Advanced Ultrasound Imaging in Glioma Surgery: Beyond Gray-Scale B-mode

Massimiliano Del Bene, Alessandro Perin, Cecilia Casali, Federico Legnani, Andrea Saladino, Luca Mattei, Ignazio Gaspare Vetrano, Marco Saini, Francesco DiMeco, Francesco Prada, Massimiliano Del Bene, Alessandro Perin, Cecilia Casali, Federico Legnani, Andrea Saladino, Luca Mattei, Ignazio Gaspare Vetrano, Marco Saini, Francesco DiMeco, Francesco Prada

Abstract

Introduction: Glioma surgery is aimed at obtaining maximal safe tumor resection while preserving or improving patient's neurological status. For this reason, there is growing interest for intra-operative imaging in neuro-oncological surgery. Intra-operative ultrasound (ioUS) provides the surgeon with real-time, anatomical and functional information. Despite this, in neurosurgery ioUS mainly relies only on gray-scale brightness mode (B-mode). Many other ultrasound imaging modalities, such as Fusion Imaging with pre-operative acquired magnetic resonance imaging (MRI), Doppler modes, Contrast Enhanced Ultrasound (CEUS), and elastosonography have been developed and have been extensively used in other organs. Although these modalities offer valuable real-time intra-operative information, so far their usage during neurosurgical procedures is still limited. Purpose: To present an US-based multimodal approach for image-guidance in glioma surgery, highlighting the different features of advanced US modalities: fusion imaging with pre-operative acquired MRI for Virtual Navigation, B-mode, Doppler (power-, color-, spectral-), CEUS, and elastosonography. Methods: We describe, in a step-by-step fashion, the applications of the most relevant advanced US modalities during different stages of surgery and their implications for surgical decision-making. Each US modality is illustrated from a technical standpoint and its application during glioma surgery is discussed. Results: B-mode offers dynamic morphological information, which can be further implemented with fusion imaging to improve image understanding and orientation. Doppler imaging permits to evaluate anatomy and function of the vascular tree. CEUS allows to perform a real-time angiosonography, providing valuable information in regards of parenchyma and tumor vascularization and perfusion. This facilitates tumor detection and surgical strategy, also allowing to characterize tumor grade and to identify residual tumor. Elastosonography is a promising tool able to better define tumor margins, parenchymal infiltration, tumor consistency and permitting differentiation of high grade and low grade lesions. Conclusions: Multimodal ioUS represents a valuable tool for glioma surgery being highly informative, rapid, repeatable, and real-time. It is able to differentiate low grade from high grade tumors and to provide the surgeon with relevant information for surgical decision-making. ioUS could be integrated with other intra-operative imaging and functional approaches in a synergistic manner to offer the best image guidance for each patient.

Keywords: B-mode; Doppler; Glioma; contrast enhanced ultrasound; elastography; fusion imaging; intra-operative ultrasound; navigated ultrasound.

