Abstract
Objectives
A clinically practical tool to assess skin biomechanical properties rapidly and accurately is still lacking. Our aim was to examine the intra- and inter-observer reproducibility of a myotonometer for objective skin property assessment in systemic sclerosis (SSc), comparing it with the modified Rodnan skin score (mRSS), and distinguishing patients from healthy controls.
Method
Thirty-four patients (21 limited and 13 diffuse SSc), and 31 age and gender-matched healthy controls were enrolled. Skin tone and stiffness were measured at four different anatomical sites (the forearm, hand, leg, and foot) using a myotonometer. The correlation between the mRSS and skin properties was assessed. Also, hand functionality was evaluated for possible correlations between the variables. The differences in skin properties between dcSSc and lcSSc patients, and healthy controls were assessed using variance analysis.
Results
Intra- and inter-examiner reproducibility were excellent (ICC = 0.70 to 0.98) for tone and stiffness except for non-dominant hand tone, which showed good reliability (ICC = 0.64 to 0.74). Stiffness and tone values of the hands, forearms, and feet significantly correlated with mRSS total score (r = 0.40 to 0.71, p < 0.05). Additionally, tone and stiffness of the hands and forearms moderately correlated with hand function (p < 0.05). Tone and stiffness values increased in patients with dcSSc compared to healthy controls, or patients with lcSSc, at the hands, forearms, and legs (p < 0.05).
Conclusions
Our findings emphasize the potential utility of the myotonometer for assessing skin properties and differentiating SSc patients from controls, demonstrating its promise as a valuable clinical evaluation tool in this context.
Key Points •The myotonometer displayed excellent intra- and inter-examiner reproducibility for assessing skin properties. •Skin tone and stiffness parameters well correlated with the mRSS scores. •The myotonometer can distinguish patients with diffuse cutaneous SSc from healthy controls. |
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Data availability
The datasets generated during and/or analyzed during the current study are available from the corresponding author on reasonable request.
References
Allanore Y, Simms R, Distler O, Trojanowska M, Pope J, Denton CP et al (2015) Systemic sclerosis. Nat Rev Dis Primers 1:1–21. https://doi.org/10.1038/nrdp.2015.2
LeRoy EC, Black C, Fleischmajer R, Jablonska S, Krieg T, Medsger T Jr et al (1988) Scleroderma (systemic sclerosis): classification, subsets and pathogenesis. J Rheumatol 15:202–205
Steen VD, Medsger TA Jr (2001) Improvement in skin thickening in systemic sclerosis associated with improved survival. Arthritis Rheumatism: Off J Am College Rheumatol 44:2828–2835. https://doi.org/10.1002/1529-0131(200112)44:12/3c2828::aid-art470/3e3.0.co;2-u
Denton CP, Khanna D (2017) Systemic sclerosis. Lancet 390:1685–1699. https://doi.org/10.1016/S0140-6736(17)30933-9
Van Lankveld W, Vonk M, Teunissen H, Van den Hoogen F (2007) Appearance self-esteem in systemic sclerosis—subjective experience of skin deformity and its relationship with physician-assessed skin involvement, disease status and psychological variables. Rheumatology 46:872–876. https://doi.org/10.1093/rheumatology/kem008
van Leeuwen NM, Ciaffi J, Liem SI, Huizinga TW, de Vries-Bouwstra JK (2021) Health-related quality of life in patients with systemic sclerosis: evolution over time and main determinants. Rheumatology 60:3646–3655. https://doi.org/10.1093/rheumatology/keaa827
Kumánovics G, Péntek M, Bae S, Opris D, Khanna D, Furst DE et al (2017) Assessment of skin involvement in systemic sclerosis. Rheumatology 56:v53–v66. https://doi.org/10.1093/rheumatology/kex202
Santiago T, Santiago M, Coutinho M, Salvador M, Da Silva J (2020) How much of skin improvement over time in systemic sclerosis is due to normal ageing? A prospective study with shear-wave elastography. Arthritis Res Ther 22:1–7
Herrick AL, Assassi S, Denton CP (2022) Skin involvement in early diffuse cutaneous systemic sclerosis: an unmet clinical need. Nat Rev Rheumatol 18:276–285. https://doi.org/10.1038/s41584-022-00765-9
Khanna D, Furst DE, Clements PJ, Allanore Y, Baron M, Czirjak L et al (2017) Standardization of the modified Rodnan skin score for use in clinical trials of systemic sclerosis. J Scleroderma Relat Disord 2:11–18. https://doi.org/10.5301/jsrd.5000231
