A database of the healthy human spinal cord morphometry in the PAM50 template space
Status PubMed-not-MEDLINE Jazyk angličtina Země Spojené státy americké Médium electronic-ecollection
Typ dokumentu časopisecké články
PubMed
40800421
PubMed Central
PMC12224433
DOI
10.1162/imag_a_00075
PII: imag_a_00075
Knihovny.cz E-zdroje
- Klíčová slova
- Spinal cord, morphometric measures, normalization, normative values,
- Publikační typ
- časopisecké články MeSH
Measures of spinal cord morphometry computed from magnetic resonance images serve as relevant prognostic biomarkers for a range of spinal cord pathologies, including traumatic and non-traumatic spinal cord injury and neurodegenerative diseases. However, interpreting these imaging biomarkers is difficult due to considerable intra- and inter-subject variability. Yet, there is no clear consensus on a normalization method that would help reduce this variability and more insights into the distribution of these morphometrics are needed. In this study, we computed a database of normative values for six commonly used measures of spinal cord morphometry: cross-sectional area, anteroposterior diameter, transverse diameter, compression ratio, eccentricity, and solidity. Normative values were computed from a large open-access dataset of healthy adult volunteers (N = 203) and were brought to the common space of the PAM50 spinal cord template using a newly proposed normalization method based on linear interpolation. Compared to traditional image-based registration, the proposed normalization approach does not involve image transformations and, therefore, does not introduce distortions of spinal cord anatomy. This is a crucial consideration in preserving the integrity of the spinal cord anatomy in conditions such as spinal cord injury. This new morphometric database allows researchers to normalize based on sex and age, thereby minimizing inter-subject variability associated with demographic and biological factors. The proposed methodology is open-source and accessible through the Spinal Cord Toolbox (SCT) v6.0 and higher.
Centre de Recherche du CHU Sainte Justine Université de Montréal Montreal Canada
Department of Neurology Faculty of Medicine and Dentistry Palacký University Olomouc Olomouc Czechia
Functional Neuroimaging Unit CRIUGM Université de Montréal Montreal Canada
Mila Quebec AI Institute Montreal Canada
NeuroPoly Lab Institute of Biomedical Engineering Polytechnique Montreal Montreal Canada
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Badhiwala, J. H., Ahuja, C. S., Akbar, M. A., Witiw, C. D., Nassiri, F., Furlan, J. C., Curt, A., Wilson, J. R., & Fehlings, M. G. (2020). Degenerative cervical myelopathy—Update and future directions. Nature Reviews Neurology, 16(2), 108–124. 10.1038/s41582-019-0303-0 PubMed DOI
Bédard, S., & Cohen-Adad, J. (2022). Automatic measure and normalization of spinal cord cross-sectional area using the pontomedullary junction. Frontiers in Neuroimaging, 1(November), 43. 10.3389/fnimg.2022.1031253 PubMed DOI PMC
Bédard, S., Enamundram N. K., Tsagkas, C., Pravatà, E., Granziera, C., Smith, A., Weber, K. A., II, & Cohen-Adad, J. (2023). Towards contrast-agnostic soft segmentation of the spinal cord. ArXiv [Eess.IV]. arXiv. http://arxiv.org/abs/2310.15402 PubMed
Calabrese, E., Adil, S. M., Cofer, G., Perone, C. S., Cohen-Adad, J., Lad, S. P., & Allan Johnson, G. (2018). Postmortem diffusion MRI of the entire human spinal cord at microscopic resolution. NeuroImage: Clinical, 18(March), 963–971. 10.1016/j.nicl.2018.03.029 PubMed DOI PMC
