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Abstract
Background Diagnosis of SS is a complex task, as no symptom or test is unique to this syndrome. The American- European Consensus Group (AECG 2002) and the American-European classification criteria of 2016 (ACR/EULAR 2016) emerged through a search for consensus. This study aims to assess the prevalence of Sjögren’s Syndrome (SS) in patients with Systemic Lupus Erythematosus (SLE), according to AECG 2002 and ACR-EULAR 2016 classifications, as well as clinical and histopathological features in this overlap. To date, there is no study that has evaluated SS in SLE, using the two current criteria. Methods This cross-sectional study evaluated 237 SLE patients at the outpatient rheumatology clinic between 2016 and 2018. Patients were submitted to a dryness questionnaire, whole unstimulated salivary flow ( WUSF), “Ocular Stain- ing Score” (OSS), Schirmer’s test I (ST-I), and labial salivary gland biopsy (LSGB). Results After verifying inclusion and exclusion criteria, a total of 117 patients were evaluated, with predominance of females (94%) and mixed ethnicity (49.6%). The prevalence of SS was 23% according to AECG 2002 and 35% to ACR- EULAR 2016. Kappa agreement between AECG 2002 and ACR-EULAR 2016 were 0.7 (p < 0.0001). After logistic regres- sion, predictors for SS were: anti/Ro (OR = 17.86, p < 0.05), focal lymphocytic sialadenitis (OR = 3.69, p < 0.05), OSS ≥ 5 (OR = 7.50, p < 0.05), ST I positive (OR = 2.67, p < 0.05), and WUSF ≤ 0.1 mL/min (OR = 4.13, p < 0.05). Conclusion The prevalence of SS in SLE was 23% (AECG 2002) and 35% (ACR-EULAR 2016). The presence of glandular dysfunction, focal lymphocytic sialadenitis, and anti/Ro were predictors of SS in SLE. The greatest advantage of the new ACR-EULAR 2016 criteria is to enable an early diagnosis and identify the overlapping of these two diseases. ACR- EULAR 2016 criteria is not yet validated for secondary SS and this study is a pioneer in investigating prevalence based on the new criteria. Keywords Systemic lupus erythematosus, Sjögren’s syndrome, Classification criteria, ACR-EULAR 2016, Prevalence, Labial salivary gland biopsy *Correspondence: Valéria Valim val.valim@gmail.com Full list of author information is available at the end of the article © The Author(s) 2023. Open Access This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article’s Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article’s Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http:// creat iveco mmons. org/ licen ses/ by/4. 0/. Gianordoli et al. Advances in Rheumatology (2023) 63:11 Page 2 of 8 not performed in all patients, which makes the differen - Introduction tial diagnosis difficult, strengthening the need for a con - Systemic Lupus Erythematosus (SLE) and Sjögren’s Syn- sensus regarding the diagnostic and classification criteria drome (SS) are similar diseases, in clinical, laboratory, for SS in the context of other autoimmune diseases. It is genetic, and pathophysiological aspects [1]. Furthermore, noteworthy that there is no study that has evaluated SS they can overlap, occurring more frequently in early stage in SLE, using the two current criteria, including salivary of the disease [2]. Patients who present an overlap of the gland biopsy, and considering systemic manifestations as two diseases are, in fact, a subgroup with clinical charac- criteria for screening for SS. teristics and prognosis different from those with isolated The present study aims to assess the frequency of SS. This characterization can determine early interven - Sjögren’s Syndrome in patients with Systemic Lupus Ery- tion, with individualized treatment, preventing possible thematosus using the new ACR-EULAR 2016 criteria complications. compared to the 2002 American-European Consensus SLE is a chronic autoimmune inflammatory disease, Group criteria. with a wide spectrum of clinical manifestations, with- out