Development and external validation of a non-invasive molecular status predictor of chromosome 1p/19q co-deletion based on MRI radiomics analysis of Low Grade Glioma patients
[en] Purpose
The 1p/19q co-deletion status has been demonstrated to be a prognostic biomarker in lower grade glioma (LGG). The objective of this study was to build a magnetic resonance (MRI)-derived radiomics model to predict the 1p/19q co-deletion status.
Method
209 pathology-confirmed LGG patients from 2 different datasets from The Cancer Imaging Archive were retrospectively reviewed; one dataset with 159 patients as the training and discovery dataset and the other one with 50 patients as validation dataset.
Radiomics features were extracted from T2- and T1-weighted post-contrast MRI resampled data using linear and cubic interpolation methods.
For each of the voxel resampling methods a three-step approach was used for feature selection and a random forest (RF) classifier was trained on the training dataset. Model performance was evaluated on training and validation datasets and clinical utility indexes (CUIs) were computed. The distributions and intercorrelation for selected features were analyzed.
Results
Seven radiomics features were selected from the cubic interpolated features and five from the linear interpolated features on the training dataset. The RF classifier showed similar performance for cubic and linear interpolation methods in the training dataset with accuracies of 0.81 (0.75−0.86) and 0.76 (0.71−0.82) respectively; in the validation dataset the accuracy dropped to 0.72 (0.6−0.82) using cubic interpolation and 0.72 (0.6−0.84) using linear resampling. CUIs showed the model achieved satisfactory negative values (0.605 using cubic interpolation and 0.569 for linear interpolation).
Conclusions
MRI has the potential for predicting the 1p/19q status in LGGs. Both cubic and linear interpolation methods showed similar performance in external validation.
Disciplines :
Radiology, nuclear medicine & imaging
Author, co-author :
Casale, Roberto; Universiteit Maastricht > Precision Medicine
Lavrova, Elizaveta ; Université de Liège - ULiège > GIGA CRC In vivo Imaging - Aging & Memory
Sanduleanu, Sebastian; Universiteit Maastricht > Precision Medicine
Woodruff, Henry; Universiteit Maastricht > Precision Medicine
Lambin, Philippe; Universiteit Maastricht > Precision Medicine
Language :
English
Title :
Development and external validation of a non-invasive molecular status predictor of chromosome 1p/19q co-deletion based on MRI radiomics analysis of Low Grade Glioma patients
H2020 - 733008 - IMMUNOSABR - Clinical proof of concept through a randomised phase II study: a combination of immunotherapy and stereotactic ablative radiotherapy as a curative treatment for limited metastatic lung cancer
Funders :
EC - European Commission
Funding text :
Authors acknowledge financial support from ERC advanced grant (ERC-ADG-2015 n° 694812 - Hypoximmuno), aERC-2018-PoC: 813200-CL-IO, ERC-2020-PoC: 957565-AUTO.DISTINCT, Authors also acknowledge financial support from EUROSTARS (DART, DECIDE), the European Union’s Horizon 2020 research and innovation programme under grant agreement: ImmunoSABR n° 733008, MSCA-ITN-PREDICT n° 766276, FETOPEN- SCANnTREAT n° 899549, CHAIMELEON n° 952172, EuCanImage n° 952103, TRANSCAN Joint Transnational Call 2016 (JTC2016 CLEARLY n° UM 2017-8295) and Interreg V-A Euregio Meuse-Rhine (EURADIOMICS n° EMR4).
Cha, S., Update on brain tumor imaging: from anatomy to physiology. AJNR Am. J. Neuroradiol., 2006, 475–487.
Lanese, A., Franceschi, E., Brandes, A.A., The risk assessment in low-grade gliomas: an analysis of the european organization for research and treatment of Cancer (EORTC) and the radiation therapy oncology group (RTOG) criteria. Oncol. Ther. 6:2 (2018), 105–108.
