diff --git a/neurolibre.00017/10.55458.neurolibre.00017.crossref.xml b/neurolibre.00017/10.55458.neurolibre.00017.crossref.xml new file mode 100644 index 0000000..2d09b47 --- /dev/null +++ b/neurolibre.00017/10.55458.neurolibre.00017.crossref.xml @@ -0,0 +1,798 @@ + + + + 20231017T020133-596d59d1c31ee620c4110b12aa008e1820fac3c8 + 20231017020133 + + NeuroLibre Admin + admin@neurolibre.org + + Centre de Recherche de l'Institut Universitaire de Geriatrie de Montreal + + + + NeuroLibre Reproducible Preprints + + + Jan + Valošek + https://orcid.org/0000-0002-7398-4990 + + + Sandrine + Bédard + https://orcid.org/0000-0001-9859-1133 + + + Miloš + Keřkovský + https://orcid.org/0000-0003-0587-9897 + + + Tomáš + Rohan + https://orcid.org/0000-0002-7105-583X + + + Julien + Cohen-Adad + https://orcid.org/0000-0003-3662-9532 + + + + A database of the healthy human spinal cord morphometry +in the PAM50 template space + + + 10 + 17 + 2023 + + + http://creativecommons.org/licenses/by/4.0/ + http://creativecommons.org/licenses/by/4.0/ + http://creativecommons.org/licenses/by/4.0/ + + + + Repository archive + 10.5281/zenodo.10002178 + + + Dataset archive + 10.5281/zenodo.10002180 + + + Book archive + 10.5281/zenodo.10002176 + + + Container archive + 10.5281/zenodo.10002182 + + + GitHub technical screening + https://github.com/neurolibre/neurolibre-reviews/issues/17 + + + Executable preprint + https://preprint.neurolibre.org/10.55458/neurolibre.00017 + + + + 10.55458/neurolibre.00017 + https://neurolibre.org/papers/10.55458/neurolibre.00017 + + + https://preprint.neurolibre.org/10.55458/neurolibre.00017.pdf + + + + + + Spinal cord normalization in multiple +sclerosis + Oh + J. 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OSF Preprints. +https://doi.org/10.31219/osf.io/h89js + + + Beyond advertising: New infrastructures for +publishing integrated research objects + DuPre + PLOS Computational Biology + 1 + 18 + 10.1371/journal.pcbi.1009651 + 2022 + DuPre, E., Holdgraf, C., Karakuzu, +A., Tetrel, L., Bellec, P., Stikov, N., & Poline, J.-B. (2022). +Beyond advertising: New infrastructures for publishing integrated +research objects. PLOS Computational Biology, 18(1), e1009651. +https://doi.org/10.1371/journal.pcbi.1009651 + + + The Canadian Open Neuroscience Platform—An +open science framework for the neuroscience community + Harding + PLOS Computational Biology + 7 + 19 + 10.1371/journal.pcbi.1011230 + 2023 + Harding, R. J., Bermudez, P., +Bernier, A., Beauvais, M., Bellec, P., Hill, S., Karakuzu, A., Knoppers, +B. M., Pavlidis, P., Poline, J.-B., Roskams, J., Stikov, N., Stone, J., +Strother, S., Consortium, C., & Evans, A. C. (2023). The Canadian +Open Neuroscience Platform—An open science framework for the +neuroscience community. PLOS Computational Biology, 19(7), 1–14. +https://doi.org/10.1371/journal.pcbi.1011230 + + + + + diff --git a/neurolibre.00017/10.55458.neurolibre.00017.jats b/neurolibre.00017/10.55458.neurolibre.00017.jats new file mode 100644 index 0000000..bd84973 --- /dev/null +++ b/neurolibre.00017/10.55458.neurolibre.00017.jats @@ -0,0 +1,2011 @@ + + +
+ + + + +NeuroLibre Reproducible Preprints +NeuroLibre + +0000-0000 + +NeuroLibre + + + +17 +10.55458/neurolibre.00017 + +A database of the healthy human spinal cord morphometry +in the PAM50 template space + + + +https://orcid.org/0000-0002-7398-4990 + +Valošek +Jan + + + + + + + +https://orcid.org/0000-0001-9859-1133 + +Bédard +Sandrine + + + + +https://orcid.org/0000-0003-0587-9897 + +Keřkovský +Miloš + + + + +https://orcid.org/0000-0002-7105-583X + +Rohan +Tomáš + + + + +https://orcid.org/0000-0003-3662-9532 + +Cohen-Adad +Julien + + + + + + + + +NeuroPoly Lab, Institute of Biomedical Engineering, +Polytechnique Montreal, Montreal, QC, Canada + + + + +Mila - Quebec AI Institute, Montreal, QC, +Canada + + + + +Department of Neurosurgery, Faculty of Medicine and +Dentistry, Palacký University Olomouc, Olomouc, Czechia + + + + +Department of Neurology, Faculty of Medicine and Dentistry, +Palacký University Olomouc, Olomouc, Czechia + + + + +Department of Radiology and Nuclear Medicine, University +Hospital Brno and Masaryk University, Brno, Czechia + + + + +Functional Neuroimaging Unit, CRIUGM, Université de +Montréal, Montreal, QC, Canada + + + + +Centre de recherche du CHU Sainte-Justine, Université de +Montréal, Montreal, QC, Canada + + + + +16 +8 +2023 + +3 +34 +17 + +Authors of papers retain copyright and release the +work under a Creative Commons Attribution 4.0 International License (CC +BY 4.0) +2022 +The article authors + +Authors of papers retain copyright and release the work under +a Creative Commons Attribution 4.0 International License (CC BY +4.0) + + + +spinal cord +morphometric measures +normative values +open-source + + + + + + Summary +