Figures

Figure 1
Figure 1
B-mode representation of different glioma grades. (A) Left temporal pilocytic astrocytoma. (B) Left temporal diffuse astrocytoma. (C) Right parietal anaplastic astrocytoma. (D) Right temporo-parietal glioblastoma. (1) pre-operative volumetric MRI. (2) Intra-operative trans-dural US scan. Note the different lesion appearances and in particular the different degree of margins definition.
Figure 2
Figure 2
Navigated intra-operative B-mode US in a case of left temporo-insular low-grade glioma. Two different configurations of navigated ioUS are displayed: (A) side-by-side or (B) superimposition. The continuous comparison between the two modalities aid in orientation and understanding of ioUS images.
Figure 3
Figure 3
Navigated intra-operative B-mode US in the final stages of surgery. (A) Left temporal anaplastic astrocytoma. (B) Right fronto-temporal glioblastoma. The comparison between ioUS and corresponding pre-operative MRI aid in identifying residual tumor and understanding ioUS semiotics: (A) side-by-side view, (B) superimposition.
Figure 4
Figure 4
Navigated ioUS (advanced modalities). (A) Color and spectral Doppler in a case of left temporo-insular anaplastic oligodendroglioma. (B) Contrast enhanced ultrasound in a case of left insular anaplastic astrocytoma. (C) Strain elastography in a case of left temporal glioblastoma; note the differences between the necrotic and the cystic areas and the interface with surrounding brain. Exploiting the continuous comparison between ioUS an pre-operative MRI is possible to understand US images and to infer about US and MRI correspondences. Legends are as follow: arrow heads: interface between tumor and brain; N: necrotic part of the tumor; C: cystic part of the tumor.
Figure 5
Figure 5
Doppler modalities. (A,B) Color Doppler and spectral doppler in a case of left temporal glioblastoma. (C,D) Power Doppler in a case of right temporal glioblastoma. Color Doppler informs on presence of flow, its direction and velocity through the setting of a region of interest. Spectral Doppler allows for a systematic analysis of flow-velocity over time thus permitting to characterize vessels nature. Power Doppler provides information on amplitude of flow depicting the number of scattering molecules (mainly erythrocytes).
Figure 6
Figure 6
CEUS representation of different glioma grades. (A,B) Right frontal low-grade glioma, (C,D) right frontal anaplastic astrocytoma, (E,F) left frontal glioblastoma. These images demonstrate the different degree and pattern of contrast enhancement among different glioma grades.
Figure 7
Figure 7
Time-frame of contrast enhancement in a case of right temporal glioblastoma. GBM have a rapid arterial and venous phase. MBs transit is chaotic and the peak is extremely intense. The major arterial supplies and draining veins are clearly visible. Contrast enhancement pattern is irregular and heterogeneous CE with both nodular high-enhanced and hypoperfused areas. Tumor borders are better defined than in B-mode.
Figure 8
Figure 8
Comparison between pre- (A) and post-resection (B) CEUS scans in a case of right temporo-parietal glioblastoma. After tumor removal, B-mode became difficult to understand because of surgical-induced artifacts whereas CEUS clearly demonstrates the presence of potential residual tumor.
Figure 9
Figure 9
Strain elastography (SE) scans in different glioma grades. (A,B) SE in a case of right parietal low grade glioma. (C,D) SE in a case of right fronto-parietal glioblastoma. SE is able to differentiate between LGG and HGG relying on their stiffness. LGG appear stiffer than brain whereas HGG softer. Furthermore, SE aid in identifying tumor borders and in distinguishing tumor and edema. (T: tumor, B: brain, arrow heads: interface between tumor and surrounding brain).

