Top

Published in:

Open Access 01-12-2024 | Glioblastoma | Original Article

Mechanical characteristics of glioblastoma and peritumoral tumor-free human brain tissue

Authors: Jessica Kren, Isabelle Skambath, Patrick Kuppler, Steffen Buschschlüter, Nicolas Detrez, Sazgar Burhan, Robert Huber, Ralf Brinkmann, Matteo Mario Bonsanto

Published in: Acta Neurochirurgica | Issue 1/2024

Abstract

Background

The diagnosis of brain tumor is a serious event for the affected patient. Surgical resection is a crucial part in the treatment of brain tumors. However, the distinction between tumor and brain tissue can be difficult, even for experienced neurosurgeons. This is especially true in the case of gliomas. In this project we examined whether the biomechanical parameters elasticity and stress relaxation behavior are suitable as additional differentiation criteria between tumorous (glioblastoma multiforme; glioblastoma, IDH-wildtype; GBM) and non-tumorous, peritumoral tissue.

Methods

Indentation measurements were used to examine non-tumorous human brain tissue and GBM samples for the biomechanical properties of elasticity and stress-relaxation behavior. The results of these measurements were then used in a classification algorithm (Logistic Regression) to distinguish between tumor and non-tumor.

Results

Differences could be found in elasticity spread and relaxation behavior between tumorous and non-tumorous tissue. Classification was successful with a sensitivity/recall of 83% (sd = 12%) and a precision of 85% (sd = 9%) for detecting tumorous tissue.

Conclusion

The findings imply that the data on mechanical characteristics, with particular attention to stress relaxation behavior, can serve as an extra element in differentiating tumorous brain tissue from non-tumorous brain tissue.

Acerbi F, Broggi M, Schebesch K, Höhne J, Cavallo C, De Laurentis C, Eoli M, Anghileri E, Servida M, Boffano C, Pollo B, Schiariti M, Visintini S, Montomoli C, Bosio L, La Corte E, Broggi G, Brawanski A, Ferroli P (2018) Fluorescein-guided surgery for resection of high-grade gliomas: a multicentric prospective phase II study (FLUOGLIO). Clin Cancer Res: Off J Am Assoc Cancer Res 24:52–61. https://doi.org/10.1158/1078-0432.CCR-17-1184

Aunan-Diop J, Halle B, Pedersen CB, Jensen U, Munthe S, Harbo F, Andersen MS, Poulsen FR (2022) Magnetic resonance elastography in intracranial neoplasms: a scoping review. Top Magn Reson Imaging 31(1):9–22. https://doi.org/10.1097/RMR.0000000000000292CrossRefPubMed

Barnes JM, Przybyla L, Weaver VM, Ewald A (2017) Tissue mechanics regulate brain development, homeostasis and disease. J Cell Sci 130(1):71–82. https://doi.org/10.1242/jcs.191742CrossRefPubMedPubMedCentral

Belykh E, Miller EJ, Carotenuto A, Patel AA, Cavallo C, Martirosyan NL, Healey DR, Byvaltsev VA, Scheck AC, Lawton MT, Eschbacher JM, Nakaji P, Preul MC (2019) Progress in confocal laser endomicroscopy for neurosurgery and technical nuances for brain tumor imaging with fluorescein. Front Oncol 9:554. https://doi.org/10.3389/fonc.2019.00554CrossRefPubMedPubMedCentral

Broggi G, Brawanski A, Ferroli P (2018) Fluorescein-guided surgery for resection of high-grade gliomas: a multicentric prospective phase II study (FLUOGLIO). Clin Cancer Res 24(1):52–61. https://doi.org/10.1158/1078-0432.CCR-17-1184CrossRefPubMed