Spinal cord morphometry measures derived from magnetic resonance + imaging (MRI) scans serve as valuable prognostic biomarkers for + various spinal cord pathologies. Despite their significance, + interpreting these biomarkers is challenging due to substantial + variability between subjects. The lack of a standardized normalization + method to mitigate this variability and the need for a better + understanding of morphometric distribution contribute to the current + knowledge gap.

+

In this work, we present a database of healthy normative values for + six commonly used measures of spinal cord morphometry built using a + new fully-automatic normalization approach. Morphometric measures were + computed from a large open-access dataset of healthy adult volunteers + (N = 203) and brought to the common space of the PAM50 spinal cord + template using a newly proposed normalization method based on linear + interpolation + [fig:figure1].

+

The database is interactive, available online + (https://preprint.neurolibre.org/10.55458/neurolibre.00017) + and allows filtering for sex, age, and MRI vendors. The proposed + method is open-source and easily accessible through the Spinal Cord + Toolbox (SCT) v6.0 and higher.

+

This new morphometric database allows researchers to normalize + morphometrics based on sex and age, thereby minimizing inter-subject + variability associated with demographic and biological factors.

+
+ + Figures + +

Schematic representation of the normalization approach. + (A) T2-weighted images of 203 participants from the spine-generic + dataset (multi-subject) were used. The spinal cord was segmented, + and vertebral levels were identified automatically using the Spinal + Cord Toolbox (SCT). (B) Six morphometric measures were computed for + each axial slice from the single-subject segmentation masks. (C) For + each vertebral level, the number of slices in the subject native + space and the corresponding vertebral level in the PAM50 template + (D) were identified. Then, the morphometric measures were linearly + interpolated to the PAM50 space using the number of slices in the + PAM50 template and the subject native space for each vertebral + level.

+ +
+
+ + Acknowledgements +

We thank Nick Guenther and Mathieu Guay-Paquet for their assistance + with dataset management, Joshua Newton for his help with implementing + the algorithm in SCT, and Allan R. Martin for his insightful + discussions on the clinical aspects of the work. We also thank Nathan + Molinier for providing valuable feedback on the manuscript figures. We + acknowledge all participants as well as collaborators of the + spine-generic study + (https://spine-generic.readthedocs.io).

