Advertisement
Original Research| Volume 110, P92-99, April 2023

Intraoperative shear-wave elastography and superb microvascular imaging contribute to the glioma grading

  • Siman Cai
    Affiliations
    Department of Diagnostic Ultrasound, Peking Union Medical College Hospital, Chinese Academy of Medical Science and Peking Union Medical College, Beijing 100730, China
    Search for articles by this author
  • Hao Xing
    Affiliations
    Department of Neurosurgery Department, Peking Union Medical College Hospital, Chinese Academy of Medical Science and Peking Union Medical College, Beijing 100730, China
    Search for articles by this author
  • Yuekun Wang
    Affiliations
    Department of Neurosurgery Department, Peking Union Medical College Hospital, Chinese Academy of Medical Science and Peking Union Medical College, Beijing 100730, China
    Search for articles by this author
  • Yu Wang
    Affiliations
    Department of Neurosurgery Department, Peking Union Medical College Hospital, Chinese Academy of Medical Science and Peking Union Medical College, Beijing 100730, China
    Search for articles by this author
  • Wenbin Ma
    Affiliations
    Department of Neurosurgery Department, Peking Union Medical College Hospital, Chinese Academy of Medical Science and Peking Union Medical College, Beijing 100730, China
    Search for articles by this author
  • Yuxin Jiang
    Affiliations
    Department of Diagnostic Ultrasound, Peking Union Medical College Hospital, Chinese Academy of Medical Science and Peking Union Medical College, Beijing 100730, China
    Search for articles by this author
  • Author Footnotes
    1 Jianchu Li and Hongyan Wang have contributed equally to this work.
    Jianchu Li
    Correspondence
    Corresponding authors.
    Footnotes
    1 Jianchu Li and Hongyan Wang have contributed equally to this work.
    Affiliations
    Department of Diagnostic Ultrasound, Peking Union Medical College Hospital, Chinese Academy of Medical Science and Peking Union Medical College, Beijing 100730, China
    Search for articles by this author
  • Author Footnotes
    1 Jianchu Li and Hongyan Wang have contributed equally to this work.
    Hongyan Wang
    Correspondence
    Corresponding authors.
    Footnotes
    1 Jianchu Li and Hongyan Wang have contributed equally to this work.
    Affiliations
    Department of Diagnostic Ultrasound, Peking Union Medical College Hospital, Chinese Academy of Medical Science and Peking Union Medical College, Beijing 100730, China
    Search for articles by this author
  • Author Footnotes
    1 Jianchu Li and Hongyan Wang have contributed equally to this work.

      Highlights

      • In the SWE mode, the diagnostic threshold of HGG and LGG is 13.05 kPa.
      • In the SMI mode, the vascular architectures of the tumor tissue and peritumoral tissues of HGG and LGG were significantly different (P < 0.05).
      • SWE and SMI are beneficial for the differentiation of HGG and LGG and may help optimize clinical surgical procedures.

      Abstract

      Background

      To explore the diagnostic value and feasibility of shear wave elastography and superb microvascular imaging in the grading diagnosis of glioma intraoperatively.

      Materials and methods

      Forty-nine patients with glioma were included in this study. B-mode ultrasonography, Young's modulus in shear-wave elastography (SWE) and vascular architecture in superb microvascular imaging(SMI) of tumor tissue and peritumoral tissue were analyzed. Receiver operating characteristic(ROC) curve analysis was used to evaluate the diagnostic effect of SWE. Logistic regression model was used to calculate the prediction probability of HGG diagnosis.

      Results

      Compared with LGG, HGG was often characterized by peritumoral edema in B mode (P < 0.05). There was a significant difference in Young's modulus between HGG and LGG; the diagnostic threshold of HGG and LGG was 13.05 kPa, the sensitivity was 78.3%, and the specificity was 76.9%. The vascular architectures of the tumor tissue and peritumoral tissues of HGG and LGG were significantly different (P < 0.05). The vascular architectures of peritumoral tissue in HGG often characterized by distorted blood flow signals surrounding the tumor (14/26,53.8%); in the tumor tissue, HGG often presents as dilated and bent vessels(19/26,73.1%). The elasticity value of SWE and the tumor vascular architectures of SMI were correlated with the diagnosis of HGG.