References

    1. Network NCC. Central Nervous System Cancers (Version 1.2016). Clinical Practice Guidelines in Oncology (2016).
    1. D'Amico RS, Englander ZK, Canoll P, Bruce JN. Extent of resection in glioma-a review of the cutting edge. World Neurosurg. (2017) 103:538–49. 10.1016/j.wneu.2017.04.041
    1. Aghi MK, Nahed BV, Sloan AE, Ryken TC, Kalkanis SN, Olson JJ. The role of surgery in the management of patients with diffuse low grade glioma: a systematic review and evidence-based clinical practice guideline. J Neurooncol. (2015) 125:503–30. 10.1007/s11060-015-1867-1
    1. Duffau H. The role of surgery in low-grade gliomas: do timing and extent of resection matter? CNS Oncol. (2017) 6:179–83. 10.2217/cns-2017-0009
    1. Jakola AS, Skjulsvik AJ, Myrmel KS, Sjavik K, Unsgard G, Torp SH, et al. . Surgical resection versus watchful waiting in low-grade gliomas. Ann Oncol. (2017) 28:1942–8. 10.1093/annonc/mdx230
    1. Orringer D, Lau D, Khatri S, Zamora-Berridi GJ, Zhang K, Wu C, et al. . Extent of resection in patients with glioblastoma: limiting factors, perception of resectability, and effect on survival. J Neurosurg. (2012) 117:851–9. 10.3171/2012.8.JNS12234
    1. Jenkinson MD, Barone DG, Bryant A, Vale L, Bulbeck H, Lawrie TA, et al. . Intraoperative imaging technology to maximise extent of resection for glioma. Cochrane Database Syst Rev. (2018) 1:Cd012788. 10.1002/14651858.CD012788.pub2
    1. Kut C, Chaichana KL, Xi J, Raza SM, Ye X, McVeigh ER, et al. . Detection of human brain cancer infiltration ex vivo and in vivo using quantitative optical coherence tomography. Sci Transl Med. (2015) 7:292ra100–292ra100. 10.1126/scitranslmed.3010611
    1. Mahboob S, McPhillips R, Qiu Z, Jiang Y, Meggs C, Schiavone G, et al. . Intraoperative ultrasound-guided resection of gliomas: a meta-analysis and review of the literature. World Neurosurg. (2016) 92:255–63. 10.1016/j.wneu.2016.05.007
    1. Prada FE, Solbiati LE, Martegani AE, DiMeco FE. (editors). Intraoperative Ultrasound (IOUS) in Neurosurgery. In: From Standard B-mode to Elastosonography. Springer International Publishing; (2016).
    1. Coburger J, Nabavi A, Konig R, Wirtz CR, Pala A. Contemporary use of intraoperative imaging in glioma surgery: a survey among EANS members. Clin Neurol Neurosurg. (2017) 163:133–41. 10.1016/j.clineuro.2017.10.033
    1. Senders JT, Muskens IS, Schnoor R, Karhade AV, Cote DJ, Smith TR, et al. . Agents for fluorescence-guided glioma surgery: a systematic review of preclinical and clinical results. Acta Neurochir. (2017) 159:151–67. 10.1007/s00701-016-3028-5
    1. Suero Molina E, Schipmann S, Stummer W. Maximizing safe resections: the roles of 5-aminolevulinic acid and intraoperative MR imaging in glioma surgery-review of the literature. Neurosurg Rev. (2017) [Epub ahead of print]. 10.1007/s10143-017-0907-z
    1. Zhang J, Fan Y, He M, Ma X, Song Y, Liu M, et al. . Accuracy of Raman spectroscopy in differentiating brain tumor from normal brain tissue. Oncotarget (2017b) 8:36824–31. 10.18632/oncotarget.15975
    1. Reid MH. Ultrasonic visualization of a cervical cord cystic astrocytoma. AJR Am J Roentgenol. (1978) 131:907–8. 10.2214/ajr.131.5.907
    1. Makuuchi M, Torzilli G, Machi J. History of intraoperative ultrasound. Ultrasound Med Biol. (1998) 24:1229–42. 10.1016/S0301-5629(98)00112-4
    1. Dohrmann GJ, Rubin JM. History of intraoperative ultrasound in neurosurgery. Neurosurg Clin N Am. (2001) 12:155–66, ix. 10.1016/S1042-3680(18)30074-3