+

Funded by the Canada Research Chair in Quantitative Magnetic + Resonance Imaging [CRC-2020-00179], the Canadian Institute of Health + Research [PJT-190258], the Canada Foundation for Innovation [32454, + 34824], the Fonds de Recherche du Québec - Santé [322736], the Natural + Sciences and Engineering Research Council of Canada + [RGPIN-2019-07244], the Canada First Research Excellence Fund (IVADO + and TransMedTech), the Courtois NeuroMod project, the Quebec + BioImaging Network [5886, 35450], INSPIRED (Spinal Research, UK; Wings + for Life, Austria; Craig H. Neilsen Foundation, USA), Mila - Tech + Transfer Funding Program. Supported by the Ministry of Health of the + Czech Republic, grant nr. NU22-04-00024. All rights reserved. JV has + received funding from the European Union’s Horizon Europe research and + innovation programme under the Marie Sktodowska-Curie grant agreement + No 101107932.

+

+ +

NOTE: The following section in this + document repeats the narrative content exactly as found in the + corresponding + NeuroLibre Reproducible Preprint (NRP). The content was + automatically incorporated into this PDF using the NeuroLibre + publication workflow + (Karakuzu, + DuPre, et al., 2022) to credit the referenced resources. The + submitting author of the preprint has verified and approved the + inclusion of this section through a GitHub pull request made to the + source + repository from which this document was built. Please + note that the figures and tables have been excluded from this + (static) document. To interactively explore such outputs and + re-generate them, please visit the corresponding + NRP. + For more information on integrated research objects (e.g., NRPs) + that bundle narrative and executable content for reproducible and + transparent publications, please refer to DuPre et al. + (2022). + NeuroLibre is sponsored by the Canadian Open Neuroscience Platform + (CONP) + (Harding + et al., 2023).

+
+
+ + 1. INTRODUCTION + + 1.1 Spinal cord morphometry measures +

The spinal cord plays a vital role in the central nervous system + by transmitting sensory and motor signals between the brain and the + rest of the body. It also contains essential networks responsible + for functions such as locomotion and pain processing. Structural + magnetic resonance imaging (MRI) is commonly used to assess spinal + cord macrostructure and to compute measures of spinal cord + morphometry like cross-sectional area (CSA) or anteroposterior (AP) + diameter. The morphometric measures serve as objective indicators to + evaluate spinal cord pathologies, such as the extent of spinal cord + atrophy in multiple sclerosis + (Losseff + et al., 1996; + Mina + et al., 2021; + Rocca + et al., 2019) and amyotrophic lateral sclerosis + (El + Mendili et al., 2023; + Paquin + et al., 2018) or the severity of spinal cord injury and + spinal cord compression in traumatic and non-traumatic spinal cord + injury, respectively + (Badhiwala + et al., 2020; + David + et al., 2019; + Miyanji + et al., 2007).

+

However, interpreting morphometric measures is challenging due to + considerable inter-subject variability associated with demographic + and biological factors. For example, significantly smaller CSA is + consistently reported in females relative to males + (Bédard + & Cohen-Adad, 2022; + Engl + et al., 2013; + Mina + et al., 2021; + Papinutto + et al., 2015, + 2020; + Rashid + et al., 2006; + Solstrand + Dahlberg et al., 2020; + Yanase + et al., 2006). Similarly, studies showed an association of + spinal cord CSA with cervical cord length + (Martin + et al., 2017a, + 2017b; + Oh + et al., 2014), spinal canal area, and spinal canal diameters + (Kesenheimer + et al., 2021; + Papinutto + et al., 2020). Other factors, such as brain volume, + intracranial volume, and thalamic volume also showed a strong + correlation with spinal cord CSA + (Bédard + & Cohen-Adad, 2022; + Papinutto + et al., 2020; + Rashid + et al., 2006; + Solstrand + Dahlberg et al., 2020).