periods of remission and activity, with lower over- Materials and methods all survival when compared to general population [3]. This is a cross-sectional and uncontrolled study of The distribution of the disease is universal, in USA, the patients diagnosed with SLE included from August 2016 prevalence varies from 14.5 to 50.8 cases/100,000 inhab- to August 2018. Patients were sequentially (convenience itants [4]. In Brazil, comparing northern and southern- sample) recruited from the rheumatology outpatient most regions, they estimated the incidence of 8.7/100,000 clinic of the University Hospital of Federal University of inhabitants in north of the country (tropical region), Espírito Santo (HUCAM-UFES/EBSERH). while in south (lower latitude), the incidence of SLE was The inclusion criteria were: patients with SLE classified 4.8/100,000 inhabitants/year [5], similar to Sweden [6] according to the SLICC (Systemic Lupus International and United Kingdom [7]. Collaborating Clinics) 2012 and/or ACR (American Col- SS is a chronic, autoimmune syndrome characterized lege of Rheumatology Classification) 1982 criteria. The morphologically by lymphocyte infiltration in salivary exclusion criteria were age under 18 years old, C hepa- and lacrimal glands, leading to reduction in tears and titis, AIDS, lymphoma, graft-host disease, sarcoidosis, saliva [8]. The clinical scenario is based on the classic HyperIgG4 syndrome, overlap with connective tissue triad: dryness, pain, and fatigue, but around 50% of cases diseases, pregnancy, head and neck radiotherapy in the can present systemic manifestations [8]. Data from a Bra- past, and patients on cyclophosphamide or methylpred- zilian population study showed that the prevalence of nisolone pulse therapy. primary SS (SSp) was 0.17% [9]. All patients were submitted to dryness question- Diagnosis of SS is a complex task, as no symptom or naire. Those who had symptoms of dryness or anti/ test is unique to this syndrome. The American-European Ro were submitted to glandular function evaluation by Consensus Group (AECG 2002) and the American-Euro- whole unstimulated salivary flow (WUSF) measurement, pean classification criteria of 2016 (ACR/EULAR 2016) Schirmer’s test I (ST I), lissamine green, and fluorescein emerged through a search for consensus, which performs test. Criteria for performing labial salivary gland biopsy a broader screening of patients to be submitted to this (LSGB) were: salivary and/or lacrimal dysfunction or classification, based on objective tests. positive anti/Ro or systemic manifestation according to In a prospective cohort study, it was found that approx- ESSDAI. imately half of the patients with SLE had manifestations Classification criteria were based on the 2002 Ameri - of dryness and fatigue and 11% had diagnosis of associ- can-European Consensus Group (AECG) consensus, ated SS [10]. The prevalence of SS is possibly underesti - which assesses ocular and oral symptoms, ocular and oral mated and could be diagnosed if patients with dryness objective tests, minor salivary gland histopathology, and and common systemic manifestations were evaluated the presence of autoantibodies. In addition, the new cri- with objective tests and, when necessary, labial salivary teria of the American College of Rheumatology and the biopsy. European League Against Rheumatism (ACR-EULAR) Few studies have assessed prevalence of SS in SLE, 2016 were used to classify SS, including the following among which it is noted that the prevalence is quite items: the presence of focal lymphocytic sialadenitis variable, according to the classification criteria used and with a focal score ≥ 1 (3 points), presence of anti/Ro (3 sample studied, ranging from 6.5% to 32.4% [1, 11–17]. In points), Schirmer test I (ST-I) ≤ 5 mm/5 min (1 point), a meta-analysis, Alani et al. (2017) demonstrated a preva- ocular surface staining score (or van Bijsterveld score) ≥ 5 lence of SS