Radiomic Quantification for MRI Assessment of Sacroiliac Joints of Patients with Spondyloarthritis | Journal of Imaging Informatics in Medicine Skip to main content

Advertisement

Springer Nature Link
Log in

Radiomic Quantification for MRI Assessment of Sacroiliac Joints of Patients with Spondyloarthritis

  • Original Paper
  • Published:
Journal of Digital Imaging Aims and scope Submit manuscript

Abstract

Spondyloarthritis (SpA) is a group of diseases primarily involving chronic inflammation of the spine and peripheral joints, as evaluated by magnetic resonance imaging (MRI). Considering the complexity of SpA, we performed a retrospective study to discover quantitative/radiomic MRI-based features correlated with SpA. We also investigated different fat-suppression MRI techniques to develop detection models for inflammatory sacroiliitis. Finally, these model results were compared with those of experienced musculoskeletal radiologists, and the concordance level was evaluated. Examinations of 46 consecutive patients were obtained using SPAIR (spectral attenuated inversion recovery) and STIR (short tau inversion recovery) MRI sequences. Musculoskeletal radiologists manually segmented the sacroiliac joints for further extraction of 230 MRI features from gray-level histogram/matrices and wavelet filters. These features were associated with sacroiliitis, SpA, and the current biomarkers of ESR (erythrocyte sedimentation rate), CRP (C-reactive protein), BASDAI (Bath Ankylosing Spondylitis Activity Index), BASFI (Bath Ankylosing Spondylitis Functional Index), and MASES (Maastricht Ankylosing Spondylitis Enthesis Score). The Mann–Whitney U test showed that the radiomic markers from both MRI sequences were associated with active sacroiliitis and with SpA and its axial and peripheral subtypes (p < 0.05). Spearman’s coefficient also identified a correlation between MRI markers and data from clinical practice (p < 0.05). Fat-suppression MRI models yielded performances that were statistically equivalent to those of specialists and presented strong concordance in identifying inflammatory sacroiliitis. SPAIR and STIR acquisition protocols showed potential for the evaluation of sacroiliac joints and the composition of a radiomic model to support the clinical assessment of SpA.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Subscribe and save

Springer+ Basic
¥17,985 /Month
  • Get 10 units per month
  • Download Article/Chapter or eBook
  • 1 Unit = 1 Article or 1 Chapter
  • Cancel anytime
Subscribe now

Buy Now

Price includes VAT (Japan)

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4

Similar content being viewed by others

Availability of Data and Material

Data used in this study have not been made publicly available as our institutional review board has not allowed yet.

Code Availability

All software used in this work are open-source and readily available in each institution website.

References

  1. Rudwaleit MV, van der Heijde D, Landewé R, Akkoc N, Brandt J, Chou CT, Dougados M, Huang F, Gu J, Kirazli Y, van den Bosch F, Olivieri I, Roussou E, Scarpato S, SØrensen IJ, Valle-Oñate R, Weber U, Wei J, Sieper J: The Assessment of SpondyloArthritis International Society classification criteria for peripheral spondyloarthritis and for spondyloarthritis in general. Ann of the Rheum Dis, 70: 25-31, 2011

    Article  CAS  Google Scholar 

  2. Faleiros MC, Nogueira-Barbosa MH, Dalto VF, Ferreira-Junior JR, Tenório APM, Luppino-Assad R, Louzada-Junior P, Rangayyan RM, Azevedo-Marques PM: Machine learning techniques for computer-aided classification of active inflammatory sacroiliitis in magnetic resonance imaging. Adv in Rheumatol, 60: 1-10, 2020.

    Article  Google Scholar 

  3. Garg N, van den Bosch F, Deodhar A: The concept of spondyloarthritis: where are we now? Best Pract & Res Clin Rheumatol, 28: 663-672, 2014.

    Article  Google Scholar 

  4. Wang R, Ward M: Epidemiology of axial spondyloarthritis: an update. Curr Opin in Rheumatol, 30: 37-143, 2018.

    Article  Google Scholar 

  5. Sieper J, Rudwaleit M, Baraliakos X, Brandt J, Braun J, Burgos-Vargas R, Dougados M, Hermann KG, Landewé R, Maksymowych W, van der Heijde D: The Assessment of SpondyloArthritis international Society (ASAS) handbook: a guide to assess spondyloarthritis. Ann of the Rheum Dis, 68: ii1-ii44, 2009

  6. Paramarta JE, Baeten D: Spondyloarthritis: from unifying concepts to improved treatment. Rheumatol, 53: 1547-1559, 2013.

