center for Mental Disorders & Beijing Key Laboratory of Mental Disorders & Beijing Institute for Brain Disorders Center of Schizophrenia, Beijing Anding Hospital, Capital Medical University, Beijing, 100088, China
3 Advanced Innovation Center for Human Brain Protection, Capital Medical University, Beijing, 100069, China
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Zheng Huang
4 Department of Neurosurgery, Xiangya Hospital, Xiangya Hospital Central South University, Changsha, China
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Le-Bao Yu
1 Department of Neurosurgery, Beijing Tiantan Hospital, Capital Medical University, Beijing, China
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Dong Zhang
1 Department of Neurosurgery, Beijing Tiantan Hospital, Capital Medical University, Beijing, China
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  • Figure 1
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    Figure 1

    Simplified research procedure in our study. ADC, apparent diffusion coefficient; ASL, arterial spin labelling; BRAVO, brain volume; DSA, digital subtraction angiography; DTI, diffusion tensor imaging; DWI, diffusion-weighted imaging; FLAIR, fluid-attenuated inversion recovery; fMRI, functional MRI; t-ASL, territorial arterial spin labelling.

  • Figure 2
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    Figure 2

    Comparison of cognitive function between MMD and healthy controls. Compared with the healthy controls matched by gender, age and education time, the adult MMD had a wide range of cognitive impairment, including IQ, PM (both TBPM and EBPM), VF, AT, time dimension of Stroop, CPT and TMT-A. Details may be found in online supplementary material table 4. *, p<0.05; #, p<0.01. AT, attention; BD, block design; C-CAMPROMPT, Cambridge Prospective Memory Test; CC, category completed; CPT, Continuous Persistence Test; EBPM, event-based prospective memory; GK, general knowledge; HC, healthy control; IM, immediate memory; MMD, moyamoya disease; PE, perseverative error; PM, prospective memory; RBANS, Repeatable Battery for the Assessment of Neuropsychological Status; RM retrospective memory; SI, similarity; TBPM, time-based prospective memory; TMT-A, Trail-Making Test Part A; VB, visual breadth; VF, verbal fluency; VP, visual puzzle; WCST, Wisconsin Card Classification Test.

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    Figure 3

    Comparison of cognitive function between MMD and healthy controls matched with gender, age,regional distribution and education level by covariate analysis (IQ adjusted). After variable controlled (IQ adjusted), significant difference between two groups in EBPM, TBPM and attention dimension could still be found. However, RM had no significant difference between the two groups. The separation between PM and RM indicated that PM and RM were independent of each other. EBPM, event-based prospective memory; HC, healthy control; MMD, moyamoya disease; PM, prospective memory; RBANS, Repeatable Battery for the Assessment of Neuropsychological Status; RM, retrospective memory; TBPM, time-based prospective memory.

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    Figure 4

    Comparison of cognitive function between male and female adult patients with MMD and HCs. For adult patients with MMD, the cognitive functions of female patients were better compared with male ones, where significant differences in PM (TBPM and EBPM), IM, Stroop and WCST-CC could be found. However, no similar results could be found between male and female in HCs. Details could be found in online supplementary material tables 8 and 9. *, p<0.05; #, p<0.01. AT, attention; BD, block design; C-CAMPROMPT, Cambridge Prospective Memory Test; CC, category completed; CPT, Continuous PersistenceTest; EBPM, event-based prospective memory; GK, general knowledge; HC, healthy control; IM, immediate memory; MMD, moyamoya disease; PE, perseverative error; PM prospective memory; RM retrospective memory; SI, similarity; TBPM, time-based prospective memory; TMT-A, Trail-Making Test Part A; VB, visual breadth; VF, verbal fluency; VP, visual puzzle; WCST, Wisconsin Card Classification Test.

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    Figure 5

    Comparison of cognitive function between ischaemic and haemorrhagic adult patients with moyamoya disease. The ischaemic patients performed better than the haemorrhagic patients, where the differences in the dimensions of EBPM and RM could be observed. The other dimensions were not significant (p>0.05). Details could be found in online supplementary material table 5. *, p<0.05; #, p<0.01. AT, attention; BD, block design; BPM, event-based prospective memory; C-CAMPROMPT, Cambridge Prospective Memory Test; CC, category completed; CPT, Continuous PersistenceTest; GK, general knowledge; IM, immediate memory; PE, perseverative error; PM prospective memory; RBANS, Repeatable Battery for the Assessment of Neuropsychological Status; RM, retrospective memory; SI, similarity; TBPM, time-based prospective memory; TMT-A, Trail-Making Test Part A; VB, visual breadth; VF, verbal fluency; VP, visual puzzle; WCST, Wisconsin Card Classification Test.

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    Figure 6

    Comparison of cognitive function between ischaemic subtypes for adult patients with moyamoya disease. For ischaemic patients, the headache subtype performed better than the TIA subtype, which was better than infarction ones. However, no significant difference between three ischaemic subtypes could be found (p>0.05). Moreover, the cognitive function of the headache subtype performed worse than that of HCs, but there was no significant difference between these two groups (p>0.05). Details could be found in online supplementary material tables 6 and 7. *, p<0.05; #, p<0.01. AT, attention; BD, block design; C-CAMPROMPT, Cambridge Prospective Memory Test; CC, category completed; CPT, Continuous Persistence Test; EBPM, event-based prospective memory; GK, general knowledge; HC, healthy control; IM, immediate memory; PE, perseverative error; PM, prospective memory; RM retrospective memory; SI, similarity; TBPM, time-based prospective memory; TIA, transient ischaemic attack; TMTA, Trail-Making Test Part A; VB, visual breadth; VF, verbal fluency; VP, visual puzzle; WCST, Wisconsin Card Classification Test.

