Oral lesions in Sjögren’s syndrome: A systematic review

Sjögren’s syndrome (SS) is an autoimmune disease related to two common symptoms: dry mouth and eyes. Although, xerostomia and hyposialia have been frequently reported in these patients, not many studies have evaluated other oral manifestations. The aim of this systematic review was to investigate prevalence rates of oral lesions (OL) in SS patients and to compare it to a control group (CG), when available.  An exhaustive search of the published literature of the Pubmed, Scopus, Web of Science and the Cochrane Library databases was conducted according to the Preferred Reporting Items for Systematic Reviews and Meta-Analyses Protocols (PRISMA-P) for relevant studies that met our eligibility criteria (up to September 1st 2017).  Seventeen cross-sectional studies and one cohort study were finally included. The results showed that SS patients presented more OL compared to non-SS patients. The most frequent types of OL registered in primary and secondary SS were angular cheilitis, atrophic glossitis, recurrent oral ulcerations and grooves or fissurations of the tongue, also when compared to a CG.  OL are common and more frequent in SS patients when compared to a CG. This may be a consequence of low levels of saliva. More studies where these OL and all the possible cofounding factors are taken into account are needed. Sjögren’s syndrome, oral lesions, oral diseases, oral manifestations, oral disorders, systematic review.

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title: Classification criteria for Sjogren's syndrome: a critical review.
abstract: Over the years, several different criteria sets have been proposed for the classification of Sjögren's syndrome (SS), but none of them has been widely adopted by the scientific community until the publication of the 1993 Preliminary European Classification criteria. These Classification criteria have been largely employed both in clinical practice and in observational and interventional studies for many years. In 2002 the Preliminary European Criteria were re-examined by a joint American and European Committee. The result of this revision were the American and European Consensus Group classification criteria (AECG-criteria) which introduced more clearly defined rules for classifying patients with primary or secondary SS, and provided more precise exclusion criteria. These AECG-criteria set is now considered to be valid to ensure a specific diagnosis of SS by the vast majority of the expert in the field. To date, the AECG-criteria have been cited more than 1.304 in literature and have been used to estimate the point prevalence of the disease in several studies conducted in Greece, UK, Turkey and Norway. However, when employed in epidemiologic studies or in daily practice, the AECG-criteria have demonstrated a higher specificity (75%), but a lesser sensitivity (65.7%) in comparison to the previous Preliminary European criteria, indicating an average prevalence of pSS at ~ 0.2% in the adult population, which is far lower than previously reported. In this paper we will critically analyse the "pro and cons" of the current AECG-criteria and of the potential usefulness of some potential revisions.

title: The epidemiology of Sjögren’s syndrome
abstract: Sjögren’s syndrome is a chronic systemic autoimmune disease characterized by lymphocytic infiltration of exocrine glands. It can present as an entity by itself, primary Sjögren’s syndrome (pSS), or in addition to another autoimmune disease, secondary Sjögren’s syndrome (sSS). pSS has a strong female propensity and is more prevalent in Caucasian women, with the mean age of onset usually in the 4th to 5th decade. Clinical presentation varies from mild symptoms, such as classic sicca symptoms of dry eyes and dry mouth, keratoconjunctivitis sicca, and xerostomia, to severe systemic symptoms, involving multiple organ systems. Furthermore, a range of autoantibodies can be present in Sjögren’s syndrome (anti-SSA/Ro and anti-SSB/La antibodies, rheumatoid factor, cryoglobulins, antinuclear antibodies), complicating the presentation. The heterogeneity of signs and symptoms has led to the development of multiple classification criteria. However, there is no accepted universal classification criterion for the diagnosis of Sjögren’s syndrome. There are a limited number of studies that have been published on the epidemiology of Sjögren’s syndrome, and the incidence and prevalence of the disease varies according to the classification criteria used. The data is further confounded by selection bias and misclassification bias, making it difficult for interpretation. The aim of this review is to understand the reported incidence and prevalence on pSS and sSS, the frequency of autoantibodies, and the risk of malignancy, which has been associated with pSS, taking into account the different classification criteria used.

title: Classification criteria for Sjögren's syndrome: a revised version of the European criteria proposed by the American-European Consensus Group
abstract: Classification criteria for Sjögren's syndrome (SS) were developed and validated between 1989 and 1996 by the European Study Group on Classification Criteria for SS, and broadly accepted. These have been re-examined by consensus group members, who have introduced some modifications, more clearly defined the rules for classifying patients with primary or secondary SS, and provided more precise exclusion criteria.

title: 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
abstract: To develop and validate an international set of classification criteria for primary Sjögren's syndrome (SS) using guidelines from the American College of Rheumatology (ACR) and the European League Against Rheumatism (EULAR). These criteria were developed for use in individuals with signs and/or symptoms suggestive of SS.