Brown TJ, Brennan MC, Li M, Church EW, Brandmeir NJ, Rakszawski KL, Patel AS, Rizk EB, Suki D, Sawaya R, Glantz M (2016) Association of the extent of resection with survival in glioblastoma: a systematic review and meta-analysis. JAMA Oncol 2(11):1460–1469. https://doi.org/10.1001/jamaoncol.2016.1373CrossRefPubMedPubMedCentral

Budday S, Nay R, Rooij Rd, Steinmann P, Wyrobek T, Ovaert TC, Kuhl E (2015) Mechanical properties of gray and white matter brain tissue by indentation. J Mech Behav Biomed Mater 46:318–330. https://doi.org/10.1016/j.jmbbm.2015.02.024CrossRefPubMedPubMedCentral

Budday S, Sommer G, Holzapfel GA, Steinmann P, Kuhl E (2017) Viscoelastic parameter identification of human brain tissue. J Mech Behav Biomed Mater 74:463–476. https://doi.org/10.1016/j.jmbbm.2017.07.014CrossRefPubMed

Budday S, Sommer G, Haybaeck J, Steinmann P, Holzapfel GA, Kuhl E (2017) Rheological characterization of human brain tissue. Acta Biomaterialia 60:315–329. https://doi.org/10.1016/j.actbio.2017.06.024CrossRefPubMed

10.

Budday S, Ovaert TC, Holzapfel GA, Steinmann P, Kuhl E (2020) Fifty shades of brain: a review on the mechanical testing and modeling of brain tissue. Arch Comput Methods Eng 27(4):1187–1230. https://doi.org/10.1007/s11831-019-09352-wCrossRef

11.

Burhan S, Detrez N, Rewerts K, Strenge P, Buschschlüter S, Kren J, Hagel C, Bonsanto MM, Brinkmann R, Huber R (2024) Phase unwrapping for MHz optical coherence elastography and application to brain tumor tissue. Biomed Opt Express 15:1038–1058. https://doi.org/10.1364/BOE.510020

12.

Cepeda S, García-García S, Arrese I, Velasco-Casares M, Sarabia R (2022) Advantages and limitations of intraoperative ultrasound strain elastography applied in brain tumor surgery: a single- center experience. Operative Neurosurgery 22(5):305–314. https://doi.org/10.1227/ons.0000000000000122CrossRefPubMed

13.

Chan HW, Uff C, Chakraborty A, Dorward N, Bamber JC (2021) Clinical application of shear wave elastography for assisting brain tumor resection. Front Oncol 11:619286. https://doi.org/10.3389/fonc.2021.619286CrossRefPubMedPubMedCentral

14.

Detrez N, Burhan S, Rewerts K, Kren J, Hagel C, Bonsanto MM, Theisen-Kunde D, Huber R, Brinkmann R (2023) Air-Jet based optical coherence elastography: processing and mechanical interpretation of brain tumor data. In: Optical Elastography and Tissue Biomechanics X Proc. SPIE 12381, Optical Elastography and Tissue Biomechanics X, 1238105. https://doi.org/10.1117/12.2649835

15.

Detrez N, Rewerts K, Matthiae M, Buschschlüter S, Bonsanto MM, Theisen-Kunde D, Brinkmann R (2021) Flow Controlled Air Puff Generator Towards In Situ Brain Tumor Detection Based on MHz Optical Coherence Elastography. Beitrag in European Conference on Biomedical Optics 2021, München, Deutschland

16.

Detrez N, Burhan S, Strenge P, Kren J, Hagel C, Bonsanto MM, Theisen-Kunde D, Huber R, Brinkmann R (2023) Air-jet based optical coherence elastography of brain tumor tissue: stiffness evaluation by structural histological analysis. In Nadkarni SK, Scarcelli G (Hrsg.) Emerging Technologies for Cell and Tissue Characterization II (Band 12629, S. 126290M). SPIE. https://doi.org/10.1117/12.2670944

17.

Dommelen JA, Sande TPJ, Hrapko M, Peters GWM (2010) Mechanical properties of brain tissue by indentation: interregional variation. J Mech Behav Biomed Mater 3(2):158–166. https://doi.org/10.1016/j.jmbbm.2009.09.001CrossRefPubMed

18.