    Article  Google Scholar 

  7. Tenório APM, Faleiros MC, Ferreira-Junior JR, Dalto VF, Assad RL, Louzada-Junior P, Yoshida H, Nogueira-Barbosa MH, Azevedo-Marques PM: A study of MRI-based radiomics biomarkers for sacroiliitis and spondyloarthritis. Int J of Comput Assist Radiol and Surg, 15: 1737-1748, 2020.

    Article  Google Scholar 

  8. Lambert R, Bakker P, van der Heijde D, Weber U, Rudwaleit M, Hermann KG, Sieper J, Baraliakos X, Bennett A, Braun J, Burgos-Vargas R, Dougados M, Pedersen SJ, Jurik A, Maksymowych WP, Marzo-Ortega H, Østergaard M, Poddubnyy D, Reijnierse M, van den Bosch F, van der Horst-Bruinsma I, Landewé R: Defining active sacroiliitis on MRI for classification of axial spondyloarthritis: update by the ASAS MRI working group. Ann of the Rheum Dis, 75: 1958-1963, 2016.

    Article  Google Scholar 

  9. Dalto VF, Assad RL, Lorenzato MM, Crema MD, Louzada-Junior P, Nogueira-Barbosa MH: Comparison between STIR and T2-weighted SPAIR sequences in the evaluation of inflammatory sacroiliitis: diagnostic performance and signal-to-noise ratio. Radiol bras, 53: 223-228, 2020.

    Article  Google Scholar 

  10. van der Heijde D, Ramiro S, Landewé R, Baraliakos X, van den Bosch F, Sepriano A, Regel A, Ciurea A, Dagfinrud H, Dougados M, van Gaalen F, Géher P, van der Horst-Bruinsma I, Inman R, Jongkees M, Kiltz U, Kvien T, Machado PM, Marzo-Ortega H, Molto A, Navarro-Compàn V, Ozgocmen S, Pimentel-Santos FM, Reveille J, Rudwaleit M, Sieper J, Sampaio-Barros P, Wiek D, Braun J: 2016 update of the ASAS-EULAR management recommendations for axial spondyloarthritis. Ann of the Rheum Dis, 76: 978-991, 2017.

    Article  Google Scholar 

  11. Giardino A, Gupta S, Olson E, Sepulveda K, Lenchik L, Ivanidze J, Rakow-Penner R, Patel MJ, Subramaniam RM, Ganeshan D: Role of imaging in the era of precision medicine. Acad Radiol, 24: 639–649, 2017.

    Article  Google Scholar 

  12. Santos M, Ferreira-Junior JR, Wada DT, Tenório APM, Nogueira-Barbosa MH, Azevedo-Marques PM: Artificial intelligence, machine learning, computer-aided diagnosis, and radiomics: advances in imaging towards to precision medicine. Radiol bras, 52: 387–396, 2019.

    Article  Google Scholar 

  13. Ferreira-Junior JR, Koenigkam-Santos M, Tenório APM, Faleiros MC, Cipriano FEG, Fabro AT, Näppi J, Yoshida H, Azevedo-Marques PM: CT-based radiomics for prediction of histologic subtype and metastatic disease in primary malignant lung neoplasms. Int J of Comput Assist Radiol and Surg, 15: 163–172, 2020.

    Article  Google Scholar 

  14. Tenorio APM, Faleiros MC, Ferreira-Junior JR, Dalto VF, Assad RL, Nogueira-Barbosa MH, Azevedo-Marques PM: Machine learning models to predict axial and peripheral spondyloarthritis: a comparative radiomic study between SPAIR and STIR MRI sequences. In: Comput Assist Radiol and Surg, Munique. Proceedings of the 34th International Congress and Exhibition, 2020.

  15. Ferreira JR, Cardenas DAC, Moreno RA, Rebelo MFS, Krieger JE, Gutierrez MA: Novel chest radiographic biomarkers for COVID-19 using radiomic features associated with diagnostics and outcomes. J Digit Imaging, 34: 297-307, 2021.

