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Ultrasound salivary gland involvement in Sjogren’s syndrome vs. other connective tissue diseases: is it autoantibody and gland dependent?

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Abstract

Abstract

This study aims to investigate ultrasound (US) findings on salivary glands (SG) in patients with Sjögren syndrome (SS) vs. other connective tissue diseases (CTDs) and to assess the relationship of SGUS abnormalities with autoantibody profile in both groups. We enrolled 81 patients, 45 diagnosed with SS (39 with primary SS, 6 with secondary SS) and 36 diagnosed with other CTDs. All patients underwent a prospective evaluation of sicca symptoms, a Schirmer’s test, and a B-mode US assessment of the parotid and submandibular glands, all blinded to the diagnosis. Each SG was semi-quantitatively scored 0–3; a grade ≥ 2 was considered pathological. SGUS involvement was classified as normal or pathological at the patient level and for each pair at the gland level. In addition, a total SGUS score of 0–12 and a parotid/submandibular score of 0–6 were calculated for each patient. Autoimmunity laboratory data were also obtained. All SGUS scores were higher in SS patients than in those with CTD (p < 0.001) and significantly more SS patients showed a pathological global (p < 0.001), parotid (p < 0.001), or submandibular (p = 0.001) US score compared with CTD patients. In SS patients, the presence of autoantibodies was significantly associated with pathological SGUS and higher scores, particularly at the parotid level, while in CTD patients, xerostomia and a pathological Schirmer’s test were associated with pathological US and higher scores at the submandibular level (p < 0.05). SGUS showed a different grade of abnormality, site involvement, and associated autoantibody profile in SS patients as compared with other CTD.

Key Points

Patients with SS and other CTDs showed different grades of SGUS abnormality.

Patients with SS and other CTDs showed different gland involvement and associated autoantibody profiles.

Anti-Ro60 and anti-Ro52 Ro60 positivity were associated with the severity of parotid involvement in SS patients.

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References

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

    Article  Google Scholar 

  2. Cornec D, Devauchelle-Pensec V, Mariette X, Jousse-Joulin S, Berthelot JM, Perdriger A, Puéchal X, le Guern V, Sibilia J, Gottenberg JE, Chiche L, Hachulla E, Yves Hatron P, Goeb V, Hayem G, Morel J, Zarnitsky C, Dubost JJ, Saliou P, Pers JO, Seror R, Saraux A (2017) Severe health-related quality of life impairment in active primary Sjögren’s syndrome and patient-reported outcomes: data from a large therapeutic trial. Arthritis Care Res (Hoboken) 69:528–535

    Article  Google Scholar 

  3. Hocevar A, Ambrozic A, Rozman B, Kveder T, Tomsic M (2005) Ultrasonographic changes of major salivary glands in primary Sjögren’s syndrome. Diagnostic value of a novel scoring system. Rheumatology (Oxford) 44:768–772

    Article  CAS  Google Scholar 

  4. Wernicke D, Hess H, Gromnica-Ihle E, Krause A, Schmidt WA (2008) Ultrasonography of salivary glands—a highly specific imaging procedure for diagnosis of Sjögren’s syndrome. J Rheumatol 35:285–293

    PubMed  Google Scholar 

  5. Milic VD, Petrovic RR, Boricic IV, Marinkovic-Eric J, Radunovic GL, Jeremic PD et al (2009) Diagnostic value of salivary gland ultrasonographic scoring system in primary Sjögren’s syndrome: a comparison with scintigraphy and biopsy. J Rheumatol 36:1495–1500

    Article  Google Scholar 

  6. Salaffi F, Argalia G, Carotti M, Giannini FB, Palombi C (2000) Salivary gland ultrasonography in the evaluation of primary Sjögren’s syndrome. Comparison with minor salivary gland biopsy. J Rheumatol 27:1229–1236

    CAS  PubMed  Google Scholar 

  7. Astorri E, Sutcliffe N, Richards PS, Suchak K, Pitzalis C, Bombardieri M, Tappuni AR (2016) Ultrasound of the salivary glands is a strong predictor of labial gland biopsy histopathology in patients with sicca symptoms. J Oral Pathol Med 45:450–454