    1. Ng A, Swanevelder J. Resolution in ultrasound imaging. Cont Educ Anaesth Critic Care Pain (2011) 11:186–92. 10.1093/bjaceaccp/mkr030
    1. Wang J, Liu X, Ba YM, Yang YL, Gao GD, Wang L, et al. . Effect of sonographically guided cerebral glioma surgery on survival time. J Ultrasound Med. (2012) 31:757–62. 10.7863/jum.2012.31.5.757
    1. Sastry R, Bi WL, Pieper S, Frisken S, Kapur T, Wells W., III, et al. . Applications of ultrasound in the resection of brain tumors. J. Neuroimaging (2017) 27:5–15. 10.1111/jon.12382
    1. Zhang G, Li Z, Si D, Shen L. Diagnostic ability of intraoperative ultrasound for identifying tumor residual in glioma surgery operation. Oncotarget (2017) 8:73105–14. 10.18632/oncotarget.20394
    1. Munkvold BKR, Jakola AS, Reinertsen I, Sagberg LM, Unsgard G, Solheim O. The diagnostic properties of intraoperative ultrasound in glioma surgery and factors associated with gross total tumor resection. World Neurosurg. (2018) 115:e129–36. 10.1016/j.wneu.2018.03.208
    1. Solheim O, Selbekk T, Jakola AS, Unsgard G. Ultrasound-guided operations in unselected high-grade gliomas–overall results, impact of image quality and patient selection. Acta Neurochir. (2010) 152:1873–86. 10.1007/s00701-010-0731-5
    1. Moiyadi AV, Shetty PM, Mahajan A, Udare A, Sridhar E. Usefulness of three-dimensional navigable intraoperative ultrasound in resection of brain tumors with a special emphasis on malignant gliomas. Acta Neurochir. (2013) 155:2217–25. 10.1007/s00701-013-1881-z
    1. Moiyadi A, Kannan S, Shetty P. Navigated intraoperative ultrasound for resection of gliomas: predictive value, influence on resection and survival. Neurol India (2015) 63:727–35. 10.4103/0028-3886.166549
    1. Steno A, Matejcik V, Steno J. Letter to the editor: identification of residual glioma using ultrasound miniprobes. Neurosurg Focus (2016) 41:E15. 10.3171/2016.5.FOCUS16180
    1. Enriquez JL, Wu TS. An introduction to ultrasound equipment and knobology. Crit Care Clin. (2014) 30:25–45, v. 10.1016/j.ccc.2013.08.006
    1. Prada F, Del Bene M, Mattei L, Lodigiani L, DeBeni S, Kolev V, et al. . Preoperative magnetic resonance and intraoperative ultrasound fusion imaging for real-time neuronavigation in brain tumor surgery. Ultraschall Med. (2015) 36:174–86. 10.1055/s-0034-1385347
    1. Stieglitz LH, Fichtner J, Andres R, Schucht P, Krahenbuhl AK, Raabe A, et al. . The silent loss of neuronavigation accuracy: a systematic retrospective analysis of factors influencing the mismatch of frameless stereotactic systems in cranial neurosurgery. Neurosurgery (2013) 72:796–807. 10.1227/NEU.0b013e318287072d
    1. Gerard IJ, Kersten-Oertel M, Petrecca K, Sirhan D, Hall JA, Collins DL. Brain shift in neuronavigation of brain tumors: a review. Med Image Anal. (2017) 35:403–20. 10.1016/j.media.2016.08.007
    1. Gibbs V, Cole D, Sassano A. Ultrasound Physics and Technology: How, Why and When. London: Churchill Livingstone/Elsevier; (2009).
    1. Sconfienza LM, Mauri G, Secchi F. Ultrasound system setup and general semeiology. In: Prada F, Solbiati L, Martegani A, DiMeco F. editors. Intraoperative Ultrasound (IOUS) in Neurosurgery: From Standard B-Mode to Elastosonography. Cham: Springer International Publishing; (2016). p. 21–8.
    1. Coburger J, König RW. Intraoperative findings in brain tumor surgery. In: Prada F, Solbiati L, Martegani A, DiMeco F. editors. Intraoperative Ultrasound (IOUS) in Neurosurgery: From Standard B-Mode to Elastosonography. Cham: Springer International Publishing; (2016). p. 41–58.