Cohen-Adad, J., Alonso-Ortiz, E., Abramovic, M., Arneitz, C., Atcheson, N., Barlow, L., Barry, R. L., Barth, M., Battiston, M., Büchel, C., Budde, M., Callot, V., Combes, A. J. E., De Leener, B., Descoteaux, M., de Sousa, P. L., Dostál, M., Doyon, J., Dvorak, A., … Xu, J. (2021a). Generic acquisition protocol for quantitative MRI of the spinal cord. Nature Protocols, 16(10), 4611–4632. 10.1038/s41596-021-00588-0 PubMed DOI PMC
Cohen-Adad, J., Alonso-Ortiz, E., Abramovic, M., Arneitz, C., Atcheson, N., Barlow, L., Barry, R. L., Barth, M., Battiston, M., Büchel, C., Budde, M., Callot, V., Combes, A. J. E., De Leener, B., Descoteaux, M., de Sousa, P. L., Dostál, M., Doyon, J., Dvorak, A., . . Xu, J. (2021b). Open-access quantitative MRI data of the spinal cord and reproducibility across participants, sites and manufacturers. Scientific Data, 8(1), 219. 10.1038/s41597-021-00941-8 PubMed DOI PMC
McCarthy, P. (2022). FSLeyes. 10.5281/zenodo.6511596 DOI
David, G., Mohammadi, S., Martin, A. R., Cohen-Adad, J., Weiskopf, N., Thompson, A., & Freund, P. (2019). Traumatic and nontraumatic spinal cord injury: Pathological insights from neuroimaging. Nature Reviews Neurology, 15(12), 718–731. 10.1038/s41582-019-0270-5 PubMed DOI
De Leener, B., Fonov, V. S., Louis Collins, D., Callot, V., Stikov, N., & Cohen-Adad, J. (2018). PAM50: Unbiased multimodal template of the brainstem and spinal cord aligned with the ICBM152 space. NeuroImage, 165, 170–179. 10.1016/j.neuroimage.2017.10.041 PubMed DOI
De Leener, B., Lévy, S., Dupont, S. M., Fonov, V. S., Stikov, N., Louis Collins, D., Callot, V., & Cohen-Adad, J. (2017). SCT: Spinal cord toolbox, an open-source software for processing spinal cord MRI data. NeuroImage, 145, 24–43. 10.1016/j.neuroimage.2016.10.009 PubMed DOI
El Mendili, M. M., Verschueren, A., Ranjeva, J. -P., Guye, M., Attarian, S., Zaaraoui, W., & Grapperon, A. -M. (2023). Association between brain and upper cervical spinal cord atrophy assessed by MRI and disease aggressiveness in amyotrophic lateral sclerosis. Neuroradiology, 65, 1395–1403. 10.1007/s00234-023-03191-0. PubMed DOI
Engl, C., Schmidt, P., Arsic, M., Boucard, C. C., Biberacher, V., Röttinger, M., Etgen, T., Nunnemann, S., Koutsouleris, N., Reiser, M., Meisenzahl, E. M., & Mühlau, M. (2013). Brain size and white matter content of cerebrospinal tracts determine the upper cervical cord area: Evidence from structural brain MRI. Neuroradiology, 55(8), 963–970. 10.1007/s00234-013-1204-3 PubMed DOI
Frostell, A., Hakim, R., Thelin, E. P., Mattsson, P., & Svensson, M. (2016). A review of the segmental diameter of the healthy human spinal cord. Frontiers in Neurology, 7(December), 238. 10.3389/fneur.2016.00238 PubMed DOI PMC
Gorgolewski, K. J., Auer, T., Calhoun, V. D., Cameron Craddock, R., Das, S., Duff, E. P., Flandin, G., Ghosh, S. S., Glatard, T., Halchenko, Y. O., Handwerker, D. A., Hanke, M., Keator, D., Li, X., Michael, Z., Maumet, C., Nolan Nichols, B., Nichols, T. E., Pellman, J., . . Poldrack, R. A. (2016). The Brain imaging data structure, a format for organizing and describing outputs of neuroimaging experiments. Scientific Data, 3(1), 160044. 10.1038/sdata.2016.44 PubMed DOI PMC
Gros, C., De Leener, B., Badji, A., Maranzano, J., Eden, D., Dupont, S. M., Talbott, J., Zhuoquiong, R., Liu Y., Granberg, T., Ouellette, R., Tachibana, Y., Hori, M., Kamiya, K., Chougar, L., Stawiarz, L., Hillert, J., Bannier, E., Kerbrat, A., … Cohen-Adad, J. (2019). Automatic segmentation of the spinal cord and intramedullary multiple sclerosis lesions with convolutional neural networks. NeuroImage, 184(January), 901–915. 10.1016/j.neuroimage.2018.09.081 PubMed DOI PMC
