Skip to main content
SpringerLink
Log in

Shear wave elastography as a potential additional diagnostic tool in primary Sjögren’s syndrome: an observational study

  • Imaging
  • Published:
Rheumatology International Aims and scope Submit manuscript

Abstract

The primary aim of this study was to verify if shear wave elastography can be used to evaluate salivary gland involvement in primary Sjögren's syndrome (pSS). The secondary objective was to establish an accurate cut-off value for parotid and submandibular salivary gland stiffness and to verify whether there are any distinctions among pSS patients with or without subjective mouth dryness. This prospective study included 45 patients with pSS (2016 ACR/EULAR classification criteria) and 108 healthy controls. All subjects underwent bilateral shear wave elastography of the parotid and submandibular salivary glands. Clinical data of pSS patients were collected and compared to elastography results. Patients with pSS had significantly higher shear wave elastography values for the parotid and submandibular salivary glands than the controls. There were no statistical differences in SWE values between patients with or without mouth dryness. The optimal cut-off value (mean value of 4 salivary glands shear wave elastography results) to distinguish patients with or without pSS was 13.19 kPa with sensitivity = 97.8% and specificity = 100.0%. It was, therefore, confirmed that shear wave elastography measurement of salivary glands has strong predictive ability in pSS detection (AUC 97.8%, 95% CI 93.4–100.0%). Shear wave elastography seems to be a promising, non-invasive and simple quantitative adjunct test to support the diagnosis of pSS with good sensitivity and specificity. More extensive prospective studies are needed to standardize a study protocol.

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

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2

Similar content being viewed by others

Data availability

The data sets used and/or analyzed during the current study are available from the corresponding author on reasonable request.

References

  1. Theander E, Mandl T (2014) Primary Sjogren’s syndrome: diagnostic and prognostic value of salivary gland ultrasonography using a simplified scoring system. Arthrit Care Res (Hoboken) 66(7):1102–1107. https://doi.org/10.1002/acr.22264

    Article  Google Scholar 

  2. Ramos-Casals M, Brito-Zerón P, Sisó-Almirall A, Bosch X (2012) Primary Sjogren syndrome. BMJ 344:e3821. https://doi.org/10.1136/bmj.e3821

    Article  CAS  PubMed  Google Scholar 

  3. Qin B, Wang J, Yang Z, Yang M, Ma N, Huang F, Zhong R (2015) Epidemiology of primary Sjögren’s syndrome: a systematic review and meta-analysis. Ann Rheum Dis 74(11):1983–1989. https://doi.org/10.1136/annrheumdis-2014-205375

    Article  CAS  PubMed  Google Scholar 

  4. Vivino FB (2017) Sjogren’s syndrome: clinical aspects. Clin Immunol 182:48–54. https://doi.org/10.1016/j.clim.2017.04.005

    Article  CAS  PubMed  Google Scholar 

  5. Xu F, Laguna L, Sarkar A (2019) Aging-related changes in quantity and quality of saliva: Where do we stand in our understanding? J Text Stud 50(1):27–35

    Article  Google Scholar 

  6. Shiboski CH, Shiboski SC, Seror R, Criswell LA, Labetoulle M, Lietman TM, Rasmussen A, Scofield H, Vitali C, Bowman SJ, Mariette X (2017) 2016 American College of Rheumatology/European League Against Rheumatism classification criteria for primary Sjogren’s syndrome: a consensus and data-driven methodology involving three international patient cohorts. Ann Rheum Dis 76(1):9–16. https://doi.org/10.1136/annrheumdis-2016-210571

    Article  PubMed  Google Scholar 

  7. Rubin P, Holt JF (1957) Secretory sialography in diseases of the major salivary glands. Am J Roentgenol Radium Ther Nucl Med 77(4):575–598

    CAS  PubMed  Google Scholar 

  8. Świecka M, Maślińska M, Paluch Ł, Zakrzewski J, Kwiatkowska B (2019) Imaging methods in primary Sjögren’s syndrome as potential tools of disease diagnostics and monitoring. Reumatologia 57(6):336–342. https://doi.org/10.5114/reum.2019.91273

    Article  PubMed  PubMed Central  Google Scholar 

  9. Taljanovic MS, Gimber LH, Becker GW, Latt LD, Klauser AS, Melville DM, Gao L, Witte RS (2017) Shear-wave elastography: basic physics and musculoskeletal applications. Radiographics 37(3):855–870. https://doi.org/10.1148/rg.2017160116

    Article  PubMed  Google Scholar 

  10. Vachutka J, Sedlackova Z, Furst T, Herman M, Herman J, Salzman R, Dolezal L (2018) Evaluation of the effect of tissue compression on the results of shear wave elastography measurements. Ultrason Imaging 40(6):380–393. https://doi.org/10.1177/0161734618793837