    1. Prada F, Del Bene M, Moiraghi A, DiMeco F. Echographic brain semeiology and topographic anatomy according to surgical approaches. In: Prada F, Solbiati L, Martegani A, DiMeco F. editors. Intraoperative Ultrasound (IOUS) in Neurosurgery: From Standard B-Mode to Elastosonography. Cham: Springer International Publishing; (2016).p. 29–39.
    1. Prada F, Mattei L, Del Bene M, Aiani L, Saini M, Casali C, et al. . Intraoperative cerebral glioma characterization with contrast enhanced ultrasound. Biomed Res Int. (2014) 2014:484261. 10.1155/2014/484261
    1. Steno A, Matejcik V, Steno J. Intraoperative ultrasound in low-grade glioma surgery. Clin Neurol Neurosurg. (2015) 135:96–9. 10.1016/j.clineuro.2015.05.012
    1. Prada F, Bene MD, Fornaro R, Vetrano IG, Martegani A, Aiani L, et al. . Identification of residual tumor with intraoperative contrast-enhanced ultrasound during glioblastoma resection. Neurosurg Focus (2016) 40:E7. 10.3171/2015.11.FOCUS15573
    1. Šteno A, Giussani C, Riva M. Multimodal imaging in glioma surgery. In: Prada F, Solbiati L, Martegani A, DiMeco F. editors. Intraoperative Ultrasound (IOUS) in Neurosurgery: From Standard B-Mode to Elastosonography. Cham: Springer International Publishing; (2016). p. 81–97.
    1. Steno A, Jezberova M, Holly V, Timarova G, Steno J. Visualization of lenticulostriate arteries during insular low-grade glioma surgeries by navigated 3D ultrasound power Doppler: technical note. J Neurosurg. (2016) 125:1016–23. 10.3171/2015.10.JNS151907
    1. Saether CA, Torsteinsen M, Torp SH, Sundstrom S, Unsgard G, Solheim O. Did survival improve after the implementation of intraoperative neuronavigation and 3D ultrasound in glioblastoma surgery? A retrospective analysis of 192 primary operations. J Neurol Surg A Cent Eur Neurosurg. (2012) 73:73–8. 10.1055/s-0031-1297247
    1. Lindner D, Trantakis C, Renner C, Arnold S, Schmitgen A, Schneider J, et al. . Application of intraoperative 3D ultrasound during navigated tumor resection. Minim Invasive Neurosurg. (2006) 49:197–202. 10.1055/s-2006-947997
    1. Rygh OM, Selbekk T, Torp SH, Lydersen S, Hernes TA, Unsgaard G. Comparison of navigated 3D ultrasound findings with histopathology in subsequent phases of glioblastoma resection. Acta Neurochir. (2008) 150:1033–41; discussion 1042. 10.1007/s00701-008-0017-3
    1. Steno A, Karlik M, Mendel P, Cik M, Steno J. Navigated three-dimensional intraoperative ultrasound-guided awake resection of low-grade glioma partially infiltrating optic radiation. Acta Neurochir. (2012) 154:1255–62. 10.1007/s00701-012-1357-6
    1. Coburger J, Konig RW, Scheuerle A, Engelke J, Hlavac M, Thal DR, et al. . Navigated high frequency ultrasound: description of technique and clinical comparison with conventional intracranial ultrasound. World Neurosurg. (2014) 82:366–75. 10.1016/j.wneu.2014.05.025
    1. Prada F, Del Bene M, Moiraghi A, Casali C, Legnani FG, Saladino A, et al. . From grey scale b-mode to elastosonography: multimodal ultrasound imaging in meningioma surgery—pictorial essay and literature review. Biomed Res Int. (2015) 2015:925729. 10.1155/2015/925729
    1. Moiyadi AV, Unsgård G. Navigable ultrasound, 3D ultrasound and fusion imaging in neurosurgery. In: Prada F, Solbiati L, Martegani A, DiMeco F. editors. Intraoperative Ultrasound (IOUS) in Neurosurgery: From Standard B-Mode to Elastosonography. Cham: Springer International Publishing; (2016). p. 135–45.
    1. Selbekk T, Solheim O, Unsgard G. Ultrasound-guided neurosurgery: experiences from 20 years of cross-disciplinary research in Trondheim, Norway. Neurosurg Focus (2016) 40:E2. 10.3171/2015.12.FOCUS15582