Guo, S., Lin, T., Wu, R., Wang, Z., Chen, G., & Liu, W. (2022). The pre-operative duration of symptoms: The most important predictor of post-operative efficacy in patients with degenerative cervical myelopathy. Brain Sciences, 12(8), 1088. 10.3390/brainsci12081088 PubMed DOI PMC
Horáková, M., Horák, T., Valošek, J., Rohan, T., Korit’áková, E., Dostál, M., Kočica, J., Skutil, T., Keřkovský, M., Kadaňka, Z., Jr, Bednařík, P., Svátková, A., Hluštík, P., & Bednařík, J. (2022). Semi-automated detection of cervical spinal cord compression with the Spinal Cord Toolbox. Quantitative Imaging in Medicine and Surgery, 12(4), 2261–2279. 10.21037/qims-21-782 PubMed DOI PMC
Horsfield, M. A., Sala, S., Neema, M., Absinta, M., Bakshi, A., Sormani, M. P., Rocca, M. A., Bakshi, R., & Filippi, M. (2010). Rapid semi-automatic segmentation of the spinal cord from magnetic resonance images: Application in multiple sclerosis. NeuroImage, 50(2), 446–455. 10.1016/j.neuroimage.2009.12.121 PubMed DOI PMC
Kadanka, Z., Adamova, B., Kerkovsky, M., Kadanka, Z., Dusek, L., Jurova, B., Vlckova, E., & Bednarik, J. (2017). Predictors of symptomatic myelopathy in degenerative cervical spinal cord compression. Brain and Behavior, 7(9), e00797. 10.1002/brb3.797 PubMed DOI PMC
Kameyama, T., Hashizume, Y., & Sobue, G. (1996). Morphologic features of the normal human cadaveric spinal cord. Spine, 21(11), 1285–1290. 10.1097/00007632-199606010-00001 PubMed DOI
Karakuzu, A., Appelhoff, S., Auer, T., Boudreau, M., Feingold, F., Khan, A. R., Lazari, A., Markiewicz, C., Mulder, M., Phillips, C., Salo, T., Stikov, N., Whitaker, K., & de Hollander, G.. (2022). QMRI-BIDS: An extension to the brain imaging data structure for quantitative magnetic resonance imaging data. Scientific Data, 9(1), 517. 10.1038/s41597-022-01571-4 PubMed DOI PMC
Kato, F., Yukawa, Y., Suda, K., Yamagata, M., & Ueta, T. (2012). Normal morphology, age-related changes and abnormal findings of the cervical spine. Part II: Magnetic resonance imaging of over 1,200 asymptomatic subjects. European Spine Journal, 21, 1499–1507 . https://link.springer.com/article/10.1007/s00586-012-2176-4. 10.1007/s00586-012-2176-4 PubMed DOI PMC
Keřkovský, M., Bednařík, J., Jurová, B., Dušek, L., Kadaňka, Z., Kadaňka, Z., Němec, M., Kovaľová, I., Šprláková-Puková, A., & Mechl, M. (2017). Spinal cord MR diffusion properties in patients with degenerative cervical cord compression. Journal of Neuroimaging: Official Journal of the American Society of Neuroimaging, 27(1), 149–157. 10.1111/jon.12372 PubMed DOI
Kesenheimer, E. M., Wendebourg, M. J., Weigel, M., Weidensteiner, C., Haas, T., Richter, L., Sander, L., Horvath, A., Barakovic, M., Cattin, P., Granziera, C., Bieri, O., & Schlaeger, R. (2021). Normalization of spinal cord total cross-sectional and gray matter areas as quantified with radially sampled averaged magnetization inversion recovery acquisitions. Frontiers in Neurology 12, 637198. 10.3389/fneur.2021.637198. PubMed DOI PMC
Kim, G., Khalid, F., Oommen, V. V., Tauhid, S., Chu, R., Horsfield, M. A., Healy, B. C., & Bakshi, R. (2015). T1- vs. T2-based MRI measures of spinal cord volume in healthy subjects and patients with multiple sclerosis. BMC Neurology 15(July), 124. 10.1186/s12883-015-0387-0 PubMed DOI PMC