      Conclusion

      Intraoperative ultrasound (ioUS), especially SWE, and SMI are beneficial for the differentiation of HGG and LGG and may help optimize clinical surgical procedures.

      Keywords

      To read this article in full you will need to make a payment

      Purchase one-time access:

      Academic & Personal: 24 hour online accessCorporate R&D Professionals: 24 hour online access
      One-time access price info
      • For academic or personal research use, select 'Academic and Personal'
      • For corporate R&D use, select 'Corporate R&D Professionals'

      Subscribe:

      Subscribe to Journal of Clinical Neuroscience
      Already a print subscriber? Claim online access
      Already an online subscriber? Sign in
      Institutional Access: Sign in to ScienceDirect

      References

        • Louis D.N.
        • Perry A.
        • Reifenberger G.
        • et al.
        The 2016 World Health Organization Classification of Tumors of the Central Nervous System: a summary.
        Acta Neuropathol. 2016 Jun; 131: 803-820
        • Gupta M.
        • Djalilvand A.
        • Fau-Brat D.J.
        • Brat D.J.
        Clarifying the diffuse gliomas: an update on the morphologic features and markers that discriminate oligodendroglioma from astrocytoma.
        Am J Clin Pathol. 2005; 124: 755-768
        • Sharma A.
        • Graber J.J.
        Overview of prognostic factors in adult gliomas.
        Ann Palliat Med. 2021; 10: 863-874
        • Gandhi S.
        • Tayebi Meybodi A.
        • Belykh E.
        • et al.
        Survival Outcomes Among Patients With High-Grade Glioma Treated With 5-Aminolevulinic Acid-Guided Surgery: A Systematic Review and Meta-Analysis.
        Front Oncol. 2019 Jul; 17: 620
        • Gulati S.
        • Jakola A.S.
        • Nerland U.S.
        • Weber C.
        • Solheim O.
        The Risk of Getting Worse: Surgically Acquired Deficits, Perioperative Complications, and Functional Outcomes After Primary Resection of Glioblastoma.
        World Neurosurg. 2011; 76: 572-579
        • D’Amico R.S.
        • Englander Z.K.
        • Canoll P.
        • Bruce J.N.
        Extent of Resection in Glioma–A Review of the Cutting Edge.
        World Neurosurg. 2017; 103: 538-549
        • Ganau L.
        • Ligarotti G.K.I.
        • Ganau M.
        Predicting complexity of tumor removal and postoperative outcome in patients with high-grade gliomas.
        Neurosurg Rev. 2018; 41: 371-373
        • Brahimaj B.C.
        • Kochanski R.B.
        • Pearce J.J.
        • et al.
        Structural and Functional Imaging in Glioma Management.
        Neurosurgery. 2021; 88: 211-221
        • Yin L.
        • Cheng L.
        • Wang F.
        • Zhu X.
        • Hua Y.
        • He W.
        Application of intraoperative B-mode ultrasound and shear wave elastography for glioma grading.
        Quant Imaging Med Surg. 2021; 11: 2733-2743
        • Chand P.
        • Amit S.
        • Gupta R.
        • Agarwal A.
        Errors, limitations, and pitfalls in the diagnosis of central and peripheral nervous system lesions in intraoperative cytology and frozen sections.
        J Cytol. 2016; 33: 93-97
        • Lu H.
        • Pollack E.
        • Young R.
        • et al.
        Predicting grade of cerebral glioma using vascular-space occupancy MR imaging.
        AJNR Am J Neuroradiol. 2008; 29: 373-378
        • Law M.
        • Yang S.
        • Wang H.
        • et al.
        Glioma grading: sensitivity, specificity, and predictive values of perfusion MR imaging and proton MR spectroscopic imaging compared with conventional MR imaging.
        AJNR Am J Neuroradiol. 2003; 24: 1989-1998
