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Individualised evaluation based on pathophysiology for moyamoya vasculopathy: application in surgical revascularisation

Xin Zhang, Yu Lei, Jiabin Su, Chao Gao, Yanjiang Li, Rui Feng, Ding Xia, Peng Gao, Yuxiang Gu, Ying Mao
DOI: 10.1136/svn-2023-002464 Published 28 August 2023
Xin Zhang
1Department of Neurosurgery, Huashan Hospital Fudan University, Shanghai, China
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Yu Lei
1Department of Neurosurgery, Huashan Hospital Fudan University, Shanghai, China
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Jiabin Su
1Department of Neurosurgery, Huashan Hospital Fudan University, Shanghai, China
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Chao Gao
1Department of Neurosurgery, Huashan Hospital Fudan University, Shanghai, China
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Yanjiang Li
1Department of Neurosurgery, Huashan Hospital Fudan University, Shanghai, China
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Rui Feng
1Department of Neurosurgery, Huashan Hospital Fudan University, Shanghai, China
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Ding Xia
2Department of Radiology, Huashan Hospital Fudan University, Shanghai, China
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Peng Gao
2Department of Radiology, Huashan Hospital Fudan University, Shanghai, China
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Yuxiang Gu
1Department of Neurosurgery, Huashan Hospital Fudan University, Shanghai, China
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Ying Mao
1Department of Neurosurgery, Huashan Hospital Fudan University, Shanghai, China
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  • Figure 1
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    Figure 1

    (A) Data processing flow chart for preoperative evaluation. (B) Data processing flow chart for intraoperative evaluation. Structural neuroImages including three-dimensional MRIs and digital subtraction angiography images are used to construct brain models and stereoscopic cerebral vessels. Arterial spin labelling (ASL) and positron emission tomography (PET) images are pseudocoloured to enhance the visualisation. Volumetric and angiographic images are fused to reflect old infarction areas and the distribution of the cortical arteries. Perfusion and metabolic images are overlayed using the preoperative navigation system, and the fused results are observed from multiple angles. with this basis, the hemispheric perfusion and metabolism statuses of different brain regions are compared with localise the surgical field and exclude invalid regions. In addition, alternative recipient arteries are determined. Both skin flap and bone windows are designed accordingly. Surgical field is further evaluated using indocyanine green (ICG) and electrocorticography (ECoG) monitoring. Multimodal neuroimaging was projected and overlaid with real-time surgical field under microscope and integrated navigation system using the augmented reality (AR) technique. The target recipient artery was identified with worse haemodynamic status using ICG-FLOW 800 and lower PSD in the high-frequency bands using ECoG. After bypass surgery, both haemodynamic and electrophysiological parameters are compared with those at baseline to determine the appropriate postoperative management strategy. ROIs, regions of interest.

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    Figure 2

    (A) Flow chart and inclusion criteria of the study. (B) Standard operating procedure of the tailored evaluating system the standard operating procedure of the tailored evaluating system for MMV is divided into three parts: preoperative, intraoperative and postoperative. Preoperatively (green box), pathophysiology-based neuroimaging is fused so that the individualised surgical field and alternative recipient arteries are determined and invalid regions are excluded. Intraoperatively (yellow box), multimodal neuroimaging data are projected onto the surgical field and regional haemodynamic parameters as well as cortical neuron activities are assessed to verify the target recipient artery. Postoperatively (blue box), the changes in haemodynamic parameters and power spectral density are analysed to determine the appropriate postoperative management. 3D-MRI, three-dimensional magnetic resonance imaging; ASL, arterial spin labelling; DSA, digital subtraction angiography; ECoG, electrocorticography; EDMS, encephalo-dural-myo-synangiosis; ICG, indocyanine green; MMV, moyamoya vasculopathy; PET, positron emission tomography; STA-MCA, superficial temporal artery to middle cerebral artery.

  • Figure 3
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    Figure 3

    (A) Perfusion/metabolism mismatch phenomenon. (B) Correlation with complication rate typical perfusion and metabolism status around anastomosis area: –/–, hypoperfusion and hypometabolism without obvious infarction; –/+, hypoperfusion and hypermetabolism with lacunar infarction; +/–, hyperperfusion and hypometabolism without obvious infarction; +/+, hyperperfusion and hypermetabolism without obvious infarction. hyper- is represented by ‘+’ while hypo- is represented by ‘–’ and the status of perfusion and metabolism is represented by */*. The total number of patients shows a downward trend with the change of perfusion and metabolism status, while the complication rate shows an upward trend. Patients with hypoperfusion and hyperpmetabolism had the lowest complication rate with statistical differences compared with other groups.

