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Open Access 01-12-2017 | Research article

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

Authors: Maëlle Le Goff, Divi Cornec, Sandrine Jousse-Joulin, Dewi Guellec, Sebastian Costa, Thierry Marhadour, Rozenn Le Berre, Steeve Genestet, Béatrice Cochener, Sylvie Boisrame-Gastrin, Yves Renaudineau, Jacques-Olivier Pers, Alain Saraux, Valérie Devauchelle-Pensec

Published in: Arthritis Research & Therapy | Issue 1/2017

Abstract

Background

The objective was to evaluate concordance between 2002 American-European Consensus Group (AECG) and 2016 American College of Rheumatology (ACR)/European League Against Rheumatism (EULAR) classification criteria for primary Sjögren’s syndrome (pSS) and to assess how salivary gland ultrasonography (SGUS) might improve the classification of patients.

Methods

Patients with suspected pSS underwent a standardised evaluation, including SGUS, at inclusion into the single-centre Brittany DIApSS cohort. Agreement between the two criteria sets was assessed using Cohen’s κ coefficient. Characteristics of discordantly categorised patients were detailed.

Results

We prospectively included 290 patients between 2006 and 2016, among whom 125 (43%) met ACR/EULAR criteria and 114 (39%) also met AECG criteria; thus, 11 (4%) patients fulfilled only ACR/EULAR, no patients AECG only, and 165 (57%) patients neither criteria set. Concordance was excellent (κ = 0.92). Compared to patients fulfilling both criteria sets, the 11 patients fulfilling only ACR/EULAR criteria had similar age and symptom duration but lower frequencies of xerophthalmia and xerostomia (p < 0.01 for each) and salivary gland dysfunction (p < 0.01); most had systemic involvement (91%), including three (27%) with no sicca symptoms; 91% had abnormal salivary gland biopsy and 46% anti-Sjögren's-syndrome-related antigen A (anti-SSA); 64% were diagnosed with pSS by the physician. SGUS was abnormal in 12% of the 165 patients fulfilling no criteria set. Including SGUS among the ACR/EULAR criteria increased sensitivity from 87.4% to 91.1% when physician diagnosis was the reference standard.

Conclusions

Agreement between AECG and ACR/EULAR criteria sets is excellent. ACR/EULAR criteria are slightly more sensitive and classified some patients without sicca symptoms as having pSS. Including SGUS in the ACR/EULAR criteria may further improve their sensitivity.

Brito-Zerón P, Baldini C, Bootsma H, Bowman SJ, Jonsson R, Mariette X, et al. Sjögren syndrome. Nat Rev Dis Primer. 2016;2:16047.CrossRef

Cornec D, Chiche L. Is primary Sjögren’s syndrome an orphan disease? A critical appraisal of prevalence studies in Europe. Ann Rheum Dis. 2015;74:e25.CrossRefPubMed

Maciel G, Crowson CS, Matteson EL, Cornec D. Prevalence of primary Sjögren’s syndrome in a population-based cohort in the United States. Arthritis Care Res (Hoboken). 2017;69(10):1612–1616.CrossRef

Brito-Zerón P, Acar-Denizli N, Zeher M, Rasmussen A, Seror R, Theander E, et al. Influence of geolocation and ethnicity on the phenotypic expression of primary Sjögren’s syndrome at diagnosis in 8310 patients: a cross-sectional study from the Big Data Sjögren Project Consortium. Ann Rheum Dis. 2017;76:1042–50.CrossRefPubMed

Maciel G, Crowson CS, Matteson EL, Cornec D. Incidence and mortality of physician-diagnosed primary Sjögren syndrome: time trends over a 40-year period in a population-based US cohort. Mayo Clin Proc. 2017;92(5):734–43.CrossRefPubMed

Cornec D, Devauchelle-Pensec V, Mariette X, Jousse-Joulin S, Berthelot J-M, Perdriger A, et al. Severe health-related quality-of-life impairment in active primary Sjögren’s syndrome is driven by patient-reported outcomes: data from a large therapeutic trial. Arthritis Care Res (Hoboken). 2017;69(4):528–535.CrossRef