between 5 and 22%, recommending investi- (1 point) and unstimulated salivary flow ≤ 0.1 ml/min (1 gation of SS in SLE with dryness. However, a biopsy was Gianor doli et al. Advances in Rheumatology (2023) 63:11 Page 3 of 8 point), being positive when result is ≥ 4 points. In SS/SLE anti/LA antibodies were performed using the ELISA patients, the ESSDAI instrument was applied to assess method (enzyme immunoassay). ANA was performed disease activity. using the indirect immunofluorescence method in The WUSF measurement procedure was performed human epithelial cells (Hep-2) and interpreted by an using the passive flow technique, for 15 min. All collected experienced examiner (MFB). The RF was performed by saliva was weighed on a calibrated precision scale equip- nephelometry. ment, brand BEL Engineering , mark 160, class II. A The specimen obtained from the LSGB was fixed in value ≤ 0.1 ml/min was considered positive. 10% formalin and processed in paraffin. Histological sec - The ST-I was performed after unstimulated salivary tions were stained using hematoxylin and eosin (H&E) flow in conjunctival sac in both eyes, for 5 min, using and evaluated under optical microscopy (OM) by an standardized paper filters (Whatman no. 41). This experienced pathologist (MCLFSS) (Fig. 2). method quantifies the tear and is considered normal The characteristics of the population were described when the moisture is > 15 mm. Values ≤ 5 mm in at least and compared. To verify the association between some one eye were considered positive [18]. qualitative variables in the study, the chi-square test or The ocular surface staining tests, lissamine green, and Fisher’s exact test were applied. fluorescein were performed without anesthetic eye drops, The Kolmogorov-Smirnoff test, Student’s t-test, and on a different day and after the ST-I (Fig. 1). The pattern the non-parametric Mann–Whitney test were used for of ocular surface impregnation (conjunctiva and cornea) continuous variables. In all analysis carried out, a signifi - was evaluated and scored according to the “Ocular Stain- cance level of 5% was considered. Kappa Index was used ing Score” (OSS) scale. The OSS ≥ 5 was considered posi- to evaluate agreement between AECG 2002 and ACR- tive [19]. EULAR 2016 classification criteria. All analyzes per - The LSGBs were performed by a trained rheumatolo - formed in the present study were obtained using the IBM gist using the 0.5–1.5 cm linear incision technique, with a SPSS 20.0 (IBM Corp.2011) statistical software. mental nerve block (EVS) [20]. The protocol was approved by Research Ethics Com - The autoantibodies for investigation of SLE/SS were mittee of the University Hospital of the Federal Univer- anti/Ro, anti/LA, Rheumatoid Factor (RF), and Anti- sity of Espírito Santo, on July 31, 2016 (approval number nuclear Autoantibody (ANA). Tests for anti/Ro and 1.655.292). Fig. 1 Ocular surface staining tests using Lissamine (a) and Fluorescein (b). Findings from a patient enrolled in the study (Courtesy of Dr. Fabiano Cade Jorge) Gianordoli et al. Advances in Rheumatology (2023) 63:11 Page 4 of 8 Fig. 2 a H&E 400 × lymphoepithelial lesion; b inflammatory focus H&E ×200. Findings from a patient enrolled in the study (photos provided by Dr. Maria Carmen L. F. Silva Santos) AECG 2002 and ACR-EULAR 2016 were 0.7 (p < 0.001). Table 1 Comparison of demographic variables in patients with There was no comparative statistical significance differ - systemic lupus erythematosus without (SS−) and with (SS+) ence between demographic characteristics and clinical Sjögren’s syndrome manifestations of SLE patients who met the 2016 cri- Variable Category SS− SS+ Total P teria but not the 2002 criteria vs SLE patients who only n (%) n (%) met the 2002 criteria. Race (n = 117) Brown 36 (47) 22 (54) 58 0.331 The patients were asked about symptoms of eye and White 21 (28) 9 (22) 30 oral dryness and others such as difficulty in swallowing