    Article  Google Scholar 

  16. Tomaszewski MR, Gillies RJ: The biological meaning of radiomic features. Radiology, 298: 505-516, 2021.

    Article  Google Scholar 

  17. Ferreira-Junior JR, Oliveira MC, Azevedo-Marques PM: Integrating 3D image descriptors of margin sharpness and texture on a GPU-optimized similar pulmonary nodule retrieval engine. J of Supercomput, 73: 3451–3467, 2017.

    Article  Google Scholar 

  18. Rudwaleit M, Jurik AG, Hermann KA, Landewé R, van der Heijde D, Baraliakos X, Marzo-Ortega H, Østergaard M, Braun J, Sieper J: Defining active sacroiliitis on magnetic resonance imaging (MRI) for classification of axial spondyloarthritis: a consensual approach by the ASAS/OMERACT MRI group. Ann of the Rheum Dis, 68: 1520-1527, 2009.

    Article  CAS  Google Scholar 

  19. Kiltz U, van der Heijde D, Boonen A, Akkoc N, Bautista-Molano W, Burgos-Vargas R, Wei JC, Chiowchanwisawakit P, Dougados M, Duruoz MT, Elzorkany BK, Gaydukova I, Gensler LS, Gilio M, Grazio S, Gu J, Inman RD, Kim T, Navarro-Compan V, Marzo-Ortega H, Ozgocmen S, Santos FP, Schirmer M, Stebbings S, van den Bosch FE, van Tubergen A, Braun J: Measurement properties of the ASAS Health Index: results of a global study in patients with axial and peripheral spondyloarthritis. Ann of the Rheum Dis, 77: 1311-1317, 2018.

    Article  Google Scholar 

  20. Yip S, Liu Y, Parmar C, Li Q, Liu S, Qu F, Ye Z, Gillies RJ, Aerts H: Associations between radiologist-defined semantic and automatically computed radiomic features in non-small cell lung cancer. Sci Rep, 7: 1-11, 2017.

    Article  Google Scholar 

  21. Ferreira JR, Oliveira MC, Azevedo-Marques PM: Characterization of pulmonary nodules based on features of margin sharpness and texture. J Digit Imaging, 314: 451-463, 2018.

    Article  Google Scholar 

  22. Chronaiou I, Thomsen RS, Huuse EM, Euceda LR, Pedersen SJ, Hoff M, Sitter B: Quantifying bone marrow inflammatory edema in the spine and sacroiliac joints with thresholding. BMC musculoskelet disord, 18: 497, 2017.

    Article  Google Scholar 

  23. Maksymowych W, Inman R, Salonen D, Dhillon S, Williams M, Stone M, Conner-Spady B, Palsat J, Lambert RGW: Spondyloarthritis Research Consortium of Canada magnetic resonance imaging index for assessment of sacroiliac joint inflammation in ankylosing spondylitis. Arthritis Rheum, 53: 703–709, 2005.

    Article  Google Scholar 

  24. Dalto VF, Assad RL, Crema MD, Louzada-Junior P, Nogueira-Barbosa MH: MRI assessment of bone marrow oedema in the sacroiliac joints of patients with spondyloarthritis: is the SPAIR T2w technique comparable to STIR? Eur Radiol, 27: 3669–3676, 2017.

    Article  Google Scholar 

  25. Deodhar A, Rozycki M, Garges C, Shukla O, Arndt T, Grabowsky T, Park Y: Use of machine learning techniques in the development and refinement of a predictive model for early diagnosis of ankylosing spondylitis. Clin Rheumatol, 39: 975-982, 2020.

    Article  Google Scholar 

  26. Zhao SS, Hong C, Cai T, Xu C, Huang J, Ermann J, Goodson NJ, Solomon DH, Cai T, Liao KP: Incorporating natural language processing to improve classification of axial spondyloarthritis using electronic health records. Rheumatol, 59: 1059-1065, 2020.

    Article  Google Scholar 

  27. Walsh JA, Shao Y, Leng J, He T, Teng C, Redd D, Burningham QTZZ, Clegg DO, Sauer BC: Identifying axial spondyloarthritis in electronic medical records of US veterans. Arthritis Care & Res, 69: 1414-1420, 2017.