        • Möller-Hartmann W.
        • Herminghaus S.
        • Krings T.
        • et al.
        Clinical application of proton magnetic resonance spectroscopy in the diagnosis of intracranial mass lesions.
        Neuroradiology. 2002; 44: 371-381
        • Wang Q.
        • Zhang H.
        • Zhang J.
        • et al.
        The diagnostic performance of magnetic resonance spectroscopy in differentiating high-from low-grade gliomas: A systematic review and meta-analysis.
        Eur Radiol. 2016; 26: 2670-2684
        • Incekara F.
        • Smits M.
        • Dirven L.
        • et al.
        Intraoperative B-Mode Ultrasound Guided Surgery and the Extent of Glioblastoma Resection: A Randomized Controlled Trial.
        Front Oncol. 2021; 11: 649797 -
        • Mahboob S.
        • McPhillips R.
        • Qiu Z.
        • et al.
        Intraoperative Ultrasound-Guided Resection of Gliomas: A Meta-Analysis and Review of the Literature.
        World Neurosurg. 2016 Aug; 92: 255-263
        • Munkvold B.K.R.
        • Jakola A.S.
        • Reinertsen I.
        • Sagberg L.M.
        • Unsgård G.
        • Solheim O.
        The Diagnostic Properties of Intraoperative Ultrasound in Glioma Surgery and Factors Associated with Gross Total Tumor Resection.
        World Neurosurg. 2018; 115: e129-e136
        • Del Bene M.
        • Perin A.
        • Casali C.
        • et al.
        Advanced Ultrasound Imaging in Glioma Surgery: Beyond Gray-Scale B-mode.
        Front Oncol. 2018; 8: 576 -
        • Xiao X.Y.
        • Chen X.
        • Guan X.F.
        • Wu H.
        • Qin W.
        • Luo B.M.
        Superb microvascular imaging in diagnosis of breast lesions: a comparative study with contrast-enhanced ultrasonographic microvascular imaging.
        Br J Radiol. 2016; 89: 20160546
        • Ahn H.S.
        • Lee J.B.
        • Seo M.
        • Park S.H.
        • Choi B.I.
        Distinguishing benign from malignant thyroid nodules using thyroid ultrasonography: utility of adding superb microvascular imaging and elastography.
        Radiol Med. 2018; 123: 260-270
        • Cai S.
        • Wang H.
        • Zhang X.
        • et al.
        Superb Microvascular Imaging Technology Can Improve the Diagnostic Efficiency of the BI-RADS System.
        Front Oncol. 2021; 11634752
        • Fu Z.
        • Zhang J.
        • Lu Y.
        • et al.
        Clinical Applications of Superb Microvascular Imaging in the Superficial Tissues and Organs: A Systematic Review.
        Acad Radiol. 2021; 28: 694-703
        • Gitto S.
        • Messina C.
        • Chianca V.
        • et al.
        Superb microvascular imaging (SMI) in the evaluation of musculoskeletal disorders: a systematic review.
        Radiol Med. 2020; 125: 481-490
        • Prado-Costa R.
        • Rebelo J.
        • Monteiro-Barroso J.
        • Preto A.S.
        Ultrasound elastography: compression elastography and shear-wave elastography in the assessment of tendon injury.
        Insights Imaging. 2018; 9: 791-814
        • Ozturk A.
        • Grajo J.R.
        • Dhyani M.
        • Anthony B.W.
        • Samir A.E.
        Principles of ultrasound elastography.
        Abdom Radiol (NY). 2018; 43: 773-785
        • Guibal A.
        • Boularan C.
        • Bruce M.
        • et al.
        Evaluation of shearwave elastography for the characterisation of focal liver lesions on ultrasound.
        Eur Radiol. 2013; 23: 1138-1149
        • Hong S.
        • Woo O.H.
        • Shin H.S.
        • Hwang S.Y.
        • Cho K.R.
        • Seo B.K.
        Reproducibility and diagnostic performance of shear wave elastography in evaluating breast solid mass.
