In vivo non-invasive skin imaging of cutaneous involvement in systemic sclerosis
Main Article Content
Abstract
Objectives: To evaluate the diagnostic and prognostic value of quantitative biomarkers derived from optical coherence tomography measurements for the management of patients with systemic sclerosis and to compare their clinical utility with the modified Rodnan skin score (mRSS).
Methods: Thirty-seven patients and 38 healthy volunteers were selected. The mRSS was performed in both groups over 17 anatomical sites and optical coherence tomography images were obtained over 7 of the 17 anatomical sites using 2 commercially available systems. For all sites, both types of images were processed to quantify the optical absorption, area and thickness of the different layers of the skin.
Results: For both systems, the 3 most extreme results and usually more affected locations provided statistically relevant data. For one system, the dermal-epidermal junction area, i.e. the integral sum of the optical density, led to significant difference between both groups. For the other system, the junction slope, i.e. the optical density gradient, demonstrated an excellent accuracy in scleroderma diagnosis when mRSS was high in the most relevant lesions, and superior sensitivity and specificity when mRSS was low.
Conclusions: This study shows promising results for optical coherence tomography to provide an objective non-invasive examination tool for early diagnosis of systemic sclerosis.
Keywords:
systemic sclerosis, skin, imaging, optical coherence tomography
Article Details
How to Cite
MARNEFFE, Alice et al.
In vivo non-invasive skin imaging of cutaneous involvement in systemic sclerosis.
Medical Research Archives, [S.l.], v. 11, n. 12, jan. 2024.
ISSN 2375-1924.
Available at: <https://esmed.org/MRA/mra/article/view/4440>. Date accessed: 15 may 2024.
doi: https://doi.org/10.18103/mra.v11i12.4440.
Section
Research Articles
The Medical Research Archives grants authors the right to publish and reproduce the unrevised contribution in whole or in part at any time and in any form for any scholarly non-commercial purpose with the condition that all publications of the contribution include a full citation to the journal as published by the Medical Research Archives.
References
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21. Vanhaecke A, Cutolo M, Heeman L, Vilela V, Deschepper E, Melsens K, et al. High frequency ultrasonography: reliable tool to measure skin fibrosis in SSC? A systematic literature review and additional pilot study. Rheumatology (Oxford). Dec 24 2021;61(1):42-52. doi:10.1093/rheumatology/keab462
22. Vos MHE, Nguyen KP, Van Erp PEJ, Van de Kerkhof PCM, Driessen RJB, Peppelman M. The value of (video)dermoscopy in the diagnosis and monitoring of common inflammatory skin diseases: a systematic review. Eur J Dermatol. Oct 1 2018;28(5):575-596. doi:10.1684/ejd.2018.3396
23. Flower VA, Barratt SL, Hart DJ, Mackenzie AB, Shipley JA, Ward SG, et al. High frequency ultrasound assessment of systemic sclerosis skin involvement: intra-observer repeatability and relationship with clinician assessment and dermal collagen content. J Rheumatol. Nov 1 2020;doi:10.3899/jrheum.200234
24. Naredo E, Pascau J, Damjanov N, Lepri G, Gordaliza PM, Janta I, et al. Performance of ultra-high-frequency ultrasound in the evaluation of skin involvement in systemic sclerosis: a preliminary report. Rheumatology (Oxford). Jul 1 2020;59(7):1671-1678. doi:10.1093/rheumatology/kez439
25. Huang D, Swanson EA, Lin CP, Schuman JS, Stinson WG, Chang W, et al. Optical coherence tomography. Science. Nov 22 1991;254 (5035):1178-81. doi:10.1126/science.1957169
26. Di Y, Ye JJ. [Application of optical coherence tomography angiography in ophthalmology]. Zhonghua Yan Ke Za Zhi. Jan 11 2017;53(1):65-72. doi:10.3760/cma.j.issn.0412-4081.2017.01.013
27. Shah R. Optical coherence tomography-guided PCI. Lancet. Apr 22 2017;389(10079):1607. doi:10.1016/S0140-6736(17)31017-6
28. Olsen J, Themstrup L, Jemec GB. Optical coherence tomography in dermatology. G Ital Dermatol Venereol. Oct 2015;150(5):603-15.