Ross L, Stevens W, Wilson M, Strickland G, Walker J, Sahhar J et al (2020) Can patient-reported symptoms be used to measure disease activity in systemic sclerosis? Arthritis Care Res 72:1459–1465. https://doi.org/10.1002/acr.24053
Merkel PA, Silliman NP, Denton CP, Furst DE, Khanna D, Emery P et al (2008) Validity, reliability, and feasibility of durometer measurements of scleroderma skin disease in a multicenter treatment trial. Arthritis Care Res: Off J Am College Rheumatol 59:699–705. https://doi.org/10.1002/art.23564
Oliveira MdFCd, Leopoldo VC, Pereira KRC, Moraes DAd, Dias JBE, Gonçalves MS, et al (2020) 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 60. https://doi.org/10.1186/s42358-020-00152-6
Lepri G, Hughes M, Allanore Y, Denton CP, Furst DE, Wang Y, et al (2023) The role of skin ultrasound in systemic sclerosis: looking below the surface to understand disease evolution. Lancet Rheumatol 5(7):e422–e425. https://doi.org/10.1016/S2665-9913(23)00100-5
Dellalana LE, Chen F, Vain A, Gandelman JS, Põldemaa M, Chen H et al (2019) Reproducibility of the durometer and myoton devices for skin stiffness measurement in healthy subjects. Skin Res Technol 25:289–293. https://doi.org/10.1111/srt.12646
Sandqvist G, Nilsson J-Å, Wuttge DM, Hesselstrand R (2014) Development of a modified hand mobility in scleroderma (HAMIS) test and its potential as an outcome measure in systemic sclerosis. J Rheumatol 41:2186–2192. https://doi.org/10.3899/jrheum.140286
Maddali Bongi S, Del Rosso A, Galluccio F, Sigismondi F, Miniati I, Conforti ML et al (2009) Efficacy of connective tissue massage and Mc Mennell joint manipulation in the rehabilitative treatment of the hands in systemic sclerosis. Clin Rheumatol 28:1167–1173. https://doi.org/10.1007/s10067-009-1216-x
Bizzini M, Mannion AF (2003) Reliability of a new, hand-held device for assessing skeletal muscle stiffness. Clin Biomech 18:459–461. https://doi.org/10.1016/s0268-0033(03)00042-1
Chen F, Dellalana LE, Gandelman JS, Vain A, Jagasia MH, Tkaczyk ER (2019) Non-invasive measurement of sclerosis in cutaneous cGVHD patients with the handheld device Myoton: a cross-sectional study. Bone Marrow Transplant 54:616–619. https://doi.org/10.1038/s41409-018-0346-7
Baker LX, Chen F, Ssempijja Y, Byrne M, Kim TK, Vain A et al (2021) Longitudinal tracking of skin dynamic stiffness to quantify evolution of sclerosis in chronic graft-versus-host disease. Bone Marrow Transplant 56:989–991. https://doi.org/10.1038/s41409-020-01158-w
Gilbert I, Gaudreault N, Gaboury I (2021) Intra-and inter-evaluator reliability of the MyotonPRO for the assessment of the viscoelastic properties of caesarean section scar and unscarred skin. Skin Res Technol 27:370–375. https://doi.org/10.1111/srt.12956
Van Den Hoogen F, Khanna D, Fransen J, Johnson SR, Baron M, Tyndall A et al (2013) 2013 classification criteria for systemic sclerosis: an American College of Rheumatology/European League against Rheumatism Collaborative Initiative. Arthritis Rheum 65:2737–2747. https://doi.org/10.1002/art.38098
LeROY EC, Medsger TA Jr (2001) Criteria for the classification of early systemic sclerosis. J Rheumatol 28:1573–1576
Von Elm E, Altman DG, Egger M, Pocock SJ, Gøtzsche PC, Vandenbroucke JP et al (2014) The Strengthening the Reporting of Observational Studies in Epidemiology (STROBE) Statement: guidelines for reporting observational studies. Int J Surg 12:1495–1499. https://doi.org/10.1016/j.ijsu.2014.07.013
Clements P, Lachenbruch P, Siebold J, White B, Weiner S, Martin R et al (1995) Inter and intraobserver variability of total skin thickness score (modified Rodnan TSS) in systemic sclerosis. J Rheumatol 22:1281–1285
Santiago T, Santiago M, Moreira S, Santos L, Salvador MJ, Da Silva JAP (2023) Influence of contextual factors and reliability of ultrasound skin measures in persons with systemic sclerosis and healthy controls. Clin Exp Rheumatol 41:1599–1604
Rosicka K, Mierzejewska-Krzyżowska B, Mrówczyński W (2022) Skin biomechanical and viscoelastic properties measured with MyotonPRO in different areas of human body. Skin Res Technol 28:236–245. https://doi.org/10.1111/srt.13116
Lucas NP, Macaskill P, Irwig L, Bogduk N (2010) The development of a quality appraisal tool for studies of diagnostic reliability (QAREL). J Clin Epidemiol 63:854–861