Claus, E.B., Walsh, K.M., Wiencke, J.K., Molinaro, A.M., Wiemels, J.L., Schildkraut, J.M., Bondy, M.L., Berger, M., Jenkins, R., Wrensch, M., Survival and low-grade glioma: the emergence of genetic information. Neurosurgical Focus, 2015, American Association of Neurological Surgeons.
Picca, A., Berzero, G., Sanson, M., Current Therapeutic Approaches to Diffuse Grade II and III Gliomas, Therapeutic Advances in Neurological Disorders. 2018, SAGE PublicationsSage UK, London, England.
Fellah, S., Caudal, D., De Paula, A.M., Dory-Lautrec, P., Figarella-Branger, D., Chinot, O., Metellus, P., Cozzone, P.J., Confort-Gouny, S., Ghattas, B., Callot, V., Girard, N., Multimodal MR imaging (Diffusion, perfusion, and spectroscopy): is it possible to distinguish oligodendroglial tumor grade and 1p/19q codeletion in the pretherapeutic diagnosis?. Am. J. Neuroradiol., 2013, 1326–1333.
Jansen, N.L., Schwartz, C., Graute, V., Eigenbrod, S., Lutz, J., Egensperger, R., Pöpperl, G., Kretzschmar, H.A., Cumming, P., Bartenstein, P., Tonn, J.-C., Kreth, F.-W., la Fougère, C., Thon, N., Prediction of oligodendroglial histology and LOH 1p/19q using dynamic [(18)F]FET-PET imaging in intracranial WHO grade II and III gliomas. Neurooncology, 2012, 1473–1480 Oxford University Press.
Iwadate, Y., Shinozaki, N., Matsutani, T., Uchino, Y., Saeki, N., Molecular imaging of 1p/19q deletion in oligodendroglial tumours with 11C-methionine positron emission tomography. J. Neurol. Neurosurg. Psychiatr., 2016, 1016–1021 BMJ Publishing Group.
Bourdillon, P., Hlaihel, C., Guyotat, J., Guillotton, L., Honnorat, J., Ducray, F., Cotton, F., Prediction of anaplastic transformation in low-grade oligodendrogliomas based on magnetic resonance spectroscopy and 1p/19q codeletion status. J. Neurooncol., 2015, 529–537 Springer US.
Woehrer, A., Sander, P., Haberler, C., Kern, S., Maier, H., Preusser, M., Hartmann, C., Kros, J.M., Hainfellner, J.A., FISH-based detection of 1p 19q codeletion in oligodendroglial tumors: procedures and protocols for neuropathological practice - A publication under the auspices of the Research Committee of the European Confederation of Neuropathological Societies (Euro-CNS). Clin. Neuropathol., 2011, 47–55.
Ruge, M.I., Simon, T., Suchorska, B., Lehrke, R., Hamisch, C., Koerber, F., Maarouf, M., Treuer, H., Berthold, F., Sturm, V., Voges, J., Stereotactic brachytherapy with iodine-125 seeds for the treatment of inoperable low-grade gliomas in children: long-term outcome. J. Clin. Oncol. 29:31 (2011), 4151–4159.
Aerts, H.J., Velazquez, E.R., Leijenaar, R.T., Parmar, C., Grossmann, P., Carvalho, S., Bussink, J., Monshouwer, R., Haibe-Kains, B., Rietveld, D., Hoebers, F., Rietbergen, M.M., Leemans, C.R., Dekker, A., Quackenbush, J., Gillies, R.J., Lambin, P., Decoding tumour phenotype by noninvasive imaging using a quantitative radiomics approach. Nat. Commun., 5, 2014, 4006.
Lambin, P., Leijenaar, R.T.H., Deist, T.M., Peerlings, J., de Jong, E.E.C., van Timmeren, J., Sanduleanu, S., Larue, R., Even, A.J.G., Jochems, A., van Wijk, Y., Woodruff, H., van Soest, J., Lustberg, T., Roelofs, E., van Elmpt, W., Dekker, A., Mottaghy, F.M., Wildberger, J.E., Walsh, S., Radiomics: the bridge between medical imaging and personalized medicine. Nat. Rev. Clin. Oncol. 14:12 (2017), 749–762.