Nocturne G, Mariette X. Advances in understanding the pathogenesis of primary Sjögren’s syndrome. Nat Rev Rheumatol. 2013;9:544–56.CrossRefPubMed

Saraux A, Pers J-O, Devauchelle-Pensec V. Treatment of primary Sjögren syndrome. Nat Rev Rheumatol. 2016;12:456–71.CrossRefPubMed

Vitali C, Bombardieri S, Jonsson R, Moutsopoulos HM, Alexander EL, Carsons SE, et al. Classification criteria for Sjögren’s syndrome: a revised version of the European criteria proposed by the American-European Consensus Group. Ann Rheum Dis. 2002;61:554–8.CrossRefPubMedPubMedCentral

10.

Daniels TE, Cox D, Shiboski CH, Schiødt M, Wu A, Lanfranchi H, et al. Associations between salivary gland histopathologic diagnoses and phenotypic features of Sjögren’s syndrome (SS) among 1726 registry participants. Arthritis Rheum. 2011;63:2021–30.CrossRefPubMedPubMedCentral

11.

Shiboski SC, Shiboski CH, Criswell LA, Baer AN, Challacombe S, Lanfranchi H, et al. 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. 2012;64:475–87.CrossRef

12.

Vitali C, Bootsma H, Bowman SJ, Dorner T, Gottenberg J-E, Mariette X, et al. Classification criteria for Sjogren’s syndrome: we actually need to definitively resolve the long debate on the issue. Ann Rheum Dis. 2013;72:476–8.CrossRefPubMed

13.

Cornec D, Saraux A, Cochener B, Pers J-O, Jousse-Joulin S, Renaudineau Y, et al. Level of agreement between 2002 American–European Consensus Group and 2012 American College of Rheumatology classification criteria for Sjögren’s syndrome and reasons for discrepancies. Arthritis Res Ther. 2014;16:R74.CrossRefPubMedPubMedCentral

14.

Rasmussen A, Ice JA, Li H, Grundahl K, Kelly JA, Radfar L, et al. Comparison of the American-European Consensus Group Sjögren’s syndrome classification criteria to newly proposed American College of Rheumatology criteria in a large, carefully characterised sicca cohort. Ann Rheum Dis. 2014;73:31–8.CrossRefPubMed

15.

Shiboski CH, Shiboski SC, Seror R, Criswell LA, Labetoulle M, Lietman TM, et al. 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. 2017;69:35–45.CrossRefPubMed

16.

17.

Seror R, Theander E, Brun JG, Ramos-Casals M, Valim V, Dörner T, et al. Validation of EULAR primary Sjögren’s syndrome disease activity (ESSDAI) and patient indexes (ESSPRI). Ann Rheum Dis. 2015;74:859–66.CrossRefPubMed

18.

Seror R, Ravaud P, Bowman SJ, Baron G, Tzioufas A, Theander E, et al. EULAR Sjogren’s syndrome disease activity index: development of a consensus systemic disease activity index for primary Sjogren’s syndrome. Ann Rheum Dis. 2010;69:1103–9.CrossRefPubMed

19.

Fisher BA, Brown RM, Bowman SJ, Barone F. A review of salivary gland histopathology in primary Sjögren’s syndrome with a focus on its potential as a clinical trials biomarker. Ann Rheum Dis. 2015;74(9):1645–50.CrossRefPubMed

20.

Fisher BA, Jonsson R, Daniels T, Bombardieri M, Brown RM, Morgan P, et al. Standardisation of labial salivary gland histopathology in clinical trials in primary Sjögren’s syndrome. Ann Rheum Dis. 2017;76(7):1161–1168.CrossRefPubMedPubMedCentral

21.

Navazesh M, Kumar SKS, University of Southern California School of Dentistry. Measuring salivary flow: challenges and opportunities. J Am Dent Assoc. 2008;139(Suppl):35S–40S.CrossRefPubMed

22.

Whitcher JP, Shiboski CH, Shiboski SC, Heidenreich AM, Kitagawa K, Zhang S, et al. A simplified quantitative method for assessing keratoconjunctivitis sicca from the Sjögren’s Syndrome International Registry. Am J Ophthalmol. 2010;149:405–15.CrossRefPubMed

23.