title: How much saliva is enough? 'Normal' function defined.
abstract: Saliva is important for the preservation and maintenance of oral health. It is unclear, however, how much saliva is required to maintain normal oral function. Major salivary gland flow rates, objective measurements of oral health, and subjective complaints of oral problems were assessed in different-aged, healthy persons. Results suggest that the comparison of major salivary gland flow rates of an individual with population standards to identify patients susceptible to the effects of salivary dysfunction is unreliable. Changes in salivary function over time are a more meaningful gauge of the impact of saliva on oral health. The clinician should monitor salivary production to identify patients with declining salivary gland output.

title: Evaluation of palatal saliva flow rate and oral manifestations in patients with Sjögren's syndrome.
abstract: The purpose of this study was to describe the oral properties of Sjögren's syndrome (SS), including the determination of palatal saliva (PS) flow rate.



Forty-nine SS patients and 43 healthy controls participated. Subjective symptoms were recorded and clinical assessments of the oral mucosal, dental and periodontal status were made. Unstimulated whole saliva (WS) and PS flow rates, the number of decayed, missing and filled teeth (DMF-T number), the gingival bleeding index (GBI) and the periodontal probing depth (PPD) were determined.



Despite the decrease in the flow rate of WS in SS patients, PS was not different from those of the controls (1.57 +/- 1.02 and 1.35 +/- 2.5 microl cm(-2) min(-1), respectively). GBI (20.0% vs. 10.5%, respectively), DMF-T (27.1 +/- 6.12 vs. 23.0 +/- 6.99, respectively) and PPD (2.28 +/- 1.09 mm vs. 1.82 +/- 0.73 mm, respectively) were higher in SS compared with the controls (P < 0.05). DMF-T and PPD showed a positive correlation with anti-SSA and/or anti-SSB antibody positivity in the serum (P < 0.05).



Data of the present study suggest that the subjective feeling of xerostomia in SS patients is the result of a decrease in the volume of the whole saliva, and not of the viscous PS. Correlation of DMF-T and PPD with autoantibody positivity reveals that the oral health status of SS patients may be associated with the general autoimmune process.

title: Sjogren's syndrome: pathology, oral presentation, and dental management.
abstract: As one of the major autoimmune conditions involving the oral, head, and neck regions, Sjögren's syndrome has a significant level of dentally related pathology. As a result of salivary dysfunction, the teeth and mucosa may develop a wide array of changes. If these changes are not managed properly, major oral dysfunction can occur. An evaluation of salivary function, the management of xerostomia and its effects, dietary counseling, and an overall appreciation of the extraoral components of Sjögren's syndrome are presented. The dental component of comprehensive patient management is one of the most important aspects of this condition, with the dental practitioner being an essential part of the health-care team.

title: Subjective and clinical oral symptoms in patients with primary Sjögren's syndrome.
abstract: To study subjective and clinical oral symptoms and their possible correlations in patients with primary Sjögren's syndrome (1 degree SS).



In 40 cases fulfilling the Copenhagen as well as the San Diego criteria for 1 degree SS, different subjective symptoms were registered during an interview and by using a questionnaire and visual analogue scales (VAS). A clinical examination was performed to record the salivary parameters, dental status, candidosis, other mucosal lesions, and oral dysfunction.



Subjectively, dryness was reported by 98%, soreness by 63%, angular lesions by 70%, and mucosal ulcerations by 40% of the patients. Frequent carious lesions were a major subjective complaint. Clinically, the dental status did not differ from that of the Swedish general population except for a somewhat increased number of filled and decayed surfaces, here 3.5 per tooth on the average. Candidosis was present in a total of 30 patients (75%), and angular cheilitis in 14 (35%). Intraoral cultivation of Candida did not correlate with the clinical findings. Very high counts of lactobacilli and mutans streptococci were found in 77% and 47% of the patients, respectively. Decreased unstimulated saliva was significantly correlated to the subjective degree of dryness, while decreased stimulated saliva could be correlated to increased focus scores in labial salivary gland biopsies and to the presence of mucosal candidosis. Statistically significant correlations were also noted between focus scores and the grades of subjective and clinical dryness. Lichenoid lesions were seen in 18% and oral dysfunction in 55% of the 1 degree SS patients.



The impaired salivary function in 1 degree SS can be related to several subjective complaints and clinical disorders. Increased attention to and treatment of the symptoms noted is a necessity for the early diagnosis and relief of oral distress.

title: Oral involvement in primary Sjögren syndrome.
abstract: In small studies, investigators have described oral features and their sequelae in primary Sjögren syndrome (PSS), but they have not provided a full picture of the aspects and implications of oral involvement. The authors describe what is, to their knowledge, the first large-scale evaluation to do so. In addition, they report data regarding utilization and cost of dental care among patients with PSS.