Black 19 (25) 8 (20) 27 dry food, crying without tears, photophobia, visual blur- Indigenous 0 (0) 1 (2) 1 ring, frequent caries, dry skin, vaginal dryness, itchy skin, Yellow 0 (0) 1 (2) 1 and dryness of the nasal mucosa. The frequency of dry - Gender (n = 117) Feminine 69 (91) 41 (100) 110 0.094 ness symptoms was similar between patients with and Masculine 7 (9) 0 (0) 7 without SS. The sensation of sand in eyes, vaginal dry - Age Group (n = 117) 17–41 40 (53) 15 (37) 55 0.169 ness, and dry skin were more frequent in patients with SS 42–65 33 (43) 22 (54) 55 (p < 0.05) (Table 2). > 66 3 (4) 4 (10) 7 The results of objective tests of ocular and oral gland function and biopsy analysis in patients with lupus are detailed in Table 3, comparing SS− and SS+ groups. Patients with SLE/SS + showed moderate disease activ- Results ity as measured by EULAR Sjögren’s Syndrome Disease A total of 237 were approached to participate, accord- Activity Index (ESSDAI) 8.9 ± 7.6. ing to their medical visiting (convenience sample). After logistic regression, the predictors for SS were: Out of them, 120 patients were excluded due to non- presence of anti/Ro, with OR = 17.86 (6.7–47.6) p < 0.001; attendance for examinations, refusal to participate, the compatible LSGB, OR = 3.69 (1.8–7.3), p < 0.001; incomplete data, or death. In the end, 117 patients were OSS ≥ 5 OR = 7.50 (2.6–21.7), p < 0.001; ST I OR = 2.67 included in the analyses. (1.028–6.8) and UWSF ≤ 0.1 ml/min, OR = 4.13 (1.7– There was a predominance of females (94%) and 10.2), p = 0.002. Symptoms of oral and ocular dryness mixed ethnicity (49.6%). The sociodemographic vari - were not predictors for diagnosis of SS. ables of the 117 (41 SS+ and 76 SS−) patients studied Of the 117 patients included in the sample, 105 individu- are shown in Table 1. als participated in the histological study. The samples sizes The prevalence of SS was 23% (27/117) based on the were satisfactory, with a mean and median area ≥ 8mm . 2002 AECG criteria and 35% (41/117) using the ACR- Considering the degree of inflammation observed in labial EULAR 2016 criteria. Kappa Agreement between minor salivary glands, 29 (24.8%) patients presented grade Gianor doli et al. Advances in Rheumatology (2023) 63:11 Page 5 of 8 Table 2 Comparison of dryness symptoms in patients with systemic lupus erythematosus with (SS+) and without (SS−) Sjögren’s syndrome Variable Total SS− SS+ p value n (%) n (%) n (%) Eye AECG Dry eyes for > 3 months 54 (46.2) 32 (42) 22 (54) 0.232 Persistent feeling of sand in the eyes 67 (57.3) 38 (50) 29 (71) 0.031 Use of lubricant eye drops > 3 times/day 28 (23.9) 15 (20) 13 (32) 0.148 Oral AECG Dry mouth feeling for > 3 months 72 (61.5) 48 (63) 24 (59) 0.624 Recurrent and persistent swelling of the parotids 30 (25.6) 18 (24) 12 (29) 0.509 Often drink liquids to help swallow dry food 52 (44.4) 33 (43) 19 (46) 0.762 Others out AECG Cry without tears 28 (24.1) 15 (20) 13 (32) 0.159 Photophobia 77 (65.8) 46 (61) 31 (76) 0.101 Visual blurring 82 (70.1) 54 (71) 28 (68) 0.756 Frequent caries 47 (40.2) 31 (41) 16 (39) 0.853 Dryness or vaginal itching 46 (39.3) 24 (32) 22 (54) 0.020 Dry skin 78 (66.7) 45 (59) 33 (80) 0.020 Itchy skin 60 (51.3) 40 (53) 20 (49) 0.691 Nasal mucosa dryness 45 (38.5) 29 (38) 16 (39) 0.927 Table 3 Criteria item comparison between systemic lupus Discussion erythematosus with (SS+) and without (SS−) Sjögren’s syndrome This study evaluated the frequency of SS in 117 patients with SLE from a tertiary hospital, using the 2002 AECG Variable Category SS− SS+ Total P criteria and the new ACR-EULAR 2016 criteria. The n (%) n (%) prevalence based on AECG criteria was similar to other Biopsy No 65 (98) 22 (56) 87 < 0.001 studies that used the same criteria [11–13]. However, Yes 1 (2) 17 (44) 18 when applying ACR-EULAR 2016 criteria, the prevalence Anti/Ro No 51 (71) 6 (15) 57 < 0.001 was higher, once ACR/EULAR criteria is slightly more Yes 21 (29) 35 (85) 56 sensitive, encompassing some patients with systemic dis- OSS No 45 (88) 19 (50) 64 < 0.001 ease but mild or no sicca symptoms as having pSS [21]. Yes 6 (12) 19 (50) 25 In the literature, it is noted that the prevalence of SS Schirmer’s Test I (mm) No 41 (77) 18 (56) 59 0.041 in patients with SLE is quite variable and studies sug- Yes 12 (23) 14 (44) 26 gest that patients with overlapping LES-SS are, in fact, a WUSF (ml/15 min) No 36 (65) 11 (31) 47 0.002 subgroup with clinical and laboratory characteristics and Yes 19 (35) 24 (69) 43 with a different prognosis from those with SLE or iso - OSS Ocular Staining Score, WUSF Whole Unstimulated Salivary Flow lated SS [22–26]. Our study found that the frequency of anti/Ro in patients with SLE/SS + was 85%, while in patients with 0, without any sign of inflammation; 58 (49.6%) patients the SLE/SS− it was 29%, with anti/Ro being an important grade 1 and 2, nonspecific; 4 (3.4%) patients the grade 3, 14 tool for investigating SS in SLE. The results shown in our (12%) patients the grade 4. In other words, 18 (17.2%) of the study are in agreement with those found in the litera- biopsies performed were characteristic of SS. Patients with ture, in which anti/Ro was significantly present in LES/ SS had a higher degree of inflammation and a tendency SS + (82%) versus LES/SS− (43.4%), which indicates the towards more adipose infiltration and ductal dilatation possibility of anti/Ro being a predictor of SS [27]. In SS, than patients without SS (Table 4). Of the 18 patients with the presence of anti/Ro 60 and anti/Ro 52 is observed. biopsy with a focal score ≥ 1, only 1 had a germinal center Anti/Ro 52 was related to pulmonary manifestations in and 4 (22%) had lymphoepithelial lesions. SS [28], while in SLE only anti/Ro 60 was observed [29]. In the present study, the frequency of anti/Ro was similar Gianordoli et al. Advances in Rheumatology (2023) 63:11 Page 6 of 8 Table 4 Frequency of alterations in salivary gland histology in SLE patients with SS (SS+) and without SS (SS−) Variable Category Total SS SS+ p value n (%) n (%) n (%) Degree of inflammation (n = 105) 0 29 (27.6) 26 (39.4) 3 (7.7) < 0.001 1 32 (30.5) 20 (30.3) 12 (30.8) 2 26 (24.8) 18 (27.3) 8 (20.5) 3 4 (3.8) 2 (3) 2 (5.1) 4 14 (13.3) 0 (0) 14 (35.9) Acinar atrophy (n = 102) Absent 44 (43.1) 29 (46) 15 (38.4) 0.129 Discreet 50 (49) 31 (49.2) 19 (48.7) Focal 1 (1) 0 (0) 1 (2.6) Moderate 7 (6.9) 3 (4.8) 4 (10.3) Ductal dilatation (n = 102) Absent 29 (28.4) 17 (27) 12 (30.8) 0.052 Discreet 64 (62.7) 43 (68.3) 21 (53.8) Moderate 9 (8.8) 3 (4.8) 6 (15.4) Adipose infiltration (n = 102) Absent 45 (44.1) 27 (42.9) 18 (46.1) 0.088 Discreet 47 (46.1) 32 (50.8) 15 (38.5) Moderate 10 (9.8) 4 (6.3) 6 (15.4) Germinal center (n = 95) Absent 94 (98.9) 63 (100) 31 (96.9) 0.359 Present 1 (1.1) 0 (0) 1 (3.1) LE infiltrate (n = 93) Absent 89 (95.7) 57 (98.3) 32 (91.4) 0.127 Present 4 (4.3) 1 (1.7) 3 (8.6) NA not available, LE Lymphoepithelial Fischer’s Exact Test was applied (categories with n < 5 or n < 10 with 1 df ) to other studies [17, 27], therefore, the subtype of anti/Ro patients [30]. In our study, focal lymphocytic sialadeni- was not evaluated. tis with a focal score ≥ 1 occurred in 18 (17.2%) of SLE The frequency of dryness symptoms was high in sample, and 17 (44%) of SS/SLE patients. Of those with patients with SLE, with or without SS. Either, nearly focal lymphocytic sialadenitis, 22% showed lymphoepi- half of the patients with SLE had salivary dysfunction thelial lesions. (WUFS ≤ 0.1 ml/min in 48.3%) and a third showed lac- Among the limitations of this study are the losses, rimal dysfunction (ST I ≤ 5 mm in 30% and OSS ≥ 5 in approximately half of the sample (120 patients) was 28.5%). Unlikely symptoms, glandular dysfunction was excluded, due to death, non-attendance, not accepting to a predictor, with a 2.6 to 7.5 more chance of SS. Con- participate, or presenting incomplete