    Article  PubMed  Google Scholar 

  11. Ferraioli G (2019) Review of liver elastography guidelines. J Ultrasound Med 38(1):9–14. https://doi.org/10.1002/jum.14856

    Article  PubMed  Google Scholar 

  12. Barr RG (2018) Shear wave liver elastography. Abdom Radiol (NY) 43(4):800–807. https://doi.org/10.1007/s00261-017-1375-1

    Article  Google Scholar 

  13. Sasaki Y, Hirooka Y, Kawashima H, Ishikawa T, Takeshita K, Goto H (2018) Measurements of renal shear wave velocities in chronic kidney disease patients. Acta Radiol 59(7):884–890. https://doi.org/10.1177/0284185117734417

    Article  PubMed  Google Scholar 

  14. Sigrist RMS, Liau J, Kaffas AE, Chammas MC, Willmann JK (2017) Ultrasound elastography: review of techniques and clinical applications. Theranostics 7(5):1303–1329. https://doi.org/10.7150/thno.18650

    Article  PubMed  PubMed Central  Google Scholar 

  15. Shoji S, Hashimoto A, Nakamura T, Hiraiwa S, Sato H, Sato Y, Tajiri T, Miyajima A (2018) Novel application of three-dimensional shear wave elastography in the detection of clinically significant prostate cancer. Biomed Rep 8(4):373–377. https://doi.org/10.3892/br.2018.1059

    Article  PubMed  PubMed Central  Google Scholar 

  16. Youk JH, Gweon HM, Son EJ (2017) Shear-wave elastography in breast ultrasonography: the state of the art. Ultrasonography 36(4):300–309. https://doi.org/10.14366/usg.17024

    Article  PubMed  PubMed Central  Google Scholar 

  17. Paluch Ł, Noszczyk B, Nitek Ż, Walecki J, Osiak K, Pietruski P (2018) Shear-wave elastography: a new potential method to diagnose ulnar neuropathy at the elbow. Eur Radiol 28(12):4932–4939. https://doi.org/10.1007/s00330-018-5517-9

    Article  PubMed  PubMed Central  Google Scholar 

  18. Paluch Ł, Pietruski P, Walecki J, Noszczyk BH (2018) Wrist to forearm ratio as a median nerve shear wave elastography test in carpal tunnel syndrome diagnosis. J Plast Reconstr Aesthet Surg 71(8):1146–1152. https://doi.org/10.1016/j.bjps.2018.03.022

    Article  PubMed  Google Scholar 

  19. Sobolewski P, Maślińska M, Zakrzewski J, Paluch Ł, Szymańska E, Walecka I (2020) Applicability of shear wave elastography for the evaluation of skin strain in systemic sclerosis. Rheumatol Int 40(5):737–745. https://doi.org/10.1007/s00296-020-04539-y

    Article  PubMed  Google Scholar 

  20. Dejaco C, De Zordo T, Heber D, Hartung W, Lipp R, Lutfi A, Magyar M, Zauner D, Lackner A, Duftner C, Horwath-Winter J, Graninger WB, Hermann J (2014) Real-time sonoelastography of salivary glands for diagnosis and functional assessment of primary Sjogren’s syndrome. Ultrasound Med Biol 40(12):2759–2767. https://doi.org/10.1016/j.ultrasmedbio.2014.06.023

    Article  PubMed  Google Scholar 

  21. Jousse-Joulin S, Coiffier G (2020) Current status of imaging of Sjogren’s syndrome. Best Pract Res Clin Rheumatol. https://doi.org/10.1016/j.berh.2020.101592

    Article  PubMed  Google Scholar 

  22. Gunes Tatar I, Altunoglu H, Kurt A, Altunoglu A, Ozturk MA, Erten S, Hekimoglu B (2014) The role of salivary gland elastosonography in Sjögren’s syndrome: preliminary results. Int J Rheum Dis 17(8):904–909. https://doi.org/10.1111/1756-185x.12503

    Article  PubMed  Google Scholar 

  23. Knopf A, Hofauer B, Thurmel K, Meier R, Stock K, Bas M, Manour N (2015) Diagnostic utility of Acoustic Radiation Force Impulse (ARFI) imaging in primary Sjoegren`s syndrome. Eur Radiol 25(10):3027–3034. https://doi.org/10.1007/s00330-015-3705-4

    Article  PubMed  Google Scholar 

  24. Samier-Guérin A, Saraux A, Gestin S, Cornec D, Marhadour T, Devauchelle-Pensec V, Bressollette L, Nonent M, Jousse-Joulin S (2016) Can ARFI elastometry of the salivary glands contribute to the diagnosis of Sjögren’s syndrome? Joint Bone Spine 83(3):301–306. https://doi.org/10.1016/j.jbspin.2015.11.002