Lambin, P., Rios-Velazquez, E., Leijenaar, R., Carvalho, S., van Stiphout, R.G., Granton, P., Zegers, C.M., Gillies, R., Boellard, R., Dekker, A., Aerts, H.J., Radiomics: extracting more information from medical images using advanced feature analysis. Eur. J. Cancer 48:4 (2012), 441–446.
Akkus, Z., Ali, I., Sedlář, J., Agrawal, J.P., Parney, I.F., Giannini, C., Erickson, B.J., Predicting deletion of chromosomal arms 1p/19q in low-grade gliomas from MR images using machine intelligence. J. Digit. Imaging, 2017, 469–476.
Zhang, S., Chiang, G.C.-Y., Magge, R.S., Fine, H.A., Ramakrishna, R., Chang, E.W., Pulisetty, T., Wang, Y., Zhu, W., Kovanlikaya, I., MRI based texture analysis to classify low grade gliomas into astrocytoma and 1p/19q codeleted oligodendroglioma. Magn. Reson. Imaging, 2019, 254–258.
van der Voort, S.R., Incekara, F., Wijnenga, M.M.J., Kapas, G., Gardeniers, M., Schouten, J.W., Starmans, M.P.A., Nandoe Tewarie, R., Lycklama, G.J., French, P.J., Dubbink, H.J., van den Bent, M.J., Vincent, A., Niessen, W.J., Klein, S., Smits, M., Predicting the 1p/19q codeletion status of presumed low-grade glioma with an externally validated machine learning algorithm. Clin. Cancer Res. 25:24 (2019), 7455–7462.
Kocak, B., Durmaz, E.S., Ates, E., Sel, I., Turgut Gunes, S., Kaya, O.K., Zeynalova, A., Kilickesmez, O., Radiogenomics of lower-grade gliomas: machine learning-based MRI texture analysis for predicting 1p/19q codeletion status. Eur. Radiol. 30:2 (2020), 877–886.
Kong, Z., Jiang, C., Zhang, Y., Liu, S., Liu, D., Liu, Z., Chen, W., Liu, P., Yang, T., Lyu, Y., Zhao, D., You, H., Wang, Y., Ma, W., Feng, F., Thin-slice magnetic resonance imaging-based radiomics signature predicts chromosomal 1p/19q Co-deletion status in grade II and III gliomas. Front. Neurol., 11, 2020, 551771.
Shboul, Z.A., Chen, J., M.I. K, Prediction of molecular mutations in diffuse low-grade gliomas using MR imaging features. Sci. Rep., 10(1), 2020, 3711.
Bhandari, A.P., Liong, R., Koppen, J., Murthy, S.V., Lasocki, A., Noninvasive determination of IDH and 1p19q status of lower-grade gliomas using MRI radiomics: a systematic review. AJNR Am. J. Neuroradiol. 42:1 (2021), 94–101.
Branzoli, F., Pontoizeau, C., Tchara, L., Di Stefano, A.L., Kamoun, A., Deelchand, D.K., Valabrègue, R., Lehéricy, S., Sanson, M., Ottolenghi, C., Marjańska, M., Cystathionine as a marker for 1p/19q codeleted gliomas by in vivo magnetic resonance spectroscopy. NeuroOncology, 2019, 765–774.
Ruijiang, L., Lei, X., Sandy, N., Daniel, L.R., Radiomics and Radiogenomics: Technical Basis and Clinical Applications. 2019, Chapman and Hall/CRC.
Zwanenburg, A., Leger, S., Vallières, M., Löck, S., Image biomarker standardisation initiative. arXiv, 1612, 2019 07003v11.
Erickson, B., Akkus, Z., Sedlar, J., Korfiatis, P., Data from LGG-1p19qDeletion. The Cancer Imaging Archive, 2017.