Eichberg DG, Shah AH, Di L, Semonche AM, Jimsheleishvili G, Luther EM, Sarkiss CA, Levi AD, Gultekin SH, Komotar RJ, Ivan ME (2021) Stimulated Raman histology for rapid and accurate intraoperative diagnosis of CNS tumors: prospective blinded study. J Neurosurg 134(1):137–143. https://doi.org/10.3171/2019.9.jns192075CrossRef

19.

Eskandari F, Rahmani Z, Shafieian M (2020) The effect of large deformation on Poisson’s ratio of brain white matter: an experimental study. Proc Inst Mech Eng Part H: J Eng Med 235:401–407CrossRef

20.

Fu Z, Zhu G, Luo C, Chen Z, Dou Z, Chen Y, Zhong C, Su S, Liu F (2022) Matricellular protein tenascin C: Implications in glioma progression, gliomagenesis, and treatment. Front Oncol 12:971462. https://doi.org/10.3389/fonc.2022.971462CrossRefPubMedPubMedCentral

21.

Goryaynov SA, Widhalm G, Goldberg MF, Chelushkin D, Spallone A, Chernyshov KA, Ryzhova M, Pavlova G, Revischin A, Shishkina L, Jukov V, Savelieva T, Victor L, Potapov A (2019) The role of 5-ALA in low-grade gliomas and the influence of antiepileptic drugs on intraoperative fluorescence. Front Oncol 9:423. https://doi.org/10.3389/fonc.2019.00423CrossRefPubMedPubMedCentral

22.

Gousias K, Markou M, Voulgaris S, Goussia A, Voulgari P, Bai M, Polyzoidis K, Kyritsis A, Alamanos Y (2009) Descriptive epidemiology of cerebral gliomas in northwest Greece and study of potential predisposing factors, 2005–2007. Neuroepidemiology 33(2):89–95. https://doi.org/10.1159/000222090CrossRefPubMed

23.

Hayes WC, Keer LM, Herrmann G, Mockros LF (1972) A mathematical analysis for indentation tests of articular cartilage. J Biomech 5(5):541–551. https://doi.org/10.1016/0021-9290(72)90010-3CrossRefPubMed

24.

Ji M, Lewis S, Camelo-Piragua S, Ramkissoon SH, Snuderl M, Venneti S, Fisher-Hubbard A, Garrard M, Fu D, Wang AC, Heth JA, Maher CO, Sanai N, Johnson TD, Freudiger CW, Sagher O, Xie XS, Orringer DA (2015) Detection of human brain tumor infiltration with quantitative stimulated Raman scattering microscopy. Sci Transl Med 7(309):309–163309163. https://doi.org/10.1126/scitranslmed.aab0195CrossRef

25.

Khoonkari M, Liang D, Kamperman M, Kruyt FAE, Rijn Pv (2022) Physics of brain cancer: multiscale alterations of glioblastoma cells under extracellular matrix stiffening. Pharmaceutics 14(5):1031. https://doi.org/10.3390/pharmaceutics14051031CrossRefPubMedPubMedCentral

26.

Kiesel B, Freund J, Reichert D, Wadiura L, Erkkilae MT, Woehrer A, Hervey-Jumper S, Berger MS, Widhalm G (2021) 5-ALA in suspected low-grade gliomas: current role, limitations, and new approaches. Front Oncol 17(11):699301. https://doi.org/10.3389/fonc.2021.699301CrossRef

27.

Korja M, Raj R, Seppä K, Luostarinen T, Malila N, Seppälä M, Mäenpää H, Pitkäniemi J (2018) Glioblastoma survival is improving despite increasing incidence rates: a nationwide study between 2000 and 2013 in Finland. Neuro-Oncology 21(3):370–379. https://doi.org/10.1093/neuonc/noy164CrossRefPubMedCentral

28.