Schouffoer AA, van der Giesen FJ, Beaart-van de Voorde LJ, Wolterbeek R, Huizinga TW, Vliet Vlieland TP (2016) Validity and responsiveness of the Michigan Hand Questionnaire in patients with systemic sclerosis. Rheumatology 55:1386–93. https://doi.org/10.1093/rheumatology/kew016
Chung KC, Pillsbury MS, Walters MR, Hayward RA (1998) Reliability and validity testing of the Michigan hand outcomes questionnaire. J Hand Surg 23:575–587
Walter S, Eliasziw M, Donner A (1998) Sample size and optimal designs for reliability studies. Stat Med 17:101–110
Weir JP (2005) Quantifying test-retest reliability using the intraclass correlation coefficient and the SEM. J Strength Cond Res 19:231–240. https://doi.org/10.1519/15184.1
Terwee CB, Bot SD, de Boer MR, van der Windt DA, Knol DL, Dekker J et al (2007) Quality criteria were proposed for measurement properties of health status questionnaires. J Clin Epidemiol 60:34–42. https://doi.org/10.1016/j.jclinepi.2006.03.012
de Vet HC, Terwee CB, Knol DL, Bouter LM (2006) When to use agreement versus reliability measures. J Clin Epidemiol 59:1033–1039. https://doi.org/10.1016/j.jclinepi.2005.10.015
Fleiss JL (2011) Design and analysis of clinical experiments. Wiley
Krieg T, Takehara K (2006) Skin disease: a cardinal feature of systemic sclerosis. Rheumatology 48:ii14-iii8. https://doi.org/10.1093/rheumatology/kep108
Khanna D, Clements PJ, Volkmann ER, Wilhalme H, Tseng C-h, Furst DE et al (2019) Minimal clinically important differences for the modified Rodnan skin score: results from the Scleroderma Lung Studies (SLS-I and SLS-II). Arthritis Res Ther 21:1–9. https://doi.org/10.1186/s13075-019-1809-y
Ghosh S, Baker L, Chen F, Khera Z, Vain A, Zhang K, et al (2013) Interrater reproducibility of the Myoton and durometer devices to quantify sclerotic chronic graft-versus-host disease. Arch Dermatol Res 1–10. https://doi.org/10.1007/s00403-023-02626-1
Moon KW, Song R, Kim JH, Lee EY, Lee EB, Song YW (2012) The correlation between durometer score and modified Rodnan skin score in systemic sclerosis. Rheumatol Int 32:2465–2470. https://doi.org/10.1007/s00296-011-1993-9
Hesselstrand R, Carlestam J, Wildt M, Sandqvist G, Andréasson K (2015) High frequency ultrasound of skin involvement in systemic sclerosis–a follow-up study. Arthritis Res Ther 17:1–6. https://doi.org/10.1186/s13075-015-0853-5
Sandler RD, Matucci-Cerinic M, Hughes M (2020) Musculoskeletal hand involvement in systemic sclerosis. Seminars in arthritis and rheumatism 50(2):329–334. https://doi.org/10.1016/j.semarthrit.2019.11.003
Yang Y, Yan F, Wang L, Xiang X, Tang Y, Li Q et al (2018) Quantification of skin stiffness in patients with systemic sclerosis using real-time shear wave elastography: a preliminary study. Clin Exp Rheumatol 36:118–125
Hou Y, Zhu Q-l, Liu H, Jiang Y-x, Wang L, Xu D et al (2015) A preliminary study of acoustic radiation force impulse quantification for the assessment of skin in diffuse cutaneous systemic sclerosis. J Rheumatol 42:449–55
Hesselstrand R, Scheja A, Wildt M, Åkesson A (2008) High-frequency ultrasound of skin involvement in systemic sclerosis reflects oedema, extension and severity in early disease. Rheumatology 47:84–87
Baker LX, Chen F, Cronin A, Chen H, Vain A, Jagasia M et al (2021) Optimal biomechanical parameters for measuring sclerotic chronic graft-versus-host disease. JID Innov 1:100037. https://doi.org/10.1016/j.xjidi.2021.100037
Acknowledgements
We thank Erdi Dirilen for his support to the methodological design of this study. We also thank all our participants for their great contribution to this present study.
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ÖÖ: conceptualization, formal analysis, investigation, methodology, validation, writing – original draft, writing – review and editing. DŞ: investigation, methodology, writing – review and editing. AÖA: conceptualization, formal analysis, methodology, writing – review and editing. TÇS: conceptualization, funding acquisition, writing – review and editing. NU: methodology, writing – review and editing. NŞ: conceptualization, investigation, writing – review and editing. MET: supervision, writing – review and editing.
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Öztürk, Ö., Şahin, D., Acar, A.Ö. et al. Performance of myotonometer in the assessment of skin involvement in systemic sclerosis. Clin Rheumatol 43, 695–705 (2024). https://doi.org/10.1007/s10067-023-06848-6
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DOI: https://doi.org/10.1007/s10067-023-06848-6