data. Furthermore, sidering the high frequency of symptoms, the dissocia- it was not possible to evaluate the Anti/Ro subtypes. tion between symptoms and the diagnosis of SS, and the greater chance of SS in patients with glandular dys- Conclusion function, gland function should be routinely assessed in The prevalence of SS was 23% based on the 2002 AECG patients with SLE, with dryness and/or positive anti-Ro. criteria and 35% using the ACR-EULAR 2016 crite- Half of the patients with SLE had some histological ria. Glandular dysfunction, salivary biopsy, and anti/Ro alteration including nonspecific inflammatory infil - were predictors of SS. The greatest advantage of the new trate, acinar atrophy, ductal dilatation, adipose infil - ACR-EULAR 2016 criteria is to enable an early diagnosis tration, and lymphoepithelial lesion. The frequency of and identify patients who present an association of the glandular histological abnormalities could explain the two diseases, thus providing individualized treatment. high frequency of glandular dysfunction in SLE without However, the ACR-EULAR criteria are not yet validated SS. Patients with SLE associated with SS had a higher for secondary SS and this study is a pioneer in investigat- degree of inflammation and focal lymphocytic sialad - ing prevalence based on the new criteria. enitis. However, SSp patients have a greater prevalence Acknowledgements of some histological features such as ductal spongiosis, The authors would also like to thank the Rheumatology and Pathology Service periductal fibroplasia, acinar fibrosis, and focal lym - of University Hospital Cassiano Antônio Moraes (HUCAM), headed by Dr. phocytic sialadenitis with a focus score ≥ 1 than SLE Valéria Valim and Dr. Maria Carmen F. S. Santos, respectively. Gianor doli et al. Advances in Rheumatology (2023) 63:11 Page 7 of 8 Author contributions Rheum Dis. 2010;69(6):1103–9. https:// doi. org/ 10. 1136/ ard. 2009. 110619. APEG, KLLM and VV participated in the conception and design of the study, Erratum in: Ann Rheum Dis. 2011;70:880. data analysis and interpretation. RVRBL, MCFSS, FCJ, LCC, EVS, STM and APEG 9. Valim V, et al. Prevalence of primary Sjögren syndrome in an important participated in the data collection and data analysis. ASS, IRM, KLLM, and APEG metropolitan area in Brazil. Braz J Rheumatol. 2013;53(1):29–34 (in participated in the data analysis and drafting of the manuscript. All authors Portuguese). read and approved the final manuscript. 10. Gilboe IM, Kvien TK, Uhlig T, Husby G. Sicca symptoms and secondary Sjögren’s syndrome in systemic lupus erythematosus: comparison with Funding rheumatoid arthritis and correlation with disease variables. Ann Rheum This work was supported by HUCAM-UFES/EBSERH. Dis. 2001;60:1103–9. 11. 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Bologna SB, Cavalcante WS, Florezi GP, Souza MM, Nico MMS, Lourenço SV. Distinct salivary gland features in Sjögren’s syndrome and lupus erythematosus sialadenite. Am J Dermatopathol. 2020;42:407–13. Publisher’s Note Springer Nature remains neutral with regard to jurisdictional claims in pub- lished maps and institutional affiliations. Re Read ady y to to submit y submit your our re researc search h ? Choose BMC and benefit fr ? Choose BMC and benefit from om: : fast, convenient online submission thorough peer review by experienced researchers in your field rapid publication on acceptance support for research data, including large and complex data types • gold Open Access which fosters wider collaboration and increased citations maximum visibility for your research: over 100M website views per year At BMC, research is always in progress. Learn more biomedcentral.com/submissions
Journal
Advances in Rheumatology – Springer Journals
Published: Mar 14, 2023
Keywords: Systemic lupus erythematosus; Sjögren's syndrome; Classification criteria; ACR-EULAR 2016; Prevalence; Labial salivary gland biopsy