+

As for weight and height, studies showed only a moderate + correlation with spinal cord CSA + (Papinutto + et al., 2020; + Yanase + et al., 2006) or did not show any significant association + (Bédard + & Cohen-Adad, 2022; + Papinutto + et al., 2020; + Solstrand + Dahlberg et al., 2020). Likewise, only a weak non-significant + association was reported between spinal cord CSA and age + (Bédard + & Cohen-Adad, 2022; + Kato + et al., 2012; + Papinutto + et al., 2020; + Yanase + et al., 2006). A single study with a wide cohort age range + reported that CSA increases until about 45 years of age and then + begins to decrease + (Papinutto + et al., 2020).

+

In addition to inter-subject variability, spinal cord anatomy + varies depending on the level. Corresponding with anatomical + textbooks + (Standring, + 2020), studies have shown an increase in CSA around vertebral + levels C4-C5 corresponding to cervical enlargement + (De + Leener et al., 2018; + Frostell + et al., 2016; + Horáková + et al., 2022; + Martin + et al., 2017b; + Mina + et al., 2021; + Rocca + et al., 2019). Then, the spinal cord cross-section becomes + smaller, which is mirrored by the decrease in CSA.

+
+ + 1.2 Normalization strategies +

Various normalization strategies have been proposed to account + for the above-mentioned factors on spinal cord morphometric + measures. Sex was used for CSA normalization in several works + (Bédard + & Cohen-Adad, 2022; + Kesenheimer + et al., 2021; + Papinutto + et al., 2020; + Rashid + et al., 2006). Other studies proposed spinal cord length as a + normalization factor + (El + Mendili et al., 2023; + Martin + et al., 2017a, + 2017b; + Oh + et al., 2014; + Rocca + et al., 2019). Additionally, combining spinal cord length + with a z-score normalization was proposed to account for variations + along the superior-inferior axis + (Martin + et al., 2017a, + 2017b). + Another approach taking into account the dependency of spinal cord + anatomy on a level involved the normalization of morphometric + measures from the compression site using non-compressed levels above + and below + (Guo + et al., 2022; + Miyanji + et al., 2007). Finally, several studies normalized CSA using + the spinal canal and brain metrics, including spinal canal area, + spinal canal diameter, brain volume, intracranial volume, thalamic + volume, and head size normalization factor + (Bédard + & Cohen-Adad, 2022; + Horsfield + et al., 2010; + Kesenheimer + et al., 2021; + Papinutto + et al., 2020; + Rashid + et al., 2006; + Rocca + et al., 2019).

+

While normalization strategies showed promising outcomes, there + is currently no accepted consensus on which method to use + (Cohen-Adad + et al., 2021a; + Papinutto + et al., 2020), and their practical implementation may + encounter several challenges. First, measuring the spinal cord + length and the spinal canal area can be time-consuming due to the + absence of reliable automatic measurement techniques. Second, + obtaining brain MRI scans, necessary for assessing brain and + thalamic volumes, may not be routinely available in spinal cord MRI + protocols, and neurodegenerative diseases such as multiple sclerosis + can influence brain measurements and potentially introduce bias + during normalization.

+
+ + 1.3 Spinal cord template +

Similarly to brain studies, spinal cord studies involving + multiple subjects frequently rely on templates — standardized, + high-resolution images of the human spinal cord used as a reference + for comparing and analyzing individual spinal cord scans. A commonly + used spinal cord template is the PAM50 + (De + Leener et al., 2018). The process of aligning individual + single-subject images to the template typically involves a series of + non-linear image transformations, which may introduce inaccuracies + when computing morphometric measures in the PAM50 vs. in the native + subject’s space. This is an important consideration, especially in + subjects with altered spinal cord anatomy, such as patients with + spinal cord injury.

+
+ + 1.4 Normative values +

Several multi-subject studies have provided normative values for + spinal cord morphometry + (De + Leener et al., 2018; + Frostell + et al., 2016; + Horáková + et al., 2022; + Kato + et al., 2012; + Taso + et al., 2016). However, these studies show inconsistency in + their reporting. Some authors only provided values for + intervertebral discs + (De + Leener et al., 2018; + Horáková + et al., 2022), while others presented values averaged across + multiple vertebral levels + (Taso + et al., 2016). Notably, none of these studies have presented + normative values separated by sex.