The authors surveyed patients with primary Sjögren syndrome as identified by their physicians (PhysR-PSS), patient-members of the Sjögren's Syndrome Foundation (SSF-PSS) and control subjects who did not have PSS. They made comparisons between the three groups.



Subjects were 277 patients with PhysR-PSS, 1,225 patients with SSF-PSS and 606 control subjects. More than 96 percent of those in the patient groups experienced oral problems. An oral complaint was the initial symptom in more than one-half of the patients. Xerostomia-associated signs and symptoms were common and severe, as evidenced by scores on an inventory of sicca symptoms. These patients' rate of dental care utilization was high, and the care was costly.



Oral and dental disease in PSS is extensive and persistent and represents a significant burden of illness.



Oral symptoms and signs are common in patients with PSS. Early recognition of the significance of these findings by oral specialists could accelerate diagnosis and minimize oral morbidities.

title: Oral manifestations in patients with Sjögren's syndrome.
abstract: To investigate oral signs and symptoms in patients with Sjögren's syndrome (SS), and to compare results with a group of healthy individuals.  Each individual completed a questionnaire designed to investigate his/her perception of oral health and dryness, as well as a list of signs and symptoms associated with xerostomia. An oral clinical evaluation was performed.



A total of 81 subjects were studied, 21 with primary SS, 29 with secondary SS, and 31 healthy individuals. Patients with SS considered that their oral health was poor. Oral dryness was perceived as intense. Symptoms most commonly expressed were: sensitivity to acids (68%), difficulty eating dry foods (66%), and sensitivity to spicy foods (58%). Dryness of the lips (76%) and the tongue (68%) were also among the most frequent complaints. Oral findings of patients with SS included cervical or atypical caries in 83%, fissured erythematous tongue in 70%, and oral candidiasis in 74%. Significant differences were found when results obtained from patients with SS were compared with the healthy group.



The oral health of this group of patients with SS was deficient. Adequate management of dry mouth was not achieved, mainly for the modifiable components such as dental decay and oral candidiasis. Therefore. treatment and prevention plans are mandatory. These measures might help to reduce the discomfort associated with oral dryness and to reduce dental loss.

title: Prevalence of oral lesions of autoimmune etiology in patients with primary Sjogren's syndrome.
abstract: The primary objective of this study was to determine the prevalence of oral lesions of autoimmune etiology (OLAIE) in a cohort of patients with primary Sjögren's syndrome (pSS).



A multi-center retrospective cohort study was conducted at the oral medicine practices of Carolinas Medical Center (CMC), Baylor College of Dentistry (BCD), and the University of Florida (UF). Each site performed a chart review of patients with well-characterized pSS. Clinical variables such as OLAIE, traumatic lesions, and medical conditions were compiled at each site. The association between clinical variables and the presence of OLAIE was then assessed for significance.



We evaluated 155 patients diagnosed with pSS. Nineteen patients with pSS (12.3%) had an OLAIE. CMC reported 11 (21.2%) patients with OLAIE, while BCD and UF reported 4 (7.3%) and 4 (8.3%), respectively. Eleven of the 19 (58%) patients with OLAIE had lichen planus, 6 (32%) had aphthous stomatitis, 1 (5%) had chronic ulcerative stomatitis, and 1 (5%) had lesions of systemic connective tissue disease by immunofluorescence.



The results of our analysis suggest that patients with pSS have a 12% prevalence of OLAIE with a wide range (7.3-21.2%) found between practices. This difference is likely related to the different screening protocols for oral dryness between sites.

title: Preferred reporting items for systematic review and meta-analysis protocols (PRISMA-P) 2015: elaboration and explanation
abstract: Protocols of systematic reviews and meta-analyses allow for planning and documentation of review methods, act as a guard against arbitrary decision making during review conduct, enable readers to assess for the presence of selective reporting against completed reviews, and, when made publicly available, reduce duplication of efforts and potentially prompt collaboration. Evidence documenting the existence of selective reporting and excessive duplication of reviews on the same or similar topics is accumulating and many calls have been made in support of the documentation and public availability of review protocols. Several efforts have emerged in recent years to rectify these problems, including development of an international register for prospective reviews (PROSPERO) and launch of the first open access journal dedicated to the exclusive publication of systematic review products, including protocols (BioMed Central’s Systematic Reviews). Furthering these efforts and building on the PRISMA (Preferred Reporting Items for Systematic Reviews and Meta-analyses) guidelines, an international group of experts has created a guideline to improve the transparency, accuracy, completeness, and frequency of documented systematic review and meta-analysis protocols—PRISMA-P (for protocols) 2015. The PRISMA-P checklist contains 17 items considered to be essential and minimum components of a systematic review or meta-analysis protocol. This PRISMA-P 2015 Explanation and Elaboration paper provides readers with a full understanding of and evidence about the necessity of each item as well as a model example from an existing published protocol. This paper should be read together with the PRISMA-P 2015 statement. Systematic review authors and assessors are strongly encouraged to make use of PRISMA-P when drafting and appraising review protocols.