    Article  PubMed  Google Scholar 

  25. Zhang S, Zhu J, Zhang X, He J, Li J (2016) Assessment of the stiffness of major salivary glands in primary Sjögren’s syndrome through quantitative acoustic radiation force impulse imaging. Ultrasound Med Biol 42(3):645–653. https://doi.org/10.1016/j.ultrasmedbio.2015.11.009

    Article  CAS  PubMed  Google Scholar 

  26. Hofauer B, Mansour N, Heiser C, Gahleitner C, Thuermel K, Bas M, Knopf A (2016) Sonoelastographic modalities in the evaluation of salivary gland characteristics in Sjögren’s syndrome. Ultrasound Med Biol 42(9):2130–2139. https://doi.org/10.1016/j.ultrasmedbio.2016.04.011

    Article  PubMed  Google Scholar 

  27. Chen S, Wang Y, Chen S, Wu Q, Chen S (2016) Virtual touch quantification of the salivary glands for diagnosis of primary Sjögren syndrome. J Ultrasound Med 35(12):2607–2613. https://doi.org/10.7863/ultra.16.01085

    Article  PubMed  Google Scholar 

  28. Turnaoglu H, KuralRahatli F, Pamukcu M, Haberal KM, Uslu N (2018) Diagnostic value of acustic radiation force impulse imaging in the assessment of salivary gland involvement in primary Sjögren’s sydrome. Med Ultrason 20(3):313–318. https://doi.org/10.11152/mu-1397

    Article  PubMed  Google Scholar 

  29. Cindil E, Oktar SO, Akkan K, Sendur HN, Mercan R, Tufan A, Ozturk MA (2018) Ultrasound elastography in assessment of salivary glands involvement in primary Sjögren’s syndrome. Clin Imaging 50:229–234. https://doi.org/10.1016/j.clinimag.2018.04.011

    Article  PubMed  Google Scholar 

  30. Pia LJ, Juan BM, Frank P, Angela AA, Jose G, Juan de Dios BS (2019) Is sonoelastography a helpful method of evaluation to diagnose Sjögren's syndrome? Int J Rheum Dis 22(2):175–181. https://onlinelibrary.wiley.com/doi/10.1111/1756-185X.13373

  31. Arslan S, Durmaz MS, Erdogan H, Esmen SE, Turgut B, Iyisoy MS (2020) Two-dimensional shear wave elastography in the assessment of salivary gland involvement in primary Sjögren’s syndrome. J Ultrasound Med 39(5):949–956. https://doi.org/10.1002/jum.15179

    Article  PubMed  Google Scholar 

  32. Bădărînză M, Serban O, Maghear L, Bocsa C, Micu M, Damian L, Felea I, Fodor D (2020) Shear wave elastography as a new method to identify parotid lymphoma in primary Sjögren Syndrome patients: an observational study. Rheumatol Int 40(8):1275–1281. https://doi.org/10.1007/s00296-020-04548-x

    Article  PubMed  Google Scholar 

  33. Mo YQ, Hao SY, Li QH, Liang JJ, Luo Y, Lan YQ, Zhong JL, Wang JW, Zhang XP, Huang WK, Dai L (2021) Ultrasonography predicts the results of labial salivary gland biopsy in patients with suspected Sjögren’s syndrome: a matrix risk model. Ther Adv Musculoskelet Dis 13:1759720x211010592. https://doi.org/10.1177/1759720x211010592

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  34. Moisoiu V, Badarinza M, Stefancu A, Iancu SD, Serban O, Leopold N, Fodor D (2020) Combining surface-enhanced Raman scattering (SERS) of saliva and two-dimensional shear wave elastography (2D-SWE) of the parotid glands in the diagnosis of Sjögren’s syndrome. Spectrochim Acta A Mol Biomol Spectrosc 235:118267. https://doi.org/10.1016/j.saa.2020.118267

    Article  CAS  PubMed  Google Scholar 

  35. Oruk YE, Çildağ MB, Karaman CZ, Çildağ S (2021) Effectiveness of ultrasonography and shear wave sonoelastography in Sjögren syndrome with salivary gland involvement. Ultrasonography 40(4):584–593. https://doi.org/10.14366/usg.21014

    Article  PubMed  PubMed Central  Google Scholar 

  36. Wierzbicka M, Kaluzny J, Ruchala M, Stajgis M, Kopec T, Szyfter W (2014) Sonoelastography–a useful adjunct for parotid gland ultrasound assessment in patients suffering from chronic inflammation. Med Sci Monit 20:2311–2317. https://doi.org/10.12659/MSM.890678

