Skip to main content

Advertisement

SpringerLink
Log in

The diagnostic performance of salivary gland ultrasound elastography in Sjögren’s syndrome and sicca symptoms: a systematic review and meta-analysis

  • Review
  • Published:
European Radiology Aims and scope Submit manuscript

Abstract

Objective

To systematically evaluate the diagnostic performance of ultrasound elastography (USE) in distinguishing primary Sjögren’s syndrome (pSS) from healthy/disease controls.

Methods

We searched the PubMed, Embase, Web of Science, and Cochrane Library databases for published literature on USE for diagnosing pSS. Bivariate random effects models were used to calculate the pooled sensitivity and specificity of USE. To determine the factors influencing heterogeneity, meta-regression and subgroup analyses were performed to assess country, diagnostic criteria, imaging mechanisms, shear wave elastography techniques, measurement location, control group category, and patient age. Publication bias was assessed using the asymmetry of the Deeks funnel plot.

Results

Fifteen articles covering 816 patients and 735 control participants were included. USE showed a pooled sensitivity of 0.80 (95% CI: 0.71–0.87) and specificity of 0.87 (95% CI: 0.78–0.92). Meta-regression and subgroup analyses revealed that shear wave elastography techniques, measurement location, and patient age were significant factors that affected study heterogeneity (p < 0.05). Elastography performs better in diagnosing patients aged ≤ 51 years compared to patients aged > 51 years. There was no significant publication bias.

Conclusion

USE demonstrates high accuracy in differentiating between pSS and healthy/disease control groups.

Clinical relevance statement

Ultrasound elastography, as a non-invasive and cost-effective technique, can be used to distinguish primary Sjögren’s syndrome from disease/healthy control groups by measuring the stiffness of salivary glands.

Key Points

• Ultrasound elastography is an acceptable technique for the diagnosis of primary Sjögren’s syndrome.

• The pooled sensitivity and specificity of ultrasound elastography for diagnosing primary Sjögren’s syndrome were 0.80 and 0.87, respectively.

• In patients aged ≤ 51 years with primary Sjögren’s syndrome, ultrasound elastography showed good diagnostic performance.

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
Fig. 3
Fig. 4
Fig. 5

Similar content being viewed by others

Abbreviations

ARFI:

Acoustic radiation force impulse imaging

CI:

Confidence intervals

HSROC:

Hierarchical summary receiver operating characteristic

pSS:

Primary Sjögren’s syndrome

SI:

Strain imaging

SWE:

Shear wave elastography

SWI:

Shear wave imaging

USE:

Ultrasound elastography

References

  1. Brito-Zerón P, Baldini C, Bootsma H et al (2016) Sjögren syndrome. Nat Rev Dis Primers 2:16047

    PubMed  Google Scholar 

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

    PubMed  Google Scholar 

  3. Mariette X, Criswell LA (2018) Primary Sjögren’s syndrome. N Engl J Med 378(10):931–939

    PubMed  Google Scholar 

  4. Ramsubeik K, Motilal S, Sanchez-Ramos L, Ramrattan LA, Kaeley GS, Singh JA (2020) Diagnostic accuracy of salivary gland ultrasound in Sjögren’s syndrome: a systematic review and meta-analysis. Ther Adv Musculoskelet Dis 12:1759720X20973560

    PubMed  PubMed Central  Google Scholar 

  5. Shiboski CH, Shiboski SC, Seror R et al (2016) 2016 American College of Rheumatology/European League Against Rheumatism classification criteria for primary Sjögren’s syndrome: a consensus and data-driven methodology involving three international patient cohorts. Arthritis Rheumatol 69(1):35–45

    PubMed  PubMed Central  Google Scholar 

  6. Vitali C, Bombardieri S, Jonsson R et al (2002) European Study Group on Classification Criteria for Sjögren’s Syndrome. Classification criteria for Sjögren’s syndrome: a revised version of the European criteria proposed by the American-European Consensus Group. Ann Rheum Dis 61(6):554–8

    CAS  PubMed  PubMed Central  Google Scholar 

  7. Milic VD, Petrovic RR, Boricic IV et al (2009) Diagnostic value of salivary gland ultrasonographic scoring system in primary Sjogren’s syndrome: a comparison with scintigraphy and biopsy. J Rheumatol 36(7):1495–1500

    PubMed  Google Scholar 

  8. Chikui T, Okamura K, Tokumori K et al (2006) Quantitative analyses of sonographic images of the parotid gland in patients with Sjögren’s syndrome. Ultrasound Med Biol 32(5):617–622

    PubMed  Google Scholar 

  9. Cindil E, Oktar SO, Akkan K et al (2018) Ultrasound elastography in assessment of salivary glands involvement in primary Sjögren’s syndrome. Clin Imaging 50:229–234