+
+ + 1.5 Study Objective +

In this study, we present a database of healthy normative values + for six commonly used measures of spinal cord morphometry built + using a new fully-automatic normalization approach. The database is + interactive, available + online + and allows filtering by sex, age, and MRI vendors. The proposed + methodology is open-source, easily accessible through the Spinal + Cord Toolbox (SCT) + (De + Leener et al., 2017), and can be used in future multi-subject + studies to minimize inter- and intra-subject variability.

+
+
+ + 2. MATERIALS AND METHODS + + 2.1 Participants +

We used data from the spine-generic + multi-subject dataset + (Cohen-Adad + et al., 2021b). The dataset is open-access, organized + according to the Brain Imaging Data Structure (BIDS) standard + (Gorgolewski + et al., 2016; + Karakuzu, + Appelhoff, et al., 2022) and managed using + git-annex + in + this + GitHub repository.

+

Participants were scanned across 43 centers on 3T MRI scanners + from 3 vendors (GE, Philips and Siemens) using the consensus + spine-generic acquisition protocol + (Cohen-Adad + et al., 2021a). For details on sequence parameters, see + Cohen-Adad et al. + (2021a); + Cohen-Adad et al. + (2021b).

+

Two experienced radiologists (MK, TR) evaluated MRI scans with a + focus on the presence of spinal cord compression. Spinal cord + compression was defined as a change in spinal cord contour at the + level of an intervertebral disc on an axial or sagittal MRI plane + compared with that at the midpoint level of neighbouring vertebrae + (Kadanka + et al., 2017; + Keřkovský + et al., 2017). Minor abnormalities such as mild disc + protrusions, spine misalignment or minimal widening of the spinal + cord central canal were not considered significant pathologies.

+

Qualitative assessment of the spine-generic + dataset by two experienced radiologists revealed mostly mild spinal + cord compression in 64 out of the total 267 volunteers (see the + “pathology” column in + this + spreadsheet). Those volunteers were excluded from the + further analysis. The final cohort used for the normative database + construction consisted of 203 healthy subjects (105 males and 98 + females). Detailed demographic characteristics are provided in Table + 1.

+
+ + 2.2 Data pre-processing +

We used the T2-weighted images (0.8 mm isotropic resolution) + covering at least C1 to T1 vertebral levels. The image processing + was performed automatically using SCT v6.0 + (De + Leener et al., 2017). For each participant, the spinal cord + was segmented using a deep learning-based algorithm + (Gros + et al., 2019) and the intervertebral discs were labeled + (Ullmann + et al., 2014) to generate the cord segmentation labeled with + vertebral levels (Figure 1A).

+

The spinal cord segmentation and disc labels were visually + inspected using SCT’s quality control report + (sct_qc function) and manually corrected when + necessary. The manual corrections ensured that the spinal cord + segmentation masks used for the computation of morphometric measures + were reliable. Segmentation masks were corrected using FSLeyes image + viewer + (McCarthy, + 2022) by adding or removing voxels when appropriate. + Regarding vertebral labeling corrections, we manually identified the + posterior tip of the intervertebral discs using SCT’s + sct_label_utils function when it was + necessary.

+
+ + 2.3 Normalization +

Figure 1 shows a schematic representation of the fully-automatic + normalization approach based on linear interpolation of morphometric + measures from the subject’s native space to the anatomical + dimensions of the PAM50 spinal cord template + (De + Leener et al., 2018).

+

After the preprocessing (i.e., spinal cord segmentation and + labeling), the morphometric measures were computed across individual + axial slices from the spinal cord segmentation mask in the subject’s + native space. Then, the number of axial slices corresponding to each + vertebral level was identified in both the subject’s native space + and in the PAM50 template based on the labeled segmentation. + Finally, the computed morphometric measures were linearly + interpolated to the PAM50 anatomical dimensions based on the number + of slices for each vertebral level in the native space and the PAM50 + template. The following morphometric measures were computed using + SCT’s sct_process_segmentation for each + participant: cross-sectional area (CSA), anteroposterior (AP) + diameter, transverse diameter, compression ratio, eccentricity, and + solidity.