29. Levine A, Wang K, Markowitz O. Optical Coherence Tomography in the Diagnosis of Skin Cancer. Dermatol Clin. Oct 2017;35(4):465-488. doi:10.1016/j.det.2017.06.008
30. Heibel HD, Hooey L, Cockerell CJ. A Review of Noninvasive Techniques for Skin Cancer Detection in Dermatology. Am J Clin Dermatol. Aug 2020;21(4):513-524. doi:10.1007/s40257-020-00517-z
31. Ha L, Hundt JE. Optical coherence tomography for fast bedside imaging, assessment and monitoring of autoimmune inflammatory skin diseases? J Dtsch Dermatol Ges. Sep 2020;18(9):937-942. doi:10.1111/ddg.14266
32. Abignano G, Aydin SZ, Castillo-Gallego C, Liakouli V, Woods D, Meekings A, et al. Virtual skin biopsy by optical coherence tomography: the first quantitative imaging biomarker for scleroderma. Ann Rheum Dis. Nov 2013;72(11):1845-51. doi:10.1136/annrheumdis-2012-202682
33. Pires NSM, Dantas AT, Duarte A, Amaral MM, Fernandes LO, Dias TJC, et al. Optical coherence tomography as a method for quantitative skin evaluation in systemic sclerosis. Ann Rheum Dis. Mar 2018;77(3):465-466. doi:10.1136/annrheumdis-2016-210875
34. Liu CH, Assassi S, Theodore S, Smith C, Schill A, Singh M, et al. Translational optical coherence elastography for assessment of systemic sclerosis. J Biophotonics. Dec 2019;12 (12):e201900236. doi:10.1002/jbio.201900236
35. Boone M, Jemec GB, Del Marmol V. High-definition optical coherence tomography enables visualization of individual cells in healthy skin: comparison to reflectance confocal microscopy. Exp Dermatol. Oct 2012;21(10):740-4. doi:10.1111/j.1600-0625.2012.01569.x
36. van den Hoogen F, Khanna D, Fransen J, Johnson SR, Baron M, Tyndall A, et al. 2013 classification criteria for systemic sclerosis: an American college of rheumatology/European league against rheumatism collaborative initiative. Ann Rheum Dis. Nov 2013;72(11):1747-55. doi:10.1136/annrheumdis-2013-204424
37. LeRoy EC, Black C, Fleischmajer R, Jablonska S, Krieg T, Medsger TA, Jr., et al. Scleroderma (systemic sclerosis): classification, subsets and pathogenesis. J Rheumatol. Feb 1988;15(2):202-5.
38. Clements PJ, Hurwitz EL, Wong WK, Seibold JR, Mayes M, White B, et al. Skin thickness score as a predictor and correlate of outcome in systemic sclerosis: high-dose versus low-dose penicillamine trial. Arthritis Rheum. Nov 2000;43(11):2445-54. doi:10.1002/1529-0131(200011)43:11<2445::AID-ANR11>3.0.CO;2-Q
2. Denton CP, Khanna D. Systemic sclerosis. Lancet. Oct 7 2017;390(10103):1685-1699. doi:10.1016/S0140-6736(17)30933-9
3. Volkmann ER, Andreasson K, Smith V. Systemic sclerosis. Lancet. Jan 28 2023;401 (10373):304-318. doi:10.1016/S0140-6736(22)01692-0
4. Desbois AC, Cacoub P. Systemic sclerosis: An update in 2016. Autoimmun Rev. May 2016;15(5):417-26. doi:10.1016/j.autrev.2016.01.007
5. Nihtyanova SI, Schreiber BE, Ong VH, Rosenberg D, Moinzadeh P, Coghlan JG, et al. Prediction of pulmonary complications and long-term survival in systemic sclerosis. Arthritis Rheumatol. Jun 2014;66(6):1625-35. doi:10.1002/art.38390
6. LeRoy EC, Medsger TA, Jr. Criteria for the classification of early systemic sclerosis. J Rheumatol. Jul 2001;28(7):1573-6.