Kuppler P, Strenge P, Lange B, Spahr-Hess S, Draxinger W, Hagel C, Theisen-Kunde D, Brinkmann R, Huber R, Tronnier V, Bonsanto MM (2023) The neurosurgical benefit of contactless in vivo optical coherence tomography regarding residual tumor detection: a clinical study. Front Oncol 13:1151149. https://doi.org/10.3389/fonc.2023.1151149CrossRefPubMedPubMedCentral

29.

Lee C-H, Jung K-W, Yoo H, Park S, Lee SH (2010) Epidemiology of primary brain and central nervous system tumors in Korea. J Korean Neurosurg Soc 48(2):145–152. https://doi.org/10.3340/jkns.2010.48.2.145CrossRefPubMedPubMedCentral

30.

Li YM, Suki D, Hess K, Sawaya R (2016) The influence of maximum safe resection of glioblastoma on survival in 1229 patients: Can we do better than gross-total resection? J Neurosurg 124(4):977–988. https://doi.org/10.3171/2015.5.JNS142087CrossRefPubMed

31.

Orringer DA, Pandian B, Niknafs YS, Hollon TC, Boyle J, Lewis S, Garrard M, Hervey-Jumper SL, Garton HJL, Maher CO, Heth JA, Sagher O, Wilkinson DA, Snuderl M, Venneti S, Ramkissoon SH, McFadden KA, Fisher-Hubbard A, Lieberman AP, Johnson TD, Xie XS, Trautman JK, Freudiger CW, Camelo-Piragua S (2017) Rapid intraoperative histology of unprocessed surgical specimens via fibre-laser-based stimulated Raman scattering microscopy. Nat Biomed Eng 1(2):0027. https://doi.org/10.1038/s41551-016-0027CrossRefPubMedPubMedCentral

32.

Palmieri G, Cofano F, Salvati LF et al (2021) Fluorescence-guided surgery for high-grade gliomas: state of the art and new perspectives. Technol Cancer Res Treat 20:153303382110216. https://doi.org/10.1177/15330338211021605CrossRef

33.

Philips A, Henshaw DL, Lamburn G, O’Carroll MJ (2018) Brain tumours: rise in glioblastoma multiforme incidence in England 1995–2015 suggests an adverse environmental or lifestyle factor. J Environ Public Health 2018:7910754. https://doi.org/10.1155/2018/7910754CrossRefPubMedPubMedCentral

34.

Restelli F, Mathis AM, Höhne J, Mazzapicchi E, Acerbi F, Pollo B, Quint K (2022) Confocal laser imaging in neurosurgery: a comprehensive review of sodium fluorescein-based CONVIVO preclinical and clinical applications. Front Oncol 12:998384. https://doi.org/10.3389/fonc.2022.998384CrossRefPubMedPubMedCentral

35.

Santos MS, Soares JP, Abreu PH, Araujo H, Santos J (2018) Cross-validation for imbalanced datasets: Avoiding overoptimistic and overfitting approaches [research frontier]. IEEE Comput Intell Mag 13(4):59–76. https://doi.org/10.1109/MCI.2018.2866730CrossRef

36.

Sasaki N (2012) Viscoelasticity - From Theory to Biological Applications. https://doi.org/10.5772/49979

37.

Steinmeier R, Rachinger J, Kaus M, Ganslandt O, Huk W, Fahlbusch R (2002) Factors influencing the application accuracy of neuronavigation systems. Stereotact Funct Neurosurg 75(4):188–202. https://doi.org/10.1159/000048404CrossRef

38.

Stewart DC, Rubiano A, Dyson K, Simmons CS (2017) Mechanical characterization of human brain tumors from patients and comparison to potential surgical phantoms. PLoS ONE 12(6):0177561. https://doi.org/10.1371/journal.pone.0177561CrossRef

39.