+

Spinal cord CSA reflects the atrophy of the spinal cord and is + computed as the area of the spinal cord in the transverse plane. The + AP diameter is the measurement of the diameter of the spinal cord in + the anterior-posterior direction, while the transverse diameter is + the measurement of the diameter of the spinal cord from side to + side. The compression ratio reflects the flattening of the spinal + cord and is defined as the ratio of the AP diameter and the + transverse diameter. Eccentricity is defined as the ratio of the + focal distance over the major axis length of an ellipse with the + same second moments as the spinal cord. The value is in the interval + [0, 1]. When it is 0, the ellipse becomes a + circle. Solidity is used to measure the indentation of the spinal + cord and is defined as the ratio of the area representing the spinal + cord to the area of the smallest convex polygon surrounding all + positive pixels in the image. Solidity is relevant in detecting + non-convex shapes, for instance, in subjects with spinal cord + compression.

+
+ + 2.4 Normative values and interactive database +

Morphometric measures normalized to the PAM50 space were used for + the calculation of normative values of the spinal cord morphometry. + The normative values were calculated as mean and standard deviation + across participants for slices in PAM50 space corresponding to each + intervertebral disc and the middle of each vertebral level. The + normative values are provided for the whole cohort and separated by + sex. For convenient introspection of the morphometric measures, + interactive figures were created using the + Plotly + Python library v5.9.0. The figures allow + interactive visualization of normative values for any slice in the + PAM50 space and filtering for sex, age decades, and MRI vendors. The + figures show values per slice (instead of per vertebral level), to + prevent the loss of information that would arise if values were + averaged within each vertebral level.

+
+ + 2.5 Statistical analysis +

Statistical analysis was conducted using the SciPy Python library + v1.10.1 + (Virtanen + et al., 2020). Descriptive statistics, including mean and + standard deviation, were computed for age, height, and weight. The + Shapiro-Wilk normality test was used to assess data normality. + Differences between males and females in age, height, and weight + were examined using the Wilcoxon rank-sum test. Morphometric + measures in PAM50 space were averaged across participants for each + slice and compared between sex and MRI vendors using the Wilcoxon + rank-sum test. The significance level was set to + alpha = 0.001.

+

The inter-subject coefficient of variation (COV), defined as the + ratio of standard deviation and mean, was computed per slice for all + morphometrics measures. The COV was then averaged for individual + vertebral levels. Additionally, the mean COV for the whole cervical + spinal cord was computed as average across all slices.

+
+
+ + 4. DISCUSSION +

This study introduced a framework to automatically normalize spinal + cord morphometric measures and computed normative metrics from a + public database of healthy adults. Normative values were reported in + the PAM50 template reference space, which facilitates the comparison + of results across past and future studies. Metrics were presented as + interactive figures, allowing readers to conveniently explore + morphometric values and filter them according to sex, MRI vendor, and + age.

+ + 4.1 Participants +

Assessment of the spine-generic MRI scans by two + experienced radiologists revealed mild spinal cord compression in + 24% of volunteers. This finding aligns with previous studies that + have reported the prevalence of asymptomatic spinal cord compression + in up to 40% of the otherwise healthy population + (Kovalova + et al., 2016; + Smith + et al., 2021). Given our objective of constructing a database + containing healthy normative morphometric values to minimize + variability in future research, we excluded the subjects with mild + compression to mitigate potential bias.

+
+ + 4.2 Normalization to PAM50 anatomical dimensions +

The proposed normalization approach is performed per slice + (instead of per vertebral level), providing a more exhaustive + picture of cord morphometry along the superior-inferior axis. + Moreover, precise quantification of cord morphometry along the + superior-inferior axis could be relevant. For example, in the case + of compression spanning only a few mm of cord tissue, it would be + desirable to know the cord morphometry on the healthy population at + the equivalent spinal cord location (ie: not the entire vertebrae, + but a smaller section).