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    Figure 4

    Illustrative case of the novel evaluating system. For preoperative part, DSA demonstrated severe stenosis of bilateral middle cerebral artery with the formation of moyamoya vessels (A, B). ASL with two postlabelling delays showed hypoperfusion in the left temporal and parietal lobes (C, D). 18F-FDG PET also confirmed hypometabolism changes in the same area (E). Individualised bone window was designed to protect the blood supply from middle meningeal artery and alternative recipient arteries were identified (F). The perfusion status in relative area could be compared accordingly (G, H). For preoperative part, all the bypass-related information could be visible and verified for the determination of the recipient artery (blue box). ICG-FLOW 800 was performed and colour mapping was available. Haemodynamic curves and parameters could be calculated and electrophysiological parameters of recipient arteries-located regions were compared (red box). Number 1 of the recipients was selected as target artery. For postoperative part, the comparison of the parameters from ICG-FLOW 800 and ECoG could help to confirm the ameliorating effects and distinguish potential risk factors. ASL, arterial spin labelling; DSA, digital subtraction angiography; ECoG, electrocorticography; ICG-FLOW, indocyanine green; PET, positron emission tomography.

Tables

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  • Table 1

    Patient demographics and postoperative complications

    ParametersGroupP value
    Novel groupTraditional group
    No of patients145230
    Age (x±s,years)44.23±10.4544.59±10.750.835
    Male (n (%))69 (47.59%)110 (47.83%)0.964
    Surgical side (right, n (%))67 (46.21%)108 (46.96%)0.887
    Clinical presentation (n (%))0.511
     Ischaemic type84 (57.93%)134 (58.26%)
     Haemorrhagic type43 (29.66%)59 (25.65%)
     Asymptomatic type18 (12.41%)37 (16.09%)
    Risk factors (n (%))   
     Hypertension62 (42.76%)105 (45.65%)0.583
     Diabetes mellitus38 (26.21%)54 (23.49%)0.550
     Hyperlipidaemia32 (22.07%)55 (23.91%)0.680
     Smoking47 (32.41%)66 (28.70%)0.445
    Suzuki stage (n (%))0.985
     I0 (0%)0 (0%)
     II10 (6.90%)18 (7.83%)
     III65 (44.83%)104 (45.22%)
     IV39 (26.89%)61 (26.52%)
     V31 (21.38%)47 (20.43%)
     VI0 (0%)0 (0%)
    Postoperative complications (n (%))<0.001
     Cerebral infarction2 (1.38%)15 (6.52%)0.009
     Intracranial haemorrhage1 (0.69%)5 (2.17%)0.180
     Hyperperfusion syndrome23 (15.86%)59 (24.35%)0.010
    Neurological outcome (modified Rankin Scale)  0.260
     0113 (77.93%)149 (64.78%) 
     121 (14.48%)42 (18.26%) 
     27 (4.83%)21 (9.13%) 
     32 (1.38%)10 (4.35%) 
     41 (0.69%)6 (2.61%) 
     5–61 (0.69%)2 (0.87%) 
  • Table 2

    Mismatch phenomenon and correlation with complications

    Perfusion/metabolic level
    Nearby anastomosis area
    TotalComplicationP value
    –/–101 (69.66%)8 (7.92%)<0.0001
    –/+22 (15.17%)7 (31.82%)
    +/–15 (10.34%)7 (46.67%)
    +/+7 (4.83%)4 (57.14%)
    • The level of hyper- was presented as ‘+’ and hypo- was presented as ‘–’.

Supplementary Materials

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    [svn-2023-002464supp001.pdf]

Additional Files

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    This web only file has been produced by the BMJ Publishing Group from an electronic file supplied by the author(s) and has not been edited for content.

    • Data supplement 1
  • Supplementary Data

    This web only file has been produced by the BMJ Publishing Group from an electronic file supplied by the author(s) and has not been edited for content.

    • Data supplement 1
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Individualised evaluation based on pathophysiology for moyamoya vasculopathy: application in surgical revascularisation
Xin Zhang, Yu Lei, Jiabin Su, Chao Gao, Yanjiang Li, Rui Feng, Ding Xia, Peng Gao, Yuxiang Gu, Ying Mao
Stroke and Vascular Neurology Aug 2023, svn-2023-002464; DOI: 10.1136/svn-2023-002464

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Individualised evaluation based on pathophysiology for moyamoya vasculopathy: application in surgical revascularisation
Xin Zhang, Yu Lei, Jiabin Su, Chao Gao, Yanjiang Li, Rui Feng, Ding Xia, Peng Gao, Yuxiang Gu, Ying Mao
Stroke and Vascular Neurology Aug 2023, svn-2023-002464; DOI: 10.1136/svn-2023-002464
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Individualised evaluation based on pathophysiology for moyamoya vasculopathy: application in surgical revascularisation
Xin Zhang, Yu Lei, Jiabin Su, Chao Gao, Yanjiang Li, Rui Feng, Ding Xia, Peng Gao, Yuxiang Gu, Ying Mao
Stroke and Vascular Neurology Aug 2023, svn-2023-002464; DOI: 10.1136/svn-2023-002464
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