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Ultrasonography in the diagnosis of suspected primary Sjögren’s syndrome and concordance with salivary gland biopsy: a Spanish single-center study

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Abstract

Objective

The study aims to evaluate the utility of major salivary gland ultrasonography for diagnosis of primary Sjögren’s syndrome (pSS) and to assess its concordance with minor salivary gland biopsy (MSGB).

Methods

A cross-sectional study of 72 patients with suspected pSS was performed. Demographic, clinical, and serological data were collected. MSGB was performed, as was ultrasonography. The ultrasound technician was blind to clinical, serological, and histological data. The validity of ultrasonography compared with MSGB, the American-European Consensus Group (AECG), and American College of Rheumatology (ACR)/European Alliance of Associations for Rheumatology (EULAR) criteria was assessed by calculating the percentage of agreement, sensitivity, specificity, positive and negative predictive values, and area under the curve (AUC).

Results

Based on MSGB as the gold standard, the percentage of agreement between both tests was 78% (AUC 0.75). Based on the ACR/EULAR criteria, the percentage of agreement was 83% (AUC 0.78) for ultrasonography and 81% (AUC 0.83) for biopsy. Sensitivity and specificity were 90% and 67%, respectively, for ultrasonography and 76% and 90% for biopsy. The results were similar with the AECG criteria. The intra- and inter-observer variability was good (κ > 0.7). Significant differences were observed for positive anti-Ro52 values and hypergammaglobulinemia in pathological ultrasound scans.

Conclusion

Diagnostic ultrasonography is as useful as MSGB in pSS. Therefore, it could be included in the classification criteria. In this cohort, it proved more sensitive than MSGB and could be used as an initial test for patients suspected of having pSS. MSGB could be used in cases where clinical and serological results are inconclusive.

Key Points

• Major salivary gland ultrasonography adds diagnostic value similar to that of MSGB, thus potentially enabling this invasive procedure to be avoided.

• Ultrasonography could be included in the classification criteria for primary Sjögren’s syndrome.

• Given that ultrasonography is more sensitive and less specific than MSGB, it could be used as an initial diagnostic test in patients with suspected Sjögren’s syndrome.

• Biopsy should be performed in those cases where ultrasonography, clinical, and serological data are inconclusive.

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References

  1. Cornec D, Jousse-Joulin S, Pers JO, Marhadour T, Cochener B, Boisramé-Gastrin S, Nowak E, Youinou P, Saraux A, Devauchelle-Pensec V (2013) Contribution of salivary gland ultrasonography to the diagnosis of Sjögren’s syndrome: toward new diagnostic criteria? Arthritis Rheum 65(1):216–225. https://doi.org/10.1002/art.37698

    Article  PubMed  Google Scholar 

  2. Bukhari AF, Farag A, Papas A, Ganguly R, Campos H, Ramesh A (2021) Salivary glands ultrasonography as a diagnostic aid in Sjögren syndrome: a prospective pilot investigation. Oral Surg Oral Med Oral Pathol Oral Radiol 132(2):172–181. https://doi.org/10.1016/j.oooo.2021.03.007

    Article  PubMed  Google Scholar 

  3. 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 

  4. Devauchelle-Pensec V, Zabotti A, Carvajal-Alegria G, Filipovic N, Jousse-Joulin S, & De Vita S (2019). Salivary gland ultrasonography in primary Sjögren’s syndrome: opportunities and challenges. Rheumatology (Oxford, England), kez079. Advance online publication. https://doi.org/10.1093/rheumatology/kez079

  5. Baldini C, Zabotti A, Filipovic N, Vukicevic A, Luciano N, Ferro F, Lorenzon M, De Vita S (2018) Imaging in primary Sjögren’s syndrome: the ‘obsolete and the new.’ Clin Exp Rheumatol 36 Suppl 112(3):215–221

    PubMed  Google Scholar 

  6. Mossel E, Arends S, van Nimwegen JF, Delli K, Stel AJ, Kroese FGM, Spijkervet FKL, Vissink A, Bootsma H, EULAR US-pSS study group (2018) Scoring hypoechogenic areas in one parotid and one submandibular gland increases feasibility of ultrasound in primary Sjögren’s syndrome. Ann Rheum Dis 77(4):556–562. https://doi.org/10.1136/annrheumdis-2017-211992