+

Compared to classical image-based registration, our normalization + approach does not introduce geometrical image distortions, which may + result in inaccuracies when computing morphometric measures. + Traditional registration to the PAM50 template involves spinal cord + straightening, vertebral alignment between the image and the + template, and iterative slice-wise non-linear registration + (De + Leener et al., 2017). Each of these steps might change the + spinal cord shape and contour (see a relevant + issue + on GitHub).

+
+ + 4.3 Interactive figures and Normative database +

Unlike previous studies + (De + Leener et al., 2018; + Horáková + et al., 2022; + Kato + et al., 2012; + Taso + et al., 2016) that presented normative values using “static” + tables, our paper features interactive figures for a more exhaustive + and convenient exploration of morphometric results.

+

Furthermore, previous studies, such as those conducted by + (De + Leener et al., 2018; + Kato + et al., 2012; + Taso + et al., 2016), only provided normative values for CSA and AP + diameter. Only one recent study + (Horáková + et al., 2022) also featured transverse diameter, compression + ratio, solidity, and torsion. Results presented in this study + feature morphometric values for all six metrics simultaneously, + offering a convenient way to explore the relationship between + individual morphometric measures. This could be particularly useful + for assessing changes in spinal anatomy between levels or for + identifying levels of spinal cord compression. Additionally, + researchers have the option to show or hide traces by clicking on + their corresponding legend items, allowing for easy exploration of + trends related to sex, age decades, and MRI vendors.

+

The proposed open-source database of normative values in the + PAM50 space allows researchers to filter subjects based on + demographic and biological factors. Researchers can thus match sex, + age, and MRI vendor with their study population and use our database + for normalization of their cohort relative to the healthy population + with respect to these factors. This is a relevant feature since + normalization per sex is the most commonly used normalization factor + for spinal cord morphometric measures + (Bédard + & Cohen-Adad, 2022; + Kesenheimer + et al., 2021; + Mina + et al., 2021; + Papinutto + et al., 2020; + Rashid + et al., 2006; + Rocca + et al., 2019).

+
+ + 4.4 Morphometric measures +

The CSA values obtained in this study for individual + intervertebral discs are in line with CSA measured in 50 healthy + subjects + (De + Leener et al., 2018). For instance, we measured a CSA of + 76.61 ± 8.35 mm2 (mean ± standard deviation) for the C3-C4 + intervertebral disc, while De Leener et al. + (2018) + obtained 77.46 ± 8.45 mm2 for the same intervertebral disc. In + contrast, other studies reported either smaller or larger CSA for + the same C3-C4 intervertebral disc. For example, Horáková et al. + (2022) + obtained a CSA of 71.7 ± 8.2 mm2, while Kesenheimer et al. + (2021) + measured a CSA of 87.4 ± 8.31 mm2. This can be attributed to various + factors, including differences in MRI contrast, variations in + population ages, and variations in the segmentation methods + used.

+

Another study based on the UK Biobank database (N = 804) measured + a CSA of 66.4 ± 6.61 mm2 at C2-C3 vertebral levels + (Bédard + & Cohen-Adad, 2022). Here, we measured larger CSAs: 73.59 + ± 7.41 mm2 at C2 and 74.32 ± 7.91 mm2 at C3 vertebral levels. This + discrepancy is likely caused by our study relying on T2-w images, + whilst Bédard and Cohen-Adad used T1-w images + (Bédard + & Cohen-Adad, 2022). It has been shown that T2-w scans + generally yield larger CSA compared to T1-w scans + (Cohen-Adad + et al., 2021b).