    Article  Google Scholar 

  28. Zwanenburg A, Vallières M, Abdalah MA, Aerts H, Andrearczyk V, Apte A, Ashrafinia S, Bakas S, Beukinga RJ, Boellaard R, Bogowicz M, Boldrini L, Buvat I, Cook GJR, Davatzikos C, Depeursinge A, Desseroit M, Dinapoli N, Dinh CV, Echegaray S, Naqa I, Fedorov AY, Gatta R, Gillies R, Goh V, Götz M, Guckenberger M, Ha S, Hatt M, Isensee F, Lambin P, Leger S, Leijenaar R, Lenkowicz J, Lippert F, Losnegård A, Maier-Hein K, Morin O, Müller H, Napel S, Nioche C, Orlhac F, Pati S, Pfaehler E, Rahmim A, Rao A, Scherer J, Siddique M, Sijtsema N, Fernandez J, Spezi E, Steenbakkers R, Tanadini-Lang S, Thorwarth D, Troost E, Upadhaya T, Valentini V, van Dijk L, van Griethuysen J, van Velden F, Whybra P, Richter C, Löck S: The Image Biomarker Standardization Initiative: standardized quantitative radiomics for high-throughput image-based phenotyping. Radiol, 295: 328-338, 2020.

    Article  Google Scholar 

Download references

Funding

This study was funded by Coordenação de Aperfeiçoamento de Pessoal de Nível Superior—Brasil (CAPES)—Finance Code 001, Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq), and Fundação de Amparo à Pesquisa do Estado de São Paulo (FAPESP) [grants numbers 2016/17078–0 and 2014/50889–7]. Coordenação de Aperfeiçoamento de Pessoal de Nível Superior,001,Paulo Mazzoncini de Azevedo-Marques,Conselho Nacional de Desenvolvimento Científico e Tecnológico,Fundação de Amparo à Pesquisa do Estado de São Paulo,2016/17078–0,Paulo Mazzoncini de Azevedo-Marques,2014/50889–7,Paulo Mazzoncini de Azevedo-Marques

Author information

Authors and Affiliations

  1. Ribeirão Preto Medical School, University of São Paulo, Av. dos Bandeirantes, 3900 Ribeirão Preto, SP, 14049-900, São Paulo, Brazil

    Ariane Priscilla Magalhães Tenório, José Raniery Ferreira-Junior, Vitor Faeda Dalto, Matheus Calil Faleiros, Rodrigo Luppino Assad, Paulo Louzada-Junior, Marcello Henrique Nogueira-Barbosa & Paulo Mazzoncini de Azevedo-Marques

  2. Department of Orthopedic Surgery, University of Missouri Health Care, Columbia, MO, USA

    Marcello Henrique Nogueira-Barbosa

  3. Schulich School of Engineering, University of Calgary, Calgary, AB, Canada

    Rangaraj Mandayam Rangayyan

Authors
  1. Ariane Priscilla Magalhães Tenório
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. José Raniery Ferreira-Junior
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Vitor Faeda Dalto
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Matheus Calil Faleiros
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Rodrigo Luppino Assad
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Paulo Louzada-Junior
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Marcello Henrique Nogueira-Barbosa
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Rangaraj Mandayam Rangayyan
    View author publications

    You can also search for this author in PubMed Google Scholar

  9. Paulo Mazzoncini de Azevedo-Marques
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Ariane Priscilla Magalhães Tenório.

Ethics declarations

Ethics Approval

All procedures performed in studies involving human participants were in accordance with the ethical standards of the institutional and/or national research committee (Comitê de Ética em Pesquisa do Hospital das Clínicas da Faculdade de Medicina de Ribeirão Preto da Universidade de São Paulo, reference number 2.356.447).

Consent to Participate

This work was a retrospective cohort study approved by our institutional review board that waived the requirement to obtain informed consent of the patients.

Consent for Publication

This work data has been approved by our institutional review board that waived the requirement to obtain informed consent of the patients.

Competing Interests

The authors declare no competing interests.

Additional information

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Supplementary Information

Below is the link to the electronic supplementary material.

Supplementary file1 (DOCX 1300 KB)

Supplementary file2 (PDF 280 KB)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Tenório, A.P.M., Ferreira-Junior, J.R., Dalto, V.F. et al. Radiomic Quantification for MRI Assessment of Sacroiliac Joints of Patients with Spondyloarthritis. J Digit Imaging 35, 29–38 (2022). https://doi.org/10.1007/s10278-021-00559-7

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10278-021-00559-7

Keywords

Search

Navigation