Cornec D, Jousse-Joulin S, Pers J-O, Marhadour T, Cochener B, Boisramé-Gastrin S, et al. Contribution of salivary gland ultrasonography to the diagnosis of Sjögren’s syndrome: toward new diagnostic criteria? Arthritis Rheum. 2013;65:216–25.CrossRefPubMed

24.

Cornec D, Jousse-Joulin S, Marhadour T, Pers J-O, Boisramé-Gastrin S, Renaudineau Y, et al. Salivary gland ultrasonography improves the diagnostic performance of the 2012 American College of Rheumatology classification criteria for Sjögren’s syndrome. Rheumatol Oxf Engl. 2014;53:1604–7.CrossRef

25.

Baldini C, Luciano N, Tarantini G, Pascale R, Sernissi F, Mosca M, et al. Salivary gland ultrasonography: a highly specific tool for the early diagnosis of primary Sjögren’s syndrome. Arthritis Res Ther. 2015;17:146.CrossRefPubMedPubMedCentral

26.

Luciano N, Baldini C, Tarantini G, Ferro F, Sernissi F, Varanini V, et al. Ultrasonography of major salivary glands: a highly specific tool for distinguishing primary Sjögren’s syndrome from undifferentiated connective tissue diseases. Rheumatol Oxf Engl. 2015;54:2198–204.

27.

Hammenfors DS, Brun JG, Jonsson R, Jonsson MV. Diagnostic utility of major salivary gland ultrasonography in primary Sjögren’s syndrome. Clin Exp Rheumatol. 2015;33:56–62.PubMed

28.

Jousse-Joulin S, Milic V, Jonsson MV, Plagou A, Theander E, Luciano N, et al. Is salivary gland ultrasonography a useful tool in Sjögren’s syndrome? A systematic review. Rheumatol Oxf Engl. 2016;55:789–800.CrossRef

29.

Cornec D, Saraux A, Jousse-Joulin S, Pers J-O, Boisramé-Gastrin S, Renaudineau Y, et al. The differential diagnosis of dry eyes, dry mouth, and parotidomegaly: a comprehensive review. Clin Rev Allergy Immunol. 2015;49:278–87.CrossRefPubMed

30.

Le Gall M, Cornec D, Pers J-O, Saraux A, Jousse-Joulin S, Cochener B, et al. A prospective evaluation of dental and periodontal status in patients with suspected Sjögren’s syndrome. Jt Bone Spine Rev Rhum. 2016;83:235–6.CrossRef

31.

van Bijsterveld OP. Diagnostic tests in the Sicca syndrome. Arch Ophthalmol. 1969;82:10–4.CrossRefPubMed

32.

Cornec D, Saraux A, Pers J-O, Jousse-Joulin S, Marhadour T, Roguedas-Contios A-M, et al. Diagnostic accuracy of blood B-cell subset profiling and autoimmunity markers in Sjögren’s syndrome. Arthritis Res Ther. 2014;16:R15.CrossRefPubMedPubMedCentral

33.

Capaldo C, Carvajal Alegria G, Cornec D, Jousse-Joulin S, Devauchelle-Pensec V, Renaudineau Y. The active immunological profile in patients with primary Sjögren’s syndrome is restricted to typically encountered autoantibodies. Clin Exp Rheumatol. 2016;34:722.PubMed

34.

Cornec D, Devauchelle-Pensec V, Saraux A, Jousse-Joulin S. [Clinical usefulness of salivary gland ultrasonography in Sjögren’s syndrome: where are we now?]. Rev Med Interne. 2016;37:186–94. Fondée Par Société Natl Francaise Médecine Interne.CrossRefPubMed

35.

Tezcan ME, Kucuk H, Goker B. ACR/EULAR Sjögren classification criteria may not be adequate for extraglandular disease and necessitates defining “seronegative Sjögren’s syndrome.” Arthritis Rheumatol. 2017;69(6):1341-1342

36.

Vitali C, Scofield H, Shiboski SC, Seror R, Criswell LA, Labetoulle M, et al. Authors’ response to Tezcan and Colleagues’ letter to the editor. Arthritis Rheumatol. 2017;69(6):1342.CrossRefPubMed

37.