    Article  CAS  Google Scholar 

  8. 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 Rheum Dis 76:1883–1889

    Article  CAS  Google Scholar 

  9. 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 47:303–310

    Article  Google Scholar 

  10. Jousse-Joulin S, Milic V, Jonsson MV, Plagou A, Theander E, Luciano N, Rachele P, Baldini C, Bootsma H, Vissink A, Hocevar A, de Vita S, Tzioufas AG, Alavi Z, Bowman SJ, Devauchelle-Pensec V, on behalf of the US-pSS Study Group (2016) Is salivary gland ultrasonography a useful tool in Sjögren’s syndrome? A systematic review. Rheumatology 55:789–800

    Article  Google Scholar 

  11. Luciano N, Baldini C, Tarantini G, Ferro F, Sernissi F, Varanini V, Donati V, Martini D, Mosca M, Caramella D, Bombardieri S (2015) Ultrasonography of mayor salivary glands: a highly specific tool for distinguishing primary Sjögren’s syndrome from undifferentiated connective tissue diseases. Rheumatology (Oxford) 54:2198–2204

    CAS  Google Scholar 

  12. De Vita S, Lorenzon G, Rossi G, Sabella M, Fossaluzza V et al (1992) Salivary gland echography in primary and secondary Sjögren’s syndrome. Clin Exp Rheumatol 10:351–356

    PubMed  Google Scholar 

  13. Couderc M, Tournadre A, Mathieu S, Pereira B, Soubrier M, Dubost JJ. Do the salivary glands of patients with systemic sclerosis show ultrasonographic modifications suggestive of Sjögren’s syndrome? Ann Rheum Dis 2019, Jun 12.pii: annrheumdis-2019-215777. https://doi.org/10.1136/annrheumdis-2019-215777

  14. Shibosky CH, Shibosky SC, Seror R, Criswell LA, Labetoulle M, Lietman TM, International Sjögren’s Syndrome Criteria Working Group et al (2017) 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. Ann Rheum Dis 76:9–16

    Article  Google Scholar 

  15. Petri M, Orbai AM, Alarcon GS, Gordon C, Merrill JT, Fortin PR et al (2012) Derivation and validation of systemic lupus international collaborating clinics classification criteria for systemic lupus erythematosus. Arthritis Rheum 64:2677–2686

    Article  Google Scholar 

  16. van den Hoogen F, Khanna D, Fransen J, Johnson SR, Baron M, Tyndall A, Matucci-Cerinic M, Naden RP, Medsger TA Jr, Carreira PE, Riemekasten G, Clements PJ, Denton CP, Distler O, Allanore Y, Furst DE, Gabrielli A, Mayes MD, van Laar JM, Seibold JR, Czirjak L, Steen VD, Inanc M, Kowal-Bielecka O, Müller-Ladner U, Valentini G, Veale DJ, Vonk MC, Walker UA, Chung L, Collier DH, Ellen Csuka M, Fessler BJ, Guiducci S, Herrick A, Hsu VM, Jimenez S, Kahaleh B, Merkel PA, Sierakowski S, Silver RM, Simms RW, Varga J, Pope JE (2013) 2013 classification criteria for systemic sclerosis: an American college of rheumatology/European league against rheumatism collaborative initiative. Ann Rheum Dis 72:1747–1755

    Article  Google Scholar 

  17. Mosca M, Neri R, Bombardieri S (1999) Undifferentiated connective tissue diseases (UCTD): a review of the literature and a proposal for preliminary classification criteria. Clin Exp Rheumatol 17:615–620

    CAS  PubMed  Google Scholar 

  18. Sharp GC, Irvin WS, Tan EM, Gould RG, Holman HR (1972) Mixed connective tissue disease-an apparently distinct rheumatic disease syndrome associated with a specific antibody to an extractable nuclear antigen (ENA). Am J Med 52:148–159

    Article  CAS  Google Scholar 

  19. Vitali C, Bombardieri S, Jonsson R, Moutsopoulos HM, Alexander EL, Carsons SE, Daniels TE, Fox PC, Fox RI, Kassan SS, Pillemer SR, Talal N, Weisman MH, European Study Group on Classification Criteria for Sjögren’s Syndrome (2002) Classification criteria for Sjögren’s syndrome: a revised version of the European criteria proposed by the American-European Consensus Group. Ann Rheum Dis 61:554–558

