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Dynamic permeability and quantitative susceptibility: related imaging biomarkers in cerebral cavernous malformations.

ABSTRACT: Hyperpermeability and iron deposition are 2 central pathophysiological phenomena in human cerebral cavernous malformation (CCM) disease. Here, we used 2 novel MRI techniques to establish a relationship between these phenomena.Subjects with CCM disease (4 sporadic and 17 familial) underwent MRI imaging using the dynamic contrast-enhanced quantitative perfusion and quantitative susceptibility mapping techniques that measure hemodynamic factors of vessel leak and iron deposition, respectively, previously demonstrated in CCM disease. Regions of interest encompassing the CCM lesions were analyzed using these techniques.Susceptibility measured by quantitative susceptibility mapping was positively correlated with permeability of lesions measured using dynamic contrast-enhanced quantitative perfusion (r=0.49; P?0.0001). The correlation was not affected by factors, including lesion volume, contrast agent, and the use of statin medication. Susceptibility was correlated with lesional blood volume (r=0.4; P=0.0001) but not with lesional blood flow.The correlation between quantitative susceptibility mapping and dynamic contrast-enhanced quantitative perfusion suggests that the phenomena of permeability and iron deposition are related in CCM; hence, more leaky lesions also manifest a more cumulative iron burden. These techniques might be used as biomarkers to monitor the course of this disease and the effect of therapy.

SUBMITTER: Mikati AG

PROVIDER: S-EPMC4351041 | biostudies-literature | 2014 Feb

REPOSITORIES: biostudies-literature

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Dynamic permeability and quantitative susceptibility: related imaging biomarkers in cerebral cavernous malformations.

Mikati Abdul Ghani AG Tan Huan H Shenkar Robert R Li Luying L Zhang Lingjiao L Guo Xiaodong X Larsson Henrik B W HB Shi Changbin C Liu Tian T Wang Yi Y Shah Akash A Edelman Robert R RR Christoforidis Gregory G Awad Issam I

Stroke 20131203 2

<h4>Background and purpose</h4>Hyperpermeability and iron deposition are 2 central pathophysiological phenomena in human cerebral cavernous malformation (CCM) disease. Here, we used 2 novel MRI techniques to establish a relationship between these phenomena.<h4>Methods</h4>Subjects with CCM disease (4 sporadic and 17 familial) underwent MRI imaging using the dynamic contrast-enhanced quantitative perfusion and quantitative susceptibility mapping techniques that measure hemodynamic factors of vess ...[more]

PMID: 24302484

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Project description:OBJECTIVE Vascular permeability and iron leakage are central features of cerebral cavernous malformation (CCM) pathogenesis. The authors aimed to correlate prospective clinical behavior of CCM lesions with longitudinal changes in biomarkers of dynamic contrast-enhanced quantitative permeability (DCEQP) and quantitative susceptibility mapping (QSM) assessed by MRI. METHODS Forty-six patients with CCMs underwent 2 or more permeability and/or susceptibility studies in conjunction with baseline and follow-up imaging and clinical surveillance during a mean 12.05 months of follow-up (range 2.4-31.27 months). Based on clinical and imaging features, cases/lesions were classified as stable, unstable, or recovering. Associated and predictive changes in quantitative permeability and susceptibility were investigated. RESULTS Lesional mean permeability and QSM values were not significantly different in stable versus unstable lesions at baseline. Mean lesional permeability in unstable CCMs with lesional bleeding or growth increased significantly (+85.9% change; p = 0.005), while mean permeability in stable and recovering lesions did not significantly change. Mean lesional QSM values significantly increased in unstable lesions (+44.1% change; p = 0.01), decreased slightly with statistical significance in stable lesions (-3.2% change; p = 0.003), and did not significantly change in recovering lesions. Familial cases developing new lesions during the follow-up period showed a higher background brain permeability at baseline (p = 0.001), as well as higher regional permeability (p = 0.003) in the area that would later develop a new lesion as compared with the homologous contralateral brain region. CONCLUSIONS In vivo assessment of vascular permeability and iron deposition on MRI can serve as objective and quantifiable biomarkers of disease activity in CCMs. This may be applied in natural history studies and may help calibrate clinical trials. The 2 techniques are likely applicable in other disorders of vascular integrity and iron leakage such as aging, hemorrhagic microangiopathy, and traumatic brain injury.

Project description:Rationale: Cerebral cavernous malformation (CCM) is prone to recurring microhemorrhage, which can lead to drug-resistant epilepsy. Surgical resection is the first choice to control seizures for CCM-associated epilepsy. At present, removal of resection-related tissue only depends on cautious visual identification of CCM lesions and perilesional yellowish hemosiderin rim by the neurosurgeon. Inspired by the resection requirements, we proposed quantitative multiphoton microscopy (qMPM) for a histopathology-level diagnostic paradigm to assist clinicians in precisely complete resection. Methods: A total of 35 sections specimens collected from 12 patients with the CCM-related epilepsy were included in this study. First, qMPM utilized a label-free multi-channel selective detection to image the histopathological features based on the spectral characteristics of CCM tissues. Then, qMPM developed three customized algorithms to provide quantitative information, a vascular patterns classifier based on linear support vector machine, visualization of microhemorrhage regions based on hemosiderin-related parameters, and the CCM-oriented virtual staining generative adversarial network (CCM-stainGAN) was constructed to generate two types of virtual staining. Results: Focused on CCM lesion and perilesional regions, qMPM imaged malformed vascular patterns and micron-scale hemosiderin-related products. Four vascular patterns were automatically identified by the classifier with an area under the receiver operating characteristic curve of 0.97. Moreover, qMPM mapped different degrees of hemorrhage regions onto fresh tissue while providing three quantitative hemosiderin-related indicators. Besides, qMPM realized virtual staining by the CCM-stainGAN with 98.8% diagnostic accuracy of CCM histopathological features in blind analysis. Finally, we provided pathologists and surgeons with the qMPM-based CCM histopathological diagnostic guidelines for a more definitive intraoperative or postoperative diagnosis. Conclusions: qMPM can provide decision-making supports for histopathological diagnosis, and resection guidance of CCM from the perspectives of high-resolution precision detection and automated quantitative assessment. Our work will promote the development of MPM diagnostic instruments and enable more optical diagnostic applications for epilepsy.

Dataset Information

Dynamic permeability and quantitative susceptibility: related imaging biomarkers in cerebral cavernous malformations.

Publications

Dynamic permeability and quantitative susceptibility: related imaging biomarkers in cerebral cavernous malformations.

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