Ko, H.-Y., Park, J. H., Shin, Y. B., & Baek, S. Y. (2004). Gross quantitative measurements of spinal cord segments in human. Spinal Cord, 42(1), 35–40. 10.1038/sj.sc.3101538 PubMed DOI
Kovalova, I., Kerkovsky, M., Kadanka, Z., Kadanka, Z., Nemec, M., Jurova, B., Dusek, L., Jarkovsky, J., & Bednarik, J. (2016). Prevalence and imaging characteristics of nonmyelopathic and myelopathic spondylotic cervical cord compression. Spine, 41(24), 1908–1916. 10.1097/brs.0000000000001842 PubMed DOI
Losseff, N. A., Webb, S. L., O’Riordan, J. I., Page, R., Wang, L., Barker, G. J., Tofts, P. S., McDonald, W. I., Miller, D. H., & Thompson, A. J. (1996). Spinal cord atrophy and disability in multiple sclerosis. A new reproducible and sensitive MRI method with potential to monitor disease progression. Brain: A Journal of Neurology, 119( Pt 3) (June), 701–708. 10.1093/brain/119.3.701 PubMed DOI
Martin, A. R., De Leener, B., Cohen-Adad, J., Cadotte, D. W., Kalsi-Ryan, S., Lange, S. F., Tetreault, L., Nouri, A., Crawley, A., Mikulis, D. J., Ginsberg, H., & Fehlings, M. G. (2017a). A novel MRI biomarker of spinal cord white matter injury: T2*-weighted white matter to gray matter signal intensity ratio. AJNR. American Journal of Neuroradiology, 38(6), 1266–1273. 10.3174/ajnr.a5162 PubMed DOI PMC
Martin, A. R., De Leener, B., Cohen-Adad, J., Cadotte, D. W., Kalsi-Ryan, S., Lange, S. F., Tetreault, L., Nouri, A., Crawley, A., Mikulis, D. J., Ginsberg, H., & Fehlings, M. G. (2017b). Clinically feasible microstructural MRI to quantify cervical spinal cord tissue injury using DTI, MT, and T2*-weighted imaging: Assessment of normative data and reliability. AJNR. American Journal of Neuroradiology, 38(6), 1257–1265. 10.3174/ajnr.a5163 PubMed DOI PMC
Mina, Y., Azodi, S., Dubuche, T., Andrada, F., Osuorah, I., Ohayon, J., Cortese, I., Wu, T., Johnson, K. R., Reich, D. S., Nair, G., & Jacobson, S. (2021). Cervical and thoracic cord atrophy in multiple sclerosis phenotypes: Quantification and correlation with clinical disability. NeuroImage Clinical, 30(January), 102680. 10.1016/j.nicl.2021.102680 PubMed DOI PMC
Miyanji, F., Furlan, J. C., Aarabi, B., Arnold, P. M., & Fehlings, M. G. (2007). Acute cervical traumatic spinal cord injury: MR imaging findings correlated with neurologic outcome—Prospective study with 100 consecutive patients. Radiology, 243(3), 820–827. 10.1148/radiol.2433060583 PubMed DOI
Oh, J., Seigo, M., Saidha, S., Sotirchos, E., Zackowski, K., Chen, M., Prince, J., Diener-West, M., Calabresi, P. A., & Reich, D. S. (2014). Spinal cord normalization in multiple sclerosis. Journal of Neuroimaging: Official Journal of the American Society of Neuroimaging, 24(6), 577–584. 10.1111/jon.12097 PubMed DOI PMC
Papinutto, N., Asteggiano, C., Bischof, A., Gundel, T. J., Caverzasi, E., Stern, W. A., Bastianello, S., Hauser, S. L., & Henry, R. G. (2020). Intersubject variability and normalization strategies for spinal cord total cross-sectional and gray matter areas. Journal of Neuroimaging: Official Journal of the American Society of Neuroimaging, 30(1), 110–18. 10.1111/jon.12666 PubMed DOI PMC
Papinutto, N., Schlaeger, R., Panara, V., Zhu, A. H., Caverzasi, E., Stern, W. A., Hauser, S. L., & Henry, R. G. (2015). Age, Gender and normalization covariates for spinal cord gray matter and total cross-sectional areas at cervical and thoracic levels: A 2D phase sensitive inversion recovery imaging study. PloS One, 10(3), e0118576. 10.1371/journal.pone.0118576 PubMed DOI PMC