    Article  PubMed  Google Scholar 

  7. Luciano N, Ferro F, Bombardieri S, Baldini C (2018) Advances in salivary gland ultrasonography in primary Sjögren’s syndrome. Clin Exp Rheumatol 36 Suppl 114(5):159–164

    PubMed  Google Scholar 

  8. Bautista-Vargas M, Vivas AJ, Tobón GJ (2020) Minor salivary gland biopsy: its role in the classification and prognosis of Sjögren’s syndrome. Autoimmunity Rev 19(12):102690. https://doi.org/10.1016/j.autrev.2020.102690

    Article  Google Scholar 

  9. Le Goff M, Cornec D, Jousse-Joulin S, Guellec D, Costa S, Marhadour T, Le Berre R, Genestet S, Cochener B, Boisrame-Gastrin S, Renaudineau Y, Pers JO, Saraux A, Devauchelle-Pensec V (2017) Comparison of 2002 AECG and 2016 ACR/EULAR classification criteria and added value of salivary gland ultrasonography in a patient cohort with suspected primary Sjögren’s syndrome. Arthritis Res Ther 19(1):269. https://doi.org/10.1186/s13075-017-1475-x

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  10. Posso-Osorio I, Nieto-Aristizábal I, Soto D, Ariza C, Urbano M, Cañas CA, Echeverri A, Castillo A, Tobón GJ (2021) Validation and adaptation to Spanish of the EULAR Sjögren’s Syndrome Patient Reported Index (ESSPRI). Reumatologia clinica 17(7):388–391. https://doi.org/10.1016/j.reumae.2020.01.003

    Article  PubMed  Google Scholar 

  11. Kobayashi I, Okura Y, Ueki M, Tozawa Y, Takezaki S, Yamada M, Ariga T (2019) Evaluation of systemic activity of pediatric primary Sjögren’s syndrome by EULAR Sjögren’s syndrome disease activity index (ESSDAI). Mod Rheumatol 29(1):130–133. https://doi.org/10.1080/14397595.2018.1452174

    Article  PubMed  Google Scholar 

  12. Fana V, Dohn UM, Krabbe S, Terslev L (2021) Application of the OMERACT Grey-scale Ultrasound Scoring System for salivary glands in a single-centre cohort of patients with suspected Sjögren’s syndrome. RMD Open 7(2):e001516. https://doi.org/10.1136/rmdopen-2020-001516

    Article  PubMed  PubMed Central  Google Scholar 

  13. Zhang X, Feng R, Zhao J, Wang Y, He J, Liu L, Cheng Y, Yao H, Tang S, Chen J, Zhang S, Zhang Z, Wang Q, He J, Li Z (2021) Salivary gland ultrasonography in primary Sjögren’s syndrome from diagnosis to clinical stratification: a multicentre study. Arthritis Res Ther 23(1):305. https://doi.org/10.1186/s13075-021-02689-3

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  14. Finzel S, Jousse-Joulin S, Costantino F, Hánová P, Hocevar A, Iagnocco A, Keen H, Naredo E, Ohrndorf S, Schmidt WA, D’Agostino MA, Terslev L, Bruyn GA (2021) Patient-based reliability of the Outcome Measures in Rheumatology (OMERACT) ultrasound scoring system for salivary gland assessment in patients with Sjögren’s syndrome. Rheumatology (Oxford) 60(5):2169–2176. https://doi.org/10.1093/rheumatology/keaa471

    Article  CAS  PubMed  Google Scholar 

  15. Delli K, van Ginkel MS, Vissink A, Stel AJ, van der Vegt B, Spijkervet FKL, Kroese FGM, Arends S, Bootsma H (2022) Can salivary gland ultrasonography replace salivary gland biopsy in the diagnosis of Sjögren’s syndrome? Clin Exp Rheumatol 40(12):2443–2449

    PubMed  Google Scholar 

  16. Mossel E, van Nimwegen JF, Stel AJ, Wijnsma RF, Delli K, van Zuiden GS, Olie L, Vehof J, Los LI, Vissink A, Kroese FGM, Arends S, Bootsma H (2021) Clinical phenotyping of primary Sjögren syndrome patients using salivary gland ultrasonography: data from the RESULT cohort. J Rheumatol 48(5):717–727. https://doi.org/10.3899/jrheum.200482