Stieglitz LH, Fichtner J, Andres R, Schucht P, Krähenbühl A-K, Raabe A, Beck J (2013) The silent loss of neuronavigation accuracy: a systematic retrospective analysis of factors influencing the mismatch of frameless stereotactic systems in cranial neurosurgery. Neurosurgery 72(5):796–807. https://doi.org/10.1227/neu.0b013e318287072dCrossRefPubMed

40.

Weickenmeier J, Rooij Rd, Budday S, Steinmann P, Ovaert TC, Kuhl E (2016) Brain stiffness increases with myelin content. Acta Biomaterialia 42:265–272. https://doi.org/10.1016/j.actbio.2016.07.040CrossRefPubMed

41.

Xia L, Fang C, Chen G, Sun C (2018) Relationship between the extent of resection and the survival of patients with low-grade gliomas: a systematic review and meta-analysis. BMC Cancer 18(1):48. https://doi.org/10.1186/s12885-017-3909-xCrossRefPubMedPubMedCentral

42.

Xu Y, Mathis AM, Pollo B, Schlegel J, Maragkou T, Seidel K, Schucht P, Smith KA, Porter RW, Raabe A, Little AS, Sanai N, Agbanyim DC, Martirosyan NL, Eschbacher JM, Quint K, Preul MC, Hewer E (2023) Intraoperative in vivo confocal laser endomicroscopy imaging at glioma margins: can we detect tumor infiltration? J Neurosurg 1–10. https://doi.org/10.3171/2023.5.jns23546

43.

Zeng L, Mei Q, Li H, Ke C, Yu J, Chen J (2021) A survival analysis of surgically treated incidental low-grade glioma patients. Sci Rep 11(1):8522. https://doi.org/10.1038/s41598-021-88023-yCrossRefPubMedPubMedCentral

44.

Zhang M, Zheng YP, Mak AFT (1997) Estimating the effective Young’s modulus of soft tissues from indentation tests—nonlinear finite element analysis of effects of friction and large deformation. Med Eng Phys 19(6):512–517. https://doi.org/10.1016/s1350-4533(97)00017-9CrossRefPubMed

Title: Mechanical characteristics of glioblastoma and peritumoral tumor-free human brain tissue
Authors: Jessica Kren
Isabelle Skambath
Patrick Kuppler
Steffen Buschschlüter
Nicolas Detrez
Sazgar Burhan
Robert Huber
Ralf Brinkmann
Matteo Mario Bonsanto
Publication date: 01-12-2024
Publisher: Springer Vienna
Keywords: Glioblastoma
Glioblastoma
Glioblastoma
Brain Tumor
Published in: Acta Neurochirurgica / Issue 1/2024
Print ISSN: 0001-6268
Electronic ISSN: 0942-0940
DOI: https://doi.org/10.1007/s00701-024-06009-x

Keynote webinar | Spotlight on medication adherence

Springer Medicine

Mechanical characteristics of glioblastoma and peritumoral tumor-free human brain tissue

Abstract

Background

Methods

Results

Conclusion

Keynote webinar | Spotlight on medication adherence

Springer Medicine

Abstract

Background

Methods

Results

Conclusion

Please log in to get access to this content

Other articles of this Issue 1/2024

Identification and decompression of superior cluneal nerve implicated in low back pain

Stereotactic frame-based biopsy of infratentorial lesions via the suboccipital-transcerebellar approach with the Zamorano-Duchovny stereotactic system—a retrospective analysis of 79 consecutive cases

Unintended dural tears during unilateral biportal endoscopic lumbar surgery: incidence and risk factors

Functional magnetic resonance imaging (fMRI) as adjunct for planning laser interstitial thermal therapy (LITT) near eloquent structures

Retrogasserian trigeminal radiofrequency-thermorhizotmoy for trigeminal neuralgia

Peripheral blood syndecan-1 levels after mechanical thrombectomy can predict the clinical prognosis of patients with acute ischemic stroke