    Article  CAS  Google Scholar 

  20. Möller I, Janta I, Backhaus M, Ohrndorf S, Bong DA, Martinoli C, Filippucci E, Sconfienza LM, Terslev L, Damjanov N, Hammer HB, Sudol-Szopinska I, Grassi W, Balint P, Bruyn GAW, D’Agostino MA, Hollander D, Siddle HJ, Supp G, Schmidt WA, Iagnocco A, Koski J, Kane D, Fodor D, Bruns A, Mandl P, Kaeley GS, Micu M, Ho C, Vlad V, Chávez-López M, Filippou G, Cerón CE, Nestorova R, Quintero M, Wakefield R, Carmona L, Naredo E (2017) The 2017 EULAR standardised procedures for ultrasound imaging in rheumatology. Ann Rheum Dis 76:1974–1979

    Article  Google Scholar 

  21. Damjanov N, Milic V, Nieto-González JC, Janta I, Martínez-Estupiñan L, Serrano B, Mata C, Montoro M, Stanciu D, Marinković-Erić J, López-Longo FJ, Carreño L, Naredo E (2016) Multiobserver reliability of ultrasound assessment of salivary glands in patients with established primary Sjögren syndrome. J Rheumatol 43:1858–1863

    Article  Google Scholar 

  22. Jousse-Joulin S, Nowak E, Cornec D, Brown J, Carr A, Carotti M, Fisher B, Fradin J, Hocevar A, Jonsson MV, Luciano N, Milic V, Rout J, Theander E, Stel A, Bootsma H, Vissink A, Baldini C, Baer A, Ng WF, Bowman S, Alavi Z, Saraux A, Devauchelle-Pensec V (2017) Salivary gland ultrasound abnormalities in primary Sjögren’s syndrome: consensual US-SG core items definition and reliability. RMD Open 3:e000364

    Article  Google Scholar 

  23. Jousse-Joulin S, D’agostino MA, Nicolas C, Naredo E, Ohrndorf S, Backhaus M et al (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 Rheum Dis 78:967–973

    Article  Google Scholar 

  24. Nieto-González JC, Ovalles-Bonilla JG, Estrada E, Serrano-Benavente B, Martínez-Barrio J, González-Fernández CM, at al. J Int Med Res 2018 Jan 1:300060518767031.https://doi.org/10.1177/0300060518767031.

  25. Inanc N, Şahinkaya Y, Mumcu G, Türe Özdemir F, Paksoy A, Ertürk Z, et al. Evaluation of salivary gland ultrasonography in primary Sjögren's syndrome: does it reflect clinical activity and outcome of the disease?. Clin Exp Rheumatol 2019;37 Suppl 118(3):140-145.

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Acknowledgments

The authors would like to thank the Spanish Society of Rheumatology for their help in the English language editing throughout the manuscript preparation process.

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This study has no financial support.

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Study design: E.N.; GMC. LP. Acquisition of data: GMC. LP; E.N; O.SP.; MJ. MB.; F. RB.; S. R.; PE. B. Analysis and interpretation of data: GMC. LP; E.N.; O.SP.; A.A.; MJ. MB.; F. RB.; S. R.; PE. B.; I. MF.; J.G.; R.G.; G. H-B. Manuscript preparation: E.N.; GMC. LP; J.G. Manuscript critical revision: GMC. LP; E.N; O.SP.; A.A.; MJ. MB.; F. RB.; S. R.; PE. B.; I. MF.; J.G.; R.G.; G. H-B. Final approval: GMC. LP; E.N.; O.SP.; A.A.; MJ. MB.; F. RB.; S. R.; PE. B.; I. MF.; J.G.; R.G.; G. H-B.

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Correspondence to Esperanza Naredo.

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La Paglia, G.M.C., Sanchez-Pernaute, O., Alunno, A. et al. Ultrasound salivary gland involvement in Sjogren’s syndrome vs. other connective tissue diseases: is it autoantibody and gland dependent?. Clin Rheumatol 39, 1207–1215 (2020). https://doi.org/10.1007/s10067-019-04780-2

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