7. Steen VD, Medsger TA. Changes in causes of death in systemic sclerosis, 1972-2002. Ann Rheum Dis. Jul 2007;66(7):940-4. doi:10.1136/ard.2006.066068
8. Elhai M, Meune C, Boubaya M, Avouac J, Hachulla E, Balbir-Gurman A, et al. Mapping and predicting mortality from systemic sclerosis. Ann Rheum Dis. Nov 2017;76(11):1897-1905. doi:10.1136/annrheumdis-2017-211448
9. Khanna D, Furst DE, Clements PJ, Allanore Y, Baron M, Czirjak L, et al. Standardization of the modified Rodnan skin score for use in clinical trials of systemic sclerosis. J Scleroderma Relat Disord. Jan-Apr 2017;2(1):11-18. doi:10.5301/jsrd.5000231
10. Shand L, Lunt M, Nihtyanova S, Hoseini M, Silman A, Black CM, et al. Relationship between change in skin score and disease outcome in diffuse cutaneous systemic sclerosis: application of a latent linear trajectory model. Arthritis Rheum. Jul 2007;56(7):2422-31. doi:10.1002/art.22721
11. Steen VD, Medsger TA, Jr. Improvement in skin thickening in systemic sclerosis associated with improved survival. Arthritis Rheum. Dec 2001;44(12):2828-35. doi:10.1002/1529-0131(200112)44:12<2828::aid-art470>3.0.co;2-u
12. Domsic RT, Rodriguez-Reyna T, Lucas M, Fertig N, Medsger TA, Jr. Skin thickness progression rate: a predictor of mortality and early internal organ involvement in diffuse scleroderma. Ann Rheum Dis. Jan 2011;70(1):104-9. doi:10.1136/ard.2009.127621
13. Wu W, Jordan S, Graf N, de Oliveira Pena J, Curram J, Allanore Y, et al. Progressive skin fibrosis is associated with a decline in lung function and worse survival in patients with diffuse cutaneous systemic sclerosis in the European Scleroderma Trials and Research (EUSTAR) cohort. Ann Rheum Dis. May 2019;78(5):648-656. doi:10.1136/annrheumdis-2018-213455
14. Clements P, Lachenbruch P, Siebold J, White B, Weiner S, Martin R, et al. Inter and intraobserver variability of total skin thickness score (modified Rodnan TSS) in systemic sclerosis. J Rheumatol. Jul 1995;22(7):1281-5.
15. Clements PJ, Lachenbruch PA, Seibold JR, Zee B, Steen VD, Brennan P, et al. Skin thickness score in systemic sclerosis: an assessment of interobserver variability in 3 independent studies. J Rheumatol. Nov 1993;20(11):1892-6.
16. Hachulla E, Agard C, Allanore Y, Avouac J, Bader-Meunier B, Belot A, et al. French recommendations for the management of systemic sclerosis. Orphanet J Rare Dis. Jul 26 2021;16(Suppl 2):322. doi:10.1186/s13023-021-01844-y
17. Fueyo-Casado A, Campos-Munoz L, Pedraz-Munoz J, Conde-Taboada A, Lopez-Bran E. Nail fold dermoscopy as screening in suspected connective tissue diseases. Lupus. Jan 2016;25(1):110-1. doi:10.1177/0961203315605369
18. de Oliveira MFC, Leopoldo VC, Pereira KRC, de Moraes DA, Dias JBE, Goncalves MS, et al. Durometry as an alternative tool to the modified Rodnan's skin score in the assessment of diffuse systemic sclerosis patients: a cross-sectional study. Adv Rheumatol. Sep 21 2020;60(1):48. doi:10.1186/s42358-020-00152-6
19. Vanhaecke A, Verschuere S, Vilela V, Heeman L, Cutolo M, Smith V. Durometry in SSc: The hard facts. A systematic literature review and additional pilot study. Rheumatology (Oxford). May 14 2021;60(5):2099-2108. doi:10.1093/rheumatology/keab028
20. Moore TL, Lunt M, McManus B, Anderson ME, Herrick AL. Seventeen-point dermal ultrasound scoring system--a reliable measure of skin thickness in patients with systemic sclerosis. Rheumatology (Oxford). Dec 2003;42(12): 1559-63. doi:10.1093/rheumatology/keg435
21. Vanhaecke A, Cutolo M, Heeman L, Vilela V, Deschepper E, Melsens K, et al. High frequency ultrasonography: reliable tool to measure skin fibrosis in SSC? A systematic literature review and additional pilot study. Rheumatology (Oxford). Dec 24 2021;61(1):42-52. doi:10.1093/rheumatology/keab462