Clark, K., Vendt, B., Smith, K., Freymann, J., Kirby, J., Koppel, P., Moore, S., Phillips, S., Maffitt, D., Pringle, M., Tarbox, L., Prior, F., The cancer imaging archive (TCIA): maintaining and operating a public information repository. J. Digit. Imaging, 2013, 1045–1057.
Pedano, N., Flanders, A.E., Scarpace, L., Mikkelsen, T., Eschbacher, J.M., Hermes, B., Sisneros, V., Barnholtz-Sloan, J., Ostrom, Q., Radiology data from the Cancer genome atlas low grade glioma [TCGA-LGG] collection. The Cancer Imaging Archive, 2016.
Frank, E., Hall, M.A., Witten, I.H., The WEKA Workbench. Online Appendix for "Data Mining: Practical Machine Learning Tools and Techniques". fourth edition, 2016, Morgan Kaufmann.
Hall, M., Frank, E., Holmes, G., Pfahringer, B., Reutemann, P., Witten, I.H., The WEKA Data Mining Software, ACM SIGKDD Explorations Newsletter. 2009, 10.
Hall, M.A., Correlation-based Feature Subset Selection for Machine Learning. 1999, Hamilton, New Zealand.
Haibo, H., Yang, B., Edwardo, A.G., Shutao, L., ADASYN: adaptive synthetic sampling approach for imbalanced learning. IEEE International Joint Conference on Neural Networks (IEEE World Congress on Computational Intelligence), Hong Kong, 2008, 1322–1328.
Sanduleanu, S., Woodruff, H.C., de Jong, E.E.C., van Timmeren, J.E., Jochems, A., Dubois, L., Lambin, P., Tracking tumor biology with radiomics: a systematic review utilizing a radiomics quality score. Radiother. Oncol. 127:3 (2018), 349–360.
Moons, K.G., Altman, D.G., Reitsma, J.B., Ioannidis, J.P., Macaskill, P., Steyerberg, E.W., Vickers, A.J., Ransohoff, D.F., Collins, G.S., Transparent Reporting of a multivariable prediction model for Individual Prognosis or Diagnosis (TRIPOD): explanation and elaboration. Ann. Intern. Med. 162:1 (2015), W1–73.
Mitchell, A.J., The clinical significance of subjective memory complaints in the diagnosis of mild cognitive impairment and dementia: a meta-analysis. Int. J. Geriatr. Psychiatry 23:11 (2008), 1191–1202.
Pentzek, M., Wollny, A., Wiese, B., Jessen, F., Haller, F., Maier, W., Riedel-Heller, S.G., Angermeyer, M.C., Bickel, H., Mosch, E., Weyerer, S., Werle, J., Bachmann, C., Zimmermann, T., van den Bussche, H., Abholz, H.H., Fuchs, A., G. AgeCoDe Study, Apart from nihilism and stigma: what influences general practitioners’ accuracy in identifying incident dementia?. Am. J. Geriatr. Psychiatry 17:11 (2009), 965–975.
Goncalves, D.C., Arnold, E., Appadurai, K., Byrne, G.J., Case finding in dementia: comparative utility of three brief instruments in the memory clinic setting. Int. Psychogeriatr. 23:5 (2011), 788–796.
Mitchell, A.J., How do we know when a screening test is clinically useful?. Mitchell, A.J., James, C., (eds.) Screening for Depression in Clinical Practice: an Evidence-Based Guide, 2009, Coyne ISBN10: 0195380193 OUP.
Davies, R.R., Larner, A.J., Addenbrooke's cognitive examination (ACE) and its revision (ACE-R). Larner, A.J., (eds.) Cognitive Screening Instruments: A Practical Approach, 2013, Springer, London, London, 61–77.
Mitchell, A.J., Sensitivity x PPV is a recognized test called the clinical utility index (CUI+). Eur. J. Epidemiol. 26:3 (2011), 251–252 author reply 252.