    Article  PubMed  Google Scholar 

  17. Al Tabaa O, Gouze H, Hamroun S, Bergé E, Belkhir R, Pavy S, Jousse-Joulin S, Mariette X (2021) Normal salivary gland ultrasonography could rule out the diagnosis of Sjögren’s syndrome in anti-SSA-negative patients with sicca syndrome. RMD Open 7(1):e001503. https://doi.org/10.1136/rmdopen-2020-001503

    Article  PubMed  PubMed Central  Google Scholar 

  18. 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 Musculoskeletal Dis 13:1759720X211010592. https://doi.org/10.1177/1759720X211010592

    Article  CAS  Google Scholar 

  19. Xu S, Luo J, Zhu C, Jiang J, Cheng H, Wang P, Hong J, Fang J, Pan J, Brown MA, Zhu X, Wang X (2021) Performance evaluation of multiple ultrasonographical methods for the detection of primary Sjögren’s syndrome. Front Immunol 12:777322. https://doi.org/10.3389/fimmu.2021.777322

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  20. Jousse-Joulin S, Gatineau F, Baldini C, Baer A, Barone F, Bootsma H, Bowman S, Brito-Zerón P, Cornec D, Dorner T, de Vita S, Fisher B, Hammenfors D, Jonsson M, Mariette X, Milic V, Nakamura H, Ng WF, Nowak E, Ramos-Casals M, … Devauchelle-Pensec V (2020). Weight of salivary gland ultrasonography compared to other items of the 2016 ACR/EULAR classification criteria for primary Sjögren’s syndrome. J Int Med, 287(2), 180–188. https://doi.org/10.1111/joim.12992

  21. Mossel E, Delli K, van Nimwegen JF, Stel AJ, Kroese FGM, Spijkervet FKL, Vissink A, Arends S, Bootsma H, & EULAR US-pSS Study Group (2017) Ultrasonography of major salivary glands compared with parotid and labial gland biopsy and classification criteria in patients with clinically suspected primary Sjögren’s syndrome. Ann Rheumatic Dis 76(11):1883–1889. https://doi.org/10.1136/annrheumdis-2017-211250

    Article  CAS  Google Scholar 

  22. Jousse-Joulin S, D’Agostino MA, Nicolas C, Naredo E, Ohrndorf S, Backhaus M, Tamborrini G, Chary-Valckenaere I, Terslev L, Iagnocco A, Collado P, Hernández-Díaz C, Gandjbakhch F, Schmidt WA, Filippou G, Dejaco C, Stradner MH, Mortada MA, Hočevar A, Chrysidis S, … Bruyn GA (2019). Video clip assessment of a salivary gland ultrasound scoring system in Sjögren’s syndrome using consensual definitions: an OMERACT ultrasound working group reliability exercise. Ann Rheumatic Dis, 78 (7), 967–973. https://doi.org/10.1136/annrheumdis-2019-215024

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Acknowledgements

The authors thank the Spanish Foundation of Rheumatology (FERBT2022) for providing medical writing/editorial assistance during the preparation of the manuscript.

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Authors and Affiliations

  1. Rheumatology Department, Hospital Universitario de Torrejón, Madrid, Spain

    Laura Barrio-Nogal & Luis Sala-Icardo

  2. Rheumatology Department, Hospital Universitario de La Paz, Madrid, Spain

    Marta Novella-Navarro

  3. Rheumatology Department, Hospital Universitario Príncipe de Asturias, Madrid, Spain

    Cristina Bohórquez Heras & Ana Pérez Gómez

  4. Rheumatology Department, Hospital Universitario Infanta Leonor, Madrid, Spain

    Enrique Calvo-Aranda

Authors
  1. Laura Barrio-Nogal
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  2. Marta Novella-Navarro
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  3. Cristina Bohórquez Heras
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  4. Luis Sala-Icardo
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  5. Enrique Calvo-Aranda
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  6. Ana Pérez Gómez
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Correspondence to Laura Barrio-Nogal.

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Barrio-Nogal, L., Novella-Navarro, M., Heras, C.B. et al. Ultrasonography in the diagnosis of suspected primary Sjögren’s syndrome and concordance with salivary gland biopsy: a Spanish single-center study. Clin Rheumatol 42, 2409–2417 (2023). https://doi.org/10.1007/s10067-023-06618-4

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  • DOI: https://doi.org/10.1007/s10067-023-06618-4

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