    Article  PubMed  PubMed Central  Google Scholar 

  37. Kimura-Hayama E, Criales-Vera S, Azpeitia-Espinosa L, Pacheco-Molina C, Reyes E, Lima G, Hernandez-Ramirez D, Llorente L, Hernandez-Molina G (2018) Elastographic ultrasound: an additional image tool in Sjogren’s syndrome. Int J Rheum Dis 21(6):1293–1300. https://doi.org/10.1111/1756-185x.13292

    Article  CAS  PubMed  Google Scholar 

  38. Satış H, Cindil E, Salman RB, Yapar D, Demir NB, Temel E, Babaoğlu H, Ataş N, Karadeniz H, Avanoğlu Güler A, Oktar S, Tufan A, Öztürk MA, Haznedaroğlu Ş, Göker B (2020) Parotid elastography: a potential alternative to replace labial biopsy in classification of patients with primary Sjögren’s syndrome? Clin Rheumatol 39(12):3707–3713. https://doi.org/10.1007/s10067-020-05146-9

    Article  PubMed  Google Scholar 

  39. Sezer İ, Erdem Toslak İ, Yağci B, Erbasan F, Ayan A, Karasu U (2019) The role of real-time tissue elastography and gray-scale ultrasound histogram analysis in the diagnosis of patients With Sjögren’s syndrome. Arch Rheumatol 34(4):371–379. https://doi.org/10.5606/ArchRheumatol.2019.7120

    Article  PubMed  PubMed Central  Google Scholar 

  40. Kim JW, Lee H, Park SH, Kim SK, Choe JY, Kim JK (2018) Salivary gland ultrasonography findings are associated with clinical, histological, and serologic features of Sjögren’s syndrome. Scand J Rheumatol 47(4):303–310. https://doi.org/10.1080/03009742.2017.1374451

    Article  PubMed  Google Scholar 

  41. Inanc N, Şahinkaya Y, Mumcu G, TüreÖzdemir F, Paksoy A, Ertürk Z, Direskeneli H, Bruyn GA (2019) Evaluation of salivary gland ultrasonography in primary Sjögren’s syndrome: does it reflect clinical activity and outcome of the disease? Clin Exp Rheumatol 37(Suppl 118):140–145

    PubMed  Google Scholar 

  42. Zhang X, Zhang S, He J, Hu F, Liu H, Li J, Zhu J, Li Z (2015) Ultrasonographic evaluation of major salivary glands in primary Sjögren’s syndrome: comparison of two scoring systems. Rheumatol (Oxf) 54(9):1680–1687. https://doi.org/10.1093/rheumatology/kev103

    Article  CAS  Google Scholar 

  43. Lee KA, Lee SH, Kim HR (2018) Diagnostic and predictive evaluation using salivary gland ultrasonography in primary Sjögren’s syndrome. Clin Exp Rheumatol 36(Suppl 112):165–172

    PubMed  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Early Arthritis Clinic, National Institute of Geriatrics, Rheumatology and Rehabilitation, Warsaw, Poland

    Marta Świecka, Maria Maślińska & Brygida Kwiatkowska

  2. Department of Radiology, Center of Postgraduate Medical Education, Gruca Orthopedic and Trauma Teaching Hospital, Otwock, Poland

    Łukasz Paluch & Jakub Zakrzewski

  3. Timeless Plastic Surgery Clinic, Warsaw, Poland

    Piotr Pietruski

Authors
  1. Marta Świecka
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Łukasz Paluch
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Piotr Pietruski
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Maria Maślińska
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Jakub Zakrzewski
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Brygida Kwiatkowska
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

All authors had substantial contribution to the acquisition and analysis of the data presented in this article. All authors revised and agreed on the final version of the work to be published. All authors take full responsibility in regard to all aspects of this work. Any questions that may be raised in the future concerning the integrity or this article will be evaluated and properly investigated and resolved.

Corresponding author

Correspondence to Marta Świecka.

Ethics declarations

Conflict of interest

The authors declare that they have no conflict of interest.

Ethical approval

All procedures were conducted in accordance with the Declaration of Helsinki (64th WMA General Assembly, Fortaleza, Brazil, October 2013). Approval was granted by the Bioetic Committee of the National Geriatrics, Rheumatology and Rehabilitation Institute (No KBT-7/2/2018). This manuscript complies with internationally accepted standards for research practice and reporting.

Informed consent

Written and informed consent was obtained from all individual participants included in the study.

Additional information

Publisher's Note

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

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Świecka, M., Paluch, Ł., Pietruski, P. et al. Shear wave elastography as a potential additional diagnostic tool in primary Sjögren’s syndrome: an observational study. Rheumatol Int 42, 1579–1587 (2022). https://doi.org/10.1007/s00296-022-05120-5

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00296-022-05120-5

Keywords

Search

Navigation