22. Vos MHE, Nguyen KP, Van Erp PEJ, Van de Kerkhof PCM, Driessen RJB, Peppelman M. The value of (video)dermoscopy in the diagnosis and monitoring of common inflammatory skin diseases: a systematic review. Eur J Dermatol. Oct 1 2018;28(5):575-596. doi:10.1684/ejd.2018.3396
23. Flower VA, Barratt SL, Hart DJ, Mackenzie AB, Shipley JA, Ward SG, et al. High frequency ultrasound assessment of systemic sclerosis skin involvement: intra-observer repeatability and relationship with clinician assessment and dermal collagen content. J Rheumatol. Nov 1 2020;doi:10.3899/jrheum.200234
24. Naredo E, Pascau J, Damjanov N, Lepri G, Gordaliza PM, Janta I, et al. Performance of ultra-high-frequency ultrasound in the evaluation of skin involvement in systemic sclerosis: a preliminary report. Rheumatology (Oxford). Jul 1 2020;59(7):1671-1678. doi:10.1093/rheumatology/kez439
25. Huang D, Swanson EA, Lin CP, Schuman JS, Stinson WG, Chang W, et al. Optical coherence tomography. Science. Nov 22 1991;254 (5035):1178-81. doi:10.1126/science.1957169
26. Di Y, Ye JJ. [Application of optical coherence tomography angiography in ophthalmology]. Zhonghua Yan Ke Za Zhi. Jan 11 2017;53(1):65-72. doi:10.3760/cma.j.issn.0412-4081.2017.01.013
27. Shah R. Optical coherence tomography-guided PCI. Lancet. Apr 22 2017;389(10079):1607. doi:10.1016/S0140-6736(17)31017-6
28. Olsen J, Themstrup L, Jemec GB. Optical coherence tomography in dermatology. G Ital Dermatol Venereol. Oct 2015;150(5):603-15.
29. Levine A, Wang K, Markowitz O. Optical Coherence Tomography in the Diagnosis of Skin Cancer. Dermatol Clin. Oct 2017;35(4):465-488. doi:10.1016/j.det.2017.06.008
30. Heibel HD, Hooey L, Cockerell CJ. A Review of Noninvasive Techniques for Skin Cancer Detection in Dermatology. Am J Clin Dermatol. Aug 2020;21(4):513-524. doi:10.1007/s40257-020-00517-z
31. Ha L, Hundt JE. Optical coherence tomography for fast bedside imaging, assessment and monitoring of autoimmune inflammatory skin diseases? J Dtsch Dermatol Ges. Sep 2020;18(9):937-942. doi:10.1111/ddg.14266
32. Abignano G, Aydin SZ, Castillo-Gallego C, Liakouli V, Woods D, Meekings A, et al. Virtual skin biopsy by optical coherence tomography: the first quantitative imaging biomarker for scleroderma. Ann Rheum Dis. Nov 2013;72(11):1845-51. doi:10.1136/annrheumdis-2012-202682
33. Pires NSM, Dantas AT, Duarte A, Amaral MM, Fernandes LO, Dias TJC, et al. Optical coherence tomography as a method for quantitative skin evaluation in systemic sclerosis. Ann Rheum Dis. Mar 2018;77(3):465-466. doi:10.1136/annrheumdis-2016-210875
34. Liu CH, Assassi S, Theodore S, Smith C, Schill A, Singh M, et al. Translational optical coherence elastography for assessment of systemic sclerosis. J Biophotonics. Dec 2019;12 (12):e201900236. doi:10.1002/jbio.201900236
35. Boone M, Jemec GB, Del Marmol V. High-definition optical coherence tomography enables visualization of individual cells in healthy skin: comparison to reflectance confocal microscopy. Exp Dermatol. Oct 2012;21(10):740-4. doi:10.1111/j.1600-0625.2012.01569.x
36. van den Hoogen F, Khanna D, Fransen J, Johnson SR, Baron M, Tyndall A, et al. 2013 classification criteria for systemic sclerosis: an American college of rheumatology/European league against rheumatism collaborative initiative. Ann Rheum Dis. Nov 2013;72(11):1747-55. doi:10.1136/annrheumdis-2013-204424
37. LeRoy EC, Black C, Fleischmajer R, Jablonska S, Krieg T, Medsger TA, Jr., et al. Scleroderma (systemic sclerosis): classification, subsets and pathogenesis. J Rheumatol. Feb 1988;15(2):202-5.
38. Clements PJ, Hurwitz EL, Wong WK, Seibold JR, Mayes M, White B, et al. Skin thickness score as a predictor and correlate of outcome in systemic sclerosis: high-dose versus low-dose penicillamine trial. Arthritis Rheum. Nov 2000;43(11):2445-54. doi:10.1002/1529-0131(200011)43:11<2445::AID-ANR11>3.0.CO;2-Q