        Clin Imaging. 2017; 44: 42-45
        • Samir A.E.
        • Dhyani M.
        • Anvari A.
        • et al.
        Shear-Wave Elastography for the Preoperative Risk Stratification of Follicular-patterned Lesions of the Thyroid: Diagnostic Accuracy and Optimal Measurement Plane.
        Radiology. 2015; 277: 565-573
        • Ishikawa M.
        • Ota Y.
        • Nagai M.
        • Kusaka G.
        • Tanaka Y.
        • Naritaka H.
        Ultrasonography Monitoring with Superb Microvascular Imaging Technique in Brain Tumor Surgery.
        World Neurosurg. 2017; 97: 749e11-e20
        • Louis D.N.
        Molecular pathology of malignant gliomas.
        Annu Rev Pathol. 2006; 1: 97-117
        • Reiss-Zimmermann M.
        • Streitberger K.J.
        • Sack I.
        • et al.
        High Resolution Imaging of Viscoelastic Properties of Intracranial Tumours by Multi-Frequency Magnetic Resonance Elastography.
        Clin Neuroradiol. 2015; 25: 371-378
        • Cepeda S.
        • Barrena C.
        • Arrese I.
        • Fernandez-Pérez G.
        • Sarabia R.
        Intraoperative Ultrasonographic Elastography: A Semi-Quantitative Analysis of Brain Tumor Elasticity Patterns and Peritumoral Region.
        World Neurosurg. 2020; 135: e258-e270
        • Chauvet D.
        • Imbault M.
        • Capelle L.
        • et al.
        In Vivo Measurement of Brain Tumor Elasticity Using Intraoperative Shear Wave Elastography.
        Ultraschall in Medizin und Biologie. 2016; 37: 584-590
        • Lu R.
        • Meng Y.
        • Zhang Y.
        • et al.
        Superb microvascular imaging (SMI) compared with conventional ultrasound for evaluating thyroid nodules.
        BMC Med Imaging. 2017 Dec 28; 17: 65
        • Shen T.T.
        • Xue J.L.
        Impact of a novel ultrasound microvascular imaging and elastography on prostate cancer classification.
        Transl Androl Urol. 2019; 8: 696-702
        • Park A.Y.
        • Seo B.K.
        • Cha S.H.
        • Yeom S.K.
        • Lee S.W.
        • Chung H.H.
        An Innovative Ultrasound Technique for Evaluation of Tumor Vascularity in Breast Cancers: Superb Micro-Vascular Imaging.
        J Breast Cancer. 2016; 19: 210-213
        • Park A.Y.
        • Seo B.K.
        • Woo O.H.
        • et al.
        The utility of ultrasound superb microvascular imaging for evaluation of breast tumour vascularity: comparison with colour and power Doppler imaging regarding diagnostic performance.
        Clin Radiol. 2018 Mar; 73: 304-311
        • Jiang Z.-A.-O.
        • Huang Y.H.
        • Shen H.L.
        • Liu X.T.
        Clinical Applications of Superb Microvascular Imaging in the Liver, Breast, Thyroid, Skeletal Muscle, and Carotid Plaques.
        J Ultrasound Med. 2019 Nov; 38: 2811-2820
        • Ayaz E.-A.-O.
        • Aslan A.-A.-O.
        • İnan İ.
        • Yıkılmaz A.
        Evaluation of Ovarian Vascularity in Children by Using the “Superb Microvascular Imaging” Ultrasound Technique in Comparison With Conventional Doppler Ultrasound Techniques.
        J Ultrasound Med. 2019 Oct; 38: 2751-2760
        • Ahir B.K.
        • Engelhard H.H.
        • Lakka S.S.
        Tumor Development and Angiogenesis in Adult Brain Tumor: Glioblastoma.
        Mol Neurobiol. 2020; 57: 2461-2478
        • Nagy J.A.
        • Chang S.-H.
        • Shih S.-C.
        • Dvorak A.M.
        • Dvorak H.F.
        Heterogeneity of the tumor vasculature.
        Semin Thromb Hemost. 2010; 36: 321-331
        • Dvorak H.F.
        Rous-Whipple Award Lecture. How tumors make bad blood vessels and stroma.
        Am J Pathol. 2003; 162: 1747-1757