    PubMed  Google Scholar 

  10. Gürüf A, Öztürk M, Bayrak IK, Polat AV (2019) Shear wave versus strain elastography in the differentiation of benign and malignant breast lesions. Turk J Med Sci 49(5):1509–1517

    PubMed  PubMed Central  Google Scholar 

  11. Sigrist RMS, Liau J, Kaffas AE, Chammas MC, Willmann JK (2017) Ultrasound elastography: review of techniques and clinical applications. Theranostics 7(5):1303–1329

    PubMed  PubMed Central  Google Scholar 

  12. García-Carrasco M, Fuentes-Alexandro S, Escárcega RO, Salgado G, Riebeling C, Cervera R (2006) Pathophysiology of Sjögren’s syndrome. Arch Med Res 37(8):921–32

    PubMed  Google Scholar 

  13. Moher D, Liberati A, Tetzlaff J, Altman DG, PRISMA Group (2010) Preferred reporting items for systematic reviews and meta-analyses: the PRISMA statement. Int J Surg 8(5):336–41

    PubMed  Google Scholar 

  14. Whiting P, Rutjes AW, Reitsma JB, Bossuyt PM, Kleijnen J (2003) The development of QUADAS: a tool for the quality assessment of studies of diagnostic accuracy included in systematic reviews. BMC Med Res Methodol 3:25

    PubMed  PubMed Central  Google Scholar 

  15. Kim KW, Lee J, Choi SH, Huh J, Park SH (2015) Systematic review and meta-analysis of studies evaluating diagnostic test accuracy: a practical review for clinical researchers-part I. General guidance and tips. Korean J Radiol 16(6):1175–87

    PubMed  PubMed Central  Google Scholar 

  16. Lee J, Kim KW, Choi SH, Huh J, Park SH (2015) Systematic review and meta-analysis of studies evaluating diagnostic test accuracy: a practical review for clinical researchers-part II. Statistical methods of meta-analysis. Korean J Radiol 16(6):1188–96

    PubMed  PubMed Central  Google Scholar 

  17. DevilléevillBuntinx F, Bouter LM et al (2002) Conducting systematic reviews of diagnostic studies: didactic guidelines. BMC Med Res Methodol 2:9

    Google Scholar 

  18. 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

    PubMed  Google Scholar 

  19. Bădărînză M, Serban O, Maghear L et al (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

    PubMed  Google Scholar 

  20. Dejaco C, De Zordo T, Heber D et al (2014) Real-time sonoelastography of salivary glands for diagnosis and functional assessment of primary Sjögren’s syndrome. Ultrasound Med Biol 40(12):2759–2767

    PubMed  Google Scholar 

  21. Chen S, Wang Y, Zhang G, Chen S (2016) Combination of salivary gland ultrasonography and virtual touch quantification for diagnosis of Sjögren’s syndrome: a preliminary study. Biomed Res Int 2016:2793898

    PubMed  PubMed Central  Google Scholar 

  22. Hofauer B, Mansour N, Heiser C et al (2016) Sonoelastographic modalities in the evaluation of salivary gland characteristics in Sjögren’s syndrome. Ultrasound Med Biol 42(9):2130–2139

    PubMed  Google Scholar 

  23. Knopf A, Hofauer B, Thürmel K et al (2015) Diagnostic utility of Acoustic Radiation Force Impulse (ARFI) imaging in primary Sjoegren`s syndrome. Eur Radiol 25(10):3027–3034

    PubMed  Google Scholar 

  24. Moisoiu V, Badarinza M, Stefancu A et al (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

    CAS  PubMed  Google Scholar 

  25. 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

    PubMed  PubMed Central  Google Scholar 

  26. Özer H, Tezcan D, Hakbilen S et al (2023) Diagnostic performance of gray-scale ultrasound and shear wave elastography in assessing salivary gland involvement in patients with primary Sjögren’s syndrome. J Clin Ultrasound 51(1):187–194

    PubMed  Google Scholar 

  27. Prata AR, Freitas JP, Marques ML et al (2020) Shear-wave elastography evaluation of major salivary glands in primary Sjögren’s syndrome. ARP Rheumatol 1(3):197–204

    Google Scholar 

  28. SatARP RhCindil E, Salman RB et al (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

    Google Scholar 

  29. Świecka M, Paluch Ł, Pietruski P, Maślińska M, Zakrzewski J, Kwiatkowska B (2022) Shear wave elastography as a potential additional diagnostic tool in primary Sjögren’s syndrome: an observational study. Rheumatol Int 42(9):1579–1587

    PubMed  Google Scholar 

  30. Turnaoglu H, Kural Rahatli 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

    PubMed  Google Scholar 

  31. Zhang X, Zhang S, Feng R, Yao H, Tang S, He J (2021) Sonoelastography of salivary glands for diagnosis and clinical evaluation in primary Sjögren’s syndrome. Clin Exp Rheumatol 39(Suppl 133):184–189