+

As for AP diameter and transverse diameter, values measured in + this study correspond with population estimates from Frostell et al. + (2016). + For instance, we measured an AP diameter of 7.86 ± 0.56 mm and a + transverse diameter of 11.9 ± 0.76 mm for the C2 vertebral level, + while Frostell et al. + (2016) + reported an AP diameter of 7.9 ± 1.6 mm and a transverse diameter of + 12.3 ± 2.4 mm for the same vertebral level.

+

Confirming previous studies + (Bédard + & Cohen-Adad, 2022; + Engl + et al., 2013; + Papinutto + et al., 2020; + Rashid + et al., 2006; + Solstrand + Dahlberg et al., 2020; + Yanase + et al., 2006), we showed that females have smaller CSA + relative to males across all vertebral levels. Smaller spinal cord + size is also mirrored by lower AP and transverse diameters in + females compared to males.

+

The increase in CSA around vertebral levels C4-C5 indicates the + location of cervical enlargement, the source of the large spinal + nerves that supply the upper limbs. This finding is consistent with + anatomical textbooks + (Standring, + 2020) and previous studies + (De + Leener et al., 2018; + Frostell + et al., 2016; + Horáková + et al., 2022; + Martin + et al., 2017b; + Mina + et al., 2021; + Rocca + et al., 2019). After the cervical enlargement (i.e., below + level C5), the spinal cord becomes smaller, which is mirrored by the + decrease in CSA, AP diameter, and transverse diameter. The decrease + in AP diameter along the superior-inferior direction, along with the + changing trends in compression ratio and eccentricity, corresponds + to the fact that the spinal cord is not cylindrical but rather + changes its shape across levels from circular shape at C1 and C2 + levels to a more elliptical shape around levels C5 and C6 + (Standring, + 2020).

+

Because various morphometric measures exhibited differing levels + of inter-subject variability (indicated by COV), we hypothesize that + normalizing measures with greater inter-subject variability, such as + CSA, would yield a more pronounced impact compared to normalizing + measures with lower inter-subject variability, such as solidity. We + measured a COV of 10.1% and 10.8% for the CSA at the C2 and C3 + vertebral levels, respectively. These values are similar to the + 9.96% COV reported by Bédard and Cohen-Adad for T1-w images at the + C2-C3 level + (Bédard + & Cohen-Adad, 2022).

+

The variability of morphometric measures between MRI vendors + might be explained by differences in sequence parameters and/or + reconstruction filters between vendors + (Cohen-Adad + et al., 2021b).

+
+ + 4.5 Limitations and Future Work +

The T2-w images from the open-access + spine-generic dataset cover only the cervical + spinal cord and have a relatively narrow age range (with 93.6% of + subjects aged 21 to 40 years). Despite this limitation, it remains + the largest open-source database of multi-contrast spinal cord MRI + data. We welcome future contributions of additional subjects across + different age groups and with data that encompasses the entire + spinal cord.

+

We are aware that the morphometric measures were derived solely + from T2-w MRI contrast and using the segmentation method trained + specifically for this contrast + (Gros + et al., 2019). This has to be considered when comparing with + other MRI contrasts, such as T1-w, which showed a smaller CSA + compared to T2-w + (Cohen-Adad + et al., 2021b). This might be mitigated in the future using a + contrast-agnostic segmentation algorithm + (Bédard, + 2023).

+

Future efforts will focus on validating the proposed methods in + pathologies such as traumatic and non-traumatic spinal cord injury + and multiple sclerosis. This validation process will provide + valuable insights into the applicability and accuracy of the methods + in the context of various spinal cord conditions.

+
+ + 4.6 Conclusions +

We introduced a new approach for the normalization of spinal cord + morphometric measures using the PAM50 spinal cord template. We built + an interactive database of spinal cord morphometric values across + 203 healthy adults. The database can be used to normalize spinal + cord morphometric features, stratified according to factors such as + sex, age, and MRI vendors. This database can also be used to further + inspect demographic, biological and image acquisition factors + associated with inter-subject variability.

+

The proposed methodology and results are open-source and fully + reproducible. The database and normalization method is applicable to + new datasets via the Spinal Cord Toolbox (SCT) + v6.0 and higher.

+
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