    1. Selbekk T, Jakola AS, Solheim O, Johansen TF, Lindseth F, Reinertsen I, et al. . Ultrasound imaging in neurosurgery: approaches to minimize surgically induced image artefacts for improved resection control. Acta Neurochir. (2013) 155:973–80. 10.1007/s00701-013-1647-7
    1. Unsgard G, Rao V, Solheim O, Lindseth F. Clinical experience with navigated 3D ultrasound angiography (power Doppler) in microsurgical treatment of brain arteriovenous malformations. Acta Neurochir. (2016) 158:875–83. 10.1007/s00701-016-2750-3
    1. Reinertsen I, Lindseth F, Askeland C, Iversen DH, Unsgard G. Intra-operative correction of brain-shift. Acta Neurochir. (2014) 156:1301–10. 10.1007/s00701-014-2052-6
    1. Comeau RM, Sadikot AF, Fenster A, Peters TM. Intraoperative ultrasound for guidance and tissue shift correction in image-guided neurosurgery. Med Phys. (2000) 27:787–800. 10.1118/1.598942
    1. Arbel T, Morandi X, Comeau RM, Collins DL. Automatic non-linear MRI-ultrasound registration for the correction of intra-operative brain deformations. Comput Aided Surg. (2004) 9:123–36. 10.1080/10929080500079248
    1. Reinertsen I, Descoteaux M, Siddiqi K, Collins DL. Validation of vessel-based registration for correction of brain shift. Med Image Anal. (2007) 11:374–88. 10.1016/j.media.2007.04.002
    1. Caldiera V, Caputi L, Ciceri E. Doppler imaging: basic principles and clinical application. In: Prada F, Solbiati L, Martegani A, DiMeco F. editors. Intraoperative Ultrasound (IOUS) in Neurosurgery: From Standard B-Mode to Elastosonography. Cham: Springer International Publishing; (2016) 101–20.
    1. Prada F, Del Bene M, Mauri G, Lamperti M, Vailati D, Richetta C, et al. . Dynamic assessment of venous anatomy and function in neurosurgery with real-time intraoperative multimodal ultrasound: technical note. Neurosurg Focus (2018) 45:E6. 10.3171/2018.4.FOCUS18101
    1. Sidhu PS, Cantisani V, Dietrich CF, Gilja OH, Saftoiu A, Bartels E, et al. . The EFSUMB guidelines and recommendations for the clinical practice of Contrast-Enhanced Ultrasound (CEUS) in non-hepatic applications: update 2017 (Long Version). Ultraschall Med. (2018) 39:e2–e44. 10.1055/a-0586-1107
    1. Prada F, Perin A, Martegani A, Aiani L, Solbiati L, Lamperti M, et al. . Intraoperative contrast-enhanced ultrasound for brain tumor surgery. Neurosurgery (2014) 74:542–52; discussion 552. 10.1227/NEU.0000000000000301
    1. Prada F, Del Bene M, DiMeco F. Contrast-Enhanced Ultrasound (CEUS) in neurosurgery. In: Prada F, Solbiati L, Martegani A, DiMeco F. editors. Intraoperative Ultrasound (IOUS) in Neurosurgery: From Standard B-Mode to Elastosonography. Cham: Springer International Publishing; (2016).p. 159–69.
    1. Dietrich CF, Averkiou M, Nielsen MB, Barr RG, Burns PN, Calliada F, et al. . How to perform Contrast-Enhanced Ultrasound (CEUS). Ultrasound Int Open (2018) 4:E2–e15. 10.1055/s-0043-123931
    1. Schrope BA, Newhouse VL. Second harmonic ultrasonic blood perfusion measurement. Ultrasound Med Biol. (1993) 19:567–79. 10.1016/0301-5629(93)90080-8
    1. Simpson DH, Chin CT, Burns PN. Pulse inversion Doppler: a new method for detecting nonlinear echoes from microbubble contrast agents. IEEE Trans Ultrason Ferroelectr Freq Control (1999) 46:372–82. 10.1109/58.753026
    1. Greis C. Technology overview: SonoVue (Bracco, Milan). Eur Radiol. (2004) 14(Suppl. 8):P11–5. 10.1007/s10406-004-0076-3
    1. Prada F, Del Bene M, Casali C, Saladino A, Legnani FG, Perin A, et al. . Intraoperative navigated angiosonography for skull base tumor surgery. World Neurosurg. (2015) 84:1699–707. 10.1016/j.wneu.2015.07.025