  • Figure 7
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    Figure 7

    Analysis of attention pattern for adult patients with MMD and HCs. The time of attention for adult patients with MMD was significantly higher than healthy controls, including valid, invalid and control patterns (A). For adult patients with MMD, the time of the valid pattern was higher than that of the invalid pattern, indicating that attention pattern had changed, though no significant difference could be found between the three subgroups (B). *, p<0.05; #, p<0.01. HC, healthy control; MMD, moyamoya disease.

Tables

  • Figures
  • Supplementary Materials
  • Table 1

    Characteristics of participants and clinical information on patients

    MMDHCχ2/tP value
    Gender0.6120.46
     Male249
     Female2514
    Age38.45±8.98937.57±9.144−0.3870.700
    Education time (year)13.35±2.88414.22±2.0881.4520.152
    Type of MMD
     Haemorrhagic12–
     Ischaemic37–
    TIA11
    Infarction21
    Headache5
    • Data are given as mean±SD.

    • HC, healthy control; MMD, moyamoya disease; TIA, transient ischaemic attack.

  • Table 2

    Comparison of cognitive function between MMD and HCs after IQ controlled (covariance analysis)

    HC (n=23)MMD (n=49)FP value
    PM
    TBPM12.30±2.7049.06±3.7618.339.005*
    EBPM14.22±2.11012.14±3.2084.353.041*
    Total scores26.52±3.86021.20±6.2328.424.005*
    RBANS domains
    IM87.43±11.31779.94±15.7150.4800.491
    VB79.26±13.08475.49±10.0170.4730.494
    VF94.04±8.93183.27±14.3194.431.039*
    AT108.70±8.97793.76±15.6259.883.002**
    RM90.04±10.22781.41±15.3811.1210.293
    SS459.48±34.927413.86±53.0276.023.017*
    TSIS88.57±8.72777.63±12.6675.916.018*
    WCST
    PE10.87±24.12512.10±24.6360.0220.881
    CC4.74±1.9124.10±2.1140.0130.910
    • Data are given as mean±SD.

    • iBoldfaced values: If P value is lower than 0.05, boldfaced was used to discriminate.

    • *P<0.05, **P<0.01.

    • AT, attention; CC, category completed; EBPM, event-based prospective memory; HC, healthy control; IM, immediate memory; MMD, moyamoya disease; PE, perseverative error; PM, prospective memory; RBANS, Repeatable Battery for the Assessment of Neuropsychological Status; RM, retrospective memory; SS, scale score; TBPM, time-based prospective memory; TSIS, total scale of index scores; VB, visual breadth; VF, verbal fluency; WCST, Wisconsin Card Classification Test.

  • Table 3

    Correlation between gender, age, education time, IQ, PM, RBANS domains and WCST for adult patients with MMD

    (A) Showed correlation between PM and gender, age, education time, IM, VB, VF, AT, RM, SS, PE and CC
    GenderAgeEducation timeIQIMVBVFATRMSSPECC
    TBPM0.334*−0.363*0.1040.312*0.444**0.1270.2580.440**0.421**0.477**−0.1160.460**
    EBTM0.314*−0.248−0.0010.2760.382**0.1640.1810.341*0.422**0.416**−0.0300.428**
    • SS, Scale score.

  • (B) Exhibited correlation between AT and gender, age, IQ, PM, RM, VB, VF, RM, SS, PE and CC
    GenderAgeIQTBPMEBPMRMVBVFRMSSPECC
    AT0.264−0.295*0.539**0.440**0.341*0.492**0.354*0.414**0.458**0.752**−0.1160.38**
    • *P<0.05, **P<0.01.

    • AT, attention; CC, category completed; EBPM, event-based prospective memory; IM, immediate memory; MMD, moyamoya disease; PE, perseverative error; PM, prospective memory; RBANS, Repeatable Battery for the Assessment of Neuropsychological Status; RM, retrospective memory; TBPM, time-based prospective memory; VB, visual breadth; VF, verbal fluency; WCST, Wisconsin Card Classification Test.

Supplementary Materials

  • Figures
  • Tables
  • Supplementary data

    [svn-2019-000309supp001.pdf]

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Different aspects of cognitive function in adult patients with moyamoya disease and its clinical subtypes
Zhiyong Shi, Yu-Jie Wen, Zheng Huang, Le-Bao Yu, Dong Zhang
Stroke and Vascular Neurology Mar 2020, 5 (1) 86-96; DOI: 10.1136/svn-2019-000309

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Different aspects of cognitive function in adult patients with moyamoya disease and its clinical subtypes
Zhiyong Shi, Yu-Jie Wen, Zheng Huang, Le-Bao Yu, Dong Zhang
Stroke and Vascular Neurology Mar 2020, 5 (1) 86-96; DOI: 10.1136/svn-2019-000309
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Different aspects of cognitive function in adult patients with moyamoya disease and its clinical subtypes
Zhiyong Shi, Yu-Jie Wen, Zheng Huang, Le-Bao Yu, Dong Zhang
Stroke and Vascular Neurology Mar 2020, 5 (1) 86-96; DOI: 10.1136/svn-2019-000309
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