Paquin, M. E., El Mendili, M. M., Gros, C., Dupont, S. M., Cohen-Adad, J., & Pradat, P. F. (2018). Spinal cord gray matter atrophy in amyotrophic lateral sclerosis. AJNR. American Journal of Neuroradiology, 39(1), 184–192. 10.3174/ajnr.a5427 PubMed DOI PMC
Rashid, W., Davies, G. R., Chard, D. T., Griffin, C. M., Altmann, D. R., Gordon, R., Kapoor, R., Thompson, A. J., & Miller, D. H. (2006). Upper cervical cord area in early relapsing-remitting multiple sclerosis: Cross-sectional study of factors influencing cord size. Journal of Magnetic Resonance Imaging: JMRI, 23(4), 473–476. 10.1002/jmri.20545 PubMed DOI
Rocca, M. A., Valsasina, P., Meani, A., Gobbi, C., Zecca, C., Rovira, A., Montalban, X., Kearney, H., Ciccarelli, O., Matthews, L., Palace, J., Gallo, A., Bisecco, A., Gass, A., Eisele, P., Lukas, C., Bellenberg, B., Barkhof, F., Vrenken, H., … MAGNIMS Study Group. (2019). Clinically relevant cranio-caudal patterns of cervical cord atrophy evolution in MS. Neurology, 93(20), E1852–E1866. 10.1212/wnl.0000000000008466 PubMed DOI
Smith, S. S., Stewart, M. E., Davies, B. M., & Kotter, M. R. N. (2021). The prevalence of asymptomatic and symptomatic spinal cord compression on magnetic resonance imaging: A systematic review and meta-analysis. Global Spine Journal, 11(4), 597–607. 10.1177/2192568220934496 PubMed DOI PMC
Solstrand Dahlberg, L., Viessmann, O., & Linnman, C. (2020). Heritability of cervical spinal cord structure. Neurology Genetics, 6(2), e401. 10.1212/nxg.0000000000000401 PubMed DOI PMC
Standring, S. (2020). Gray’s anatomy: The anatomical basis of clinical practice. Elsevier. 10.1302/0301-620x.91b7.22719 DOI
Taso, M., Girard, O. M., Duhamel, G., Le Troter, A., Feiweier, T., Guye, M., Ranjeva, J. P., & Callot, V. (2016). Tract-specific and age-related variations of the spinal cord microstructure: A multi-parametric MRI study using diffusion tensor imaging (DTI) and inhomogeneous magnetization transfer (IhMT). NMR in Biomedicine, 29(6), 817–832. 10.1002/nbm.3530 PubMed DOI
Ullmann, E., Paquette, J. F. P., Thong, W. E., & Cohen-Adad, J. (2014). Automatic labeling of vertebral levels using a robust template-based approach. International Journal of Biomedical Imaging, 2014, 719520. 10.1155/2014/719520 PubMed DOI PMC
Virtanen, P., Gommers, R., Oliphant, T. E., Haberland, M., Reddy, T., Cournapeau, D., Burovski, E., Peterson, P., Weckesser, W., Bright, J., van der Walt, S. J., Brett, M., Wilson, J., Jarrod Millman, K., Mayorov, N., Nelson, A. R. J., Jones, E., Kern, R., Larson, E., … SciPy 1.0 Contributors. (2020). SciPy 1.0: Fundamental algorithms for scientific computing in Python. Nature Methods, 17(3), 261–272. 10.1038/s41592-020-0772-5 PubMed DOI PMC
Weeda, M. M., Middelkoop, S. M., Steenwijk, M. D., Daams, M., Amiri, H, Brouwer, I., Killestein, J., Uitdehaag, B. M. J., Dekker, I., Lukas, C., Bellenberg, B., Barkhof, F., Pouwels, P.J. W., & Vrenken, H. (2019). Validation of mean upper cervical cord area (MUCCA) measurement techniques in multiple sclerosis (MS): High reproducibility and robustness to lesions, but large software and scanner effects. NeuroImage: Clinical, 24(January), 101962. 10.1016/j.nicl.2019.101962 PubMed DOI PMC
Yanase, M., Matsuyama, Y., Hirose, K., Takagi, H., Yamada, M., Iwata, H., & Ishiguro, N. (2006). Measurement of the cervical spinal cord volume on MRI. Journal of Spinal Disorders & Techniques, 19(2), 125–29. 10.1097/01.bsd.0000181294.67212.79 PubMed DOI
Monitoring morphometric drift in lifelong learning segmentation of the spinal cord