    1. Prada F, Del Bene M, Saini M, Ferroli P, DiMeco F. Intraoperative cerebral angiosonography with ultrasound contrast agents: how I do it. Acta Neurochir. (2015) 157:1025–9. 10.1007/s00701-015-2412-x
    1. Vetrano IG, Prada F, Erbetta A, DiMeco F. Intraoperative ultrasound and Contrast-Enhanced Ultrasound (CEUS) features in a case of intradural extramedullary dorsal schwannoma mimicking an intramedullary lesion. Ultraschall Med. (2015) 36:307–10. 10.1055/s-0035-1552129
    1. Vetrano IG, Prada F, Nataloni IF, Bene MD, Dimeco F, Valentini LG. Discrete or diffuse intramedullary tumor? Contrast-enhanced intraoperative ultrasound in a case of intramedullary cervicothoracic hemangioblastomas mimicking a diffuse infiltrative glioma: technical note and case report. Neurosurg Focus (2015) 39:E17. 10.3171/2015.5.FOCUS15162
    1. Prada F, Del Bene M, DiMeco F. Image guidance in skull base tumor resection: a synergistic approach using intraoperative navigated angiosonography for real-time vessel visualization. Surg Neurol Int. (2016) 7:82. 10.4103/2152-7806.190437
    1. Prada F, Del Bene M, Farago G, DiMeco F. Spinal dural arteriovenous fistula: is there a role for intraoperative contrast-enhanced ultrasound? World Neurosurg (2017) 100:712.e715–8. 10.1016/j.wneu.2017.01.045
    1. Prada F, Vitale V, Del Bene M, Boffano C, Sconfienza LM, Pinzi V, et al. . Contrast-enhanced MR imaging versus contrast-enhanced US: a comparison in glioblastoma surgery by using intraoperative fusion imaging. Radiology (2017) 285:242–9. 10.1148/radiol.2017161206
    1. Bamber J, Cosgrove D, Dietrich CF, Fromageau J, Bojunga J, Calliada F, et al. . EFSUMB guidelines and recommendations on the clinical use of ultrasound elastography. Part 1: basic principles and technology. Ultraschall Med. (2013) 34:169–84. 10.1055/s-0033-1335205
    1. Shiina T, Nightingale KR, Palmeri ML, Hall TJ, Bamber JC, Barr RG, et al. . WFUMB guidelines and recommendations for clinical use of ultrasound elastography: part 1: basic principles and terminology. Ultrasound Med Biol. (2015) 41:1126–47. 10.1016/j.ultrasmedbio.2015.03.009
    1. Cosgrove D, Piscaglia F, Bamber J, Bojunga J, Correas JM, Gilja OH, et al. . EFSUMB guidelines and recommendations on the clinical use of ultrasound elastography. Part 2: Clinical applications. Ultraschall Med. (2013) 34:238–53. 10.1055/s-0033-1335375
    1. Selbekk T, Bang J, Unsgaard G. Strain processing of intraoperative ultrasound images of brain tumours: initial results. Ultrasound Med Biol. (2005) 31:45–51. 10.1016/j.ultrasmedbio.2004.09.011
    1. Uff CE, Garcia L, Fromageau J, Dorward N, Bamber JC. Real-time ultrasound elastography in neurosurgery. In: 2009 IEEE International Ultrasonics Symposium (2009). p. 467–70.
    1. Selbekk T, Brekken R, Solheim O, Lydersen S, Hernes TA, Unsgaard G. Tissue motion and strain in the human brain assessed by intraoperative ultrasound in glioma patients. Ultrasound Med Biol. (2010) 36:2–10. 10.1016/j.ultrasmedbio.2009.05.007
    1. Selbekk T, Brekken R, Indergaard M, Solheim O, Unsgard G. Comparison of contrast in brightness mode and strain ultrasonography of glial brain tumours. BMC Med Imaging (2012) 12:11. 10.1186/1471-2342-12-11
    1. Chauvet D, Imbault M, Capelle L, Demene C, Mossad M, Karachi C, et al. . In vivo measurement of brain tumor elasticity using intraoperative shear wave elastography. Ultraschall Med. (2016) 37:584–90. 10.1055/s-0034-1399152

Source: PubMed

스폰서 및 공동 작업자

건강 상태

약물 개입

3
구독하다