    PubMed  Google Scholar 

  32. Shiboski SC, Shiboski CH, Criswell LA et al (2012) American College of Rheumatology classification criteria for Sjögren’s syndrome: a data-driven, expert consensus approach in the Sjögren’s International Collaborative Clinical Alliance cohort. Arthritis Care Res 64(4):475–487

    CAS  Google Scholar 

  33. Dewall RJ (2013) Ultrasound elastography: principles, techniques, and clinical applications. Crit Rev Biomed Eng 41(1):1–19

    PubMed  Google Scholar 

  34. Bamber J, Cosgrove D, Dietrich CF et al (2013) EFSUMB guidelines and recommendations on the clinical use of ultrasound elastography. Part 1: basic principles and technology. Ultraschall Med 34:169–184

    CAS  PubMed  Google Scholar 

  35. Cosgrove D, Piscaglia F, Bamber J et al (2013) EFSUMB guidelines and recommendations on the clinical use of ultrasound elastography. Part 2: clinical applications. Ultraschall Med 34:238–253

    CAS  PubMed  Google Scholar 

  36. ToanNK ASG (2021) Aging-related metabolic dysfunction in the salivary gland: a review of the literature. Int JMol Sci 22:5835

    Google Scholar 

  37. Maślińska M, Przygodzka M, Kwiatkowska B, Sikorska-Siudek K (2015) Sjögren’s syndrome: still not fully understood disease. Rheumatol Int 35(2):233–241

    PubMed  Google Scholar 

  38. Jiali C, Yuebo J, Jing Li, Shi C, Jing He (2018) Gender differences in clinical and immunological characteristics and the pathogenic study of primary SjiJgren s syndrome. Chin J Rheumatol 22(8):526–531

    Google Scholar 

  39. Fujibayashi T, Sugai S, Miyasaka N et al (2004) Revised Japanese criteria for Sjögren’s syndrome (1999): availability and validity. Mod Rheumatol 14:425–34

    PubMed  Google Scholar 

  40. Vitali C, Del Papa N (2017) Classification and diagnostic criteria in Sjögren’s syndrome: a long-standing and still open controversy. Ann Rheum Dis 76(12):1953–1954

    PubMed  Google Scholar 

  41. Yanqing W, Fang N, Longli W, Yangyang Z, Yuting T (2021) Clinical value of virtual touch tissue imaging quantification in diagnosing salivary gland Sjögren’s syndrome. Chin J Med Ultrasound (Electronic Edition) 18(1):11–16

    Google Scholar 

  42. Giuseppetti GM, Argalia G, Salera D, Ranaldi R, Danieli G, Cappelli M (2005) Ultrasonographic contrast-enhanced study of sicca syndrome. Eur J Radiol 54(2):225–232

    PubMed  Google Scholar 

  43. Samier-Guérin A, Saraux A, Gestin S et al (2016) Can ARFI elastometry of the salivary glands contribute to the diagnosis of Sjögren’s syndrome? Joint Bone Spine 83(3):301–306

    PubMed  Google Scholar 

Download references

Funding

The authors state that this work has not received any funding.

Author information

Authors and Affiliations

  1. Department of Ultrasound, Hebei Medical University Third Affiliated Hospital, No.139 Ziqiang Road, Qiaoxi District, Shijiazhuang, Hebei Province, China

    Xinpeng Dai, Xin Sui, Simei Chen, Bingxin Zhao & Zongjie Liu

  2. Department of Ultrasound, Hebei General Hospital, NO.348 Heping West Road, Xinhua District, Shijiazhuang, Hebei Province, China

    Xiaoyan Wang

Authors
  1. Xinpeng Dai
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Xin Sui
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Simei Chen
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Bingxin Zhao
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Zongjie Liu
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Xiaoyan Wang
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Xin Sui.

Ethics declarations

Guarantor

The scientific guarantor of this publication is Xin Sui.

Conflict of interest

The authors of this manuscript declare no relationships with any companies, whose products or services may be related to the subject matter of the article.

Statistics and biometry

One of the authors (Xinpeng Dai) has significant statistical expertise.

Informed consent

Written informed consent was not required for this study because this study is a systematic review and meta-analysis of published studies.

Ethical approval

Institutional Review Board approval was not required because this study is a systematic review and meta-analysis of published studies.

Methodology

•Systematic review

• Meta-analysis

• Performed at one institution

Additional information

Publisher's note

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

Rights and permissions

Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Dai, X., Sui, X., Chen, S. et al. The diagnostic performance of salivary gland ultrasound elastography in Sjögren’s syndrome and sicca symptoms: a systematic review and meta-analysis. Eur Radiol 34, 1545–1555 (2024). https://doi.org/10.1007/s00330-023-10166-5

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00330-023-10166-5

Keywords

Search

Navigation