Baer AN, McAdams DeMarco M, Shiboski SC, Lam MY, Challacombe S, Daniels TE, et al. The SSB-positive/SSA-negative antibody profile is not associated with key phenotypic features of Sjögren’s syndrome. Ann Rheum Dis. 2015;74:1557–61.CrossRefPubMed

38.

Gazeau P, Cornec D, Jousse-Joulin S, Guellec D, Saraux A, Devauchelle-Pensec V. Time-course of ultrasound abnormalities of major salivary glands in suspected Sjögren’s syndrome. Joint Bone Spine. 2017. doi:10.1016/j.jbspin.2017.02.007. [Epub ahead of print].

39.

Cornec D, Jousse-Joulin S, Costa S, Marhadour T, Marcorelles P, Berthelot J-M, et al. High-grade salivary-gland involvement, assessed by histology or ultrasonography, is associated with a poor response to a single rituximab course in primary Sjögren’s syndrome: data from the TEARS randomized trial. PLoS One. 2016;11:e0162787.CrossRefPubMedPubMedCentral

40.

Jousse-Joulin S, Devauchelle-Pensec V, Cornec D, Marhadour T, Bressollette L, Gestin S, et al. Brief Report: Ultrasonographic assessment of salivary gland response to rituximab in primary Sjögren’s syndrome. Arthritis Rheumatol. 2015;67:1623–8.CrossRefPubMed

41.

Jousse-Joulin S, Nowak E, Cornec D, Brown J, Carr A, Carotti M, et al. Salivary gland ultrasound abnormalities in primary Sjögren’s syndrome: consensual US-SG core items definition and reliability. RMD Open. 2017;3:e000364.CrossRefPubMedPubMedCentral

42.

Delli K, Arends S, van Nimwegen JF, Dijkstra PU, Stel AJ, Spijkervet FKL, et al. Ultrasound of the major salivary glands is a reliable imaging technique in patients with clinically suspected primary Sjögren’s syndrome. Ultraschall Med. 2017. doi:10.1055/s-0043-104631. [Epub ahead of print]

43.

Mossel E, Delli K, van Nimwegen JF, Stel AJ, Kroese FGM, Spijkervet FKL, et al. 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. 2017;76(11):1883–9.CrossRefPubMed

44.

Carvajal Alegria G, Costa S, Jousse-Joulin S, Marcorelles P, Pers J-O, Saraux A, et al. What is the agreement between pathological features of parotid gland and labial salivary gland biopsies? Ann Rheum Dis. 2017. doi:10.1136/annrheumdis-2017-212289. [Epub ahead of print].

45.

Mossel E, Delli K, van Nimwegen JF, Stel AJ, Haacke EA, Kroese FGM, et al. The parotid gland connection: ultrasound and biopsies in primary Sjögren’s syndrome. Ann Rheum Dis. 2017. doi:10.1136/annrheumdis-2017-212331. [Epub ahead of print].

46.

Tsuboi H, Hagiwara S, Asashima H, Takahashi H, Hirota T, Noma H, et al. Comparison of performance of the 2016 ACR-EULAR classification criteria for primary Sjögren’s syndrome with other sets of criteria in Japanese patients. Ann Rheum Dis. 2017;76(12):1980–5.CrossRefPubMed

47.

Fujibayashi T, Sugai S, Miyasaka N, Hayashi Y, Tsubota K. Revised Japanese criteria for Sjögren’s syndrome (1999): availability and validity. Mod Rheumatol. 2004;14:425–34.CrossRefPubMed

Title: 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
Authors: Maëlle Le Goff
Divi Cornec
Sandrine Jousse-Joulin
Dewi Guellec
Sebastian Costa
Thierry Marhadour
Rozenn Le Berre
Steeve Genestet
Béatrice Cochener
Sylvie Boisrame-Gastrin
Yves Renaudineau
Jacques-Olivier Pers
Alain Saraux
Valérie Devauchelle-Pensec
Publication date: 01-12-2017
Publisher: BioMed Central
Published in: Arthritis Research & Therapy / Issue 1/2017
Electronic ISSN: 1478-6362
DOI: https://doi.org/10.1186/s13075-017-1475-x

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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

Abstract

Background

Methods

Results

Conclusions

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