title: Oral candidiasis and Sjögren's syndrome.
abstract: To determine the prevalence of oral candidiasis (OC) in patients with Sjögren's syndrome (SS), to identify oral signs and symptoms associated with OC, and to compare them with a healthy group.



Patients with primary SS, and with SS associated with autoimmune disease were identified according to established criteria. Each individual had: (1) a questionnaire, (2) an oral clinical evaluation, (3) a set of microbiological tests: tongue smear, culture of tongue smear, and saliva sample. Diagnosis of OC was established with 2 positive results and the presence of any sign or symptom.



A total of 81 subjects were studied, 21 with primary SS, 29 secondary SS, and 31 healthy subjects. We diagnosed OC in 74% of patients with SS, which was statistically significant compared to the healthy group (23%) p < 0.001. Frequent symptoms associated with OC were increased sensitivity to spicy foods (58%) and unpleasant metallic taste (40%). Common signs of OC were erythematous lesion on the dorsum of the tongue (68%) and angular cheilitis (24%).



Prevalence of OC was high in patients with SS. The frequency of signs and symptoms associated with OC may explain some of the clinical manifestations. If chronic erythematous OC is found in patients with SS an oral assessment at every appointment may help provide appropriate treatment.

title: Oral Candida albicans in Patients with Sjögren's Syndrome
abstract: Candida species are common inhabitants of the oral cavity of patients with salivary gland dysfunction. The purpose of this study was to determine the prevalence and density of oral Candida albicans in patients with Sjögren's syndrome, to assess the infectious agent's oral manifestations and to compare the number of colony-forming units (CFU) of C. albicans in patients with primary (n=9) and secondary Sjögren's (n=18) with the whole unstimulated salivary flow rate in each group. An age- and sex-matched group of control subjects (n=14) was selected for comparison. An oropharyngeal collection of samples was taken from each subject and cultured. Quantitative cultures specific for C. albicans were obtained. The frequency distribution showed that more than 80% of all research subjects had positive results for C. albicans whereas the control subjects had no positive results. The most common lesion was erythematous candidiasis, followed by angular cheilitis. The Sjögren's subjects also demonstrated significantly higher numbers of C. albicans CFU than controls. Findings from this study demonstrate that patients with primary or secondary Sjögren's syndrome had significantly greater C. albicans colonization compared with the control population. C. albicans colonization was greater in primary Sjögren's patients than in secondary Sjögren's patients; however, the quantity of C. albicans found in each population was not universally relative to salivary flow.

title: Oral mucosal manifestations in primary and secondary Sjögren syndrome and dry mouth syndrome
abstract: One of the most important symptoms of Sjögren syndrome is xerostomia. The oral cavity deprived of saliva and its natural lubricative, protective and antibacterial properties is prone to a number of unfavourable consequences.  To present the most important lesions on the oral mucosa in primary and secondary Sjögren syndrome and in dry mouth syndrome.  The study group comprised 55 patients including 52 women and 3 men aged 20–72 years (average: 28.25 years).  Basing on the accepted criteria, primary Sjögren syndrome was diagnosed in 22 (40%) patients, secondary Sjögren syndrome in 18 (32.7%) patients, and dry mouth syndrome in 15 (27.27%) patients. The physical examination and the examination of the mouth were performed and history was elicited from every patient.  The most common pathologies appearing on the oral mucosa in primary and secondary Sjögren syndrome are angular cheilitis, cheilitis, increased lip dryness as well as non-specific ulcerations, aphthae and aphthoid conditions.

title: Prevalence and intraoral distribution of Candida albicans in Sjögren's syndrome.
abstract: An imprint culture technique has been employed to study the prevalence and intraoral distribution of Candida albicans in 16 patients with Sjögren's syndrome and in 16 healthy controls matched for age, sex, and dental status. The prevalence and intraoral density of C. albicans was found to be significantly higher at almost all sites in the Sjögren's patients than in the controls. The distribution of candida was also altered, being significantly higher in the floor of the mouth and anterior labial sulcus in the Sjögren's group. There was an approximate inverse relationship between candida populations and rate of salivary flow. Mean candida densities were found to be significantly higher in those Sjögren's patients with detectable serum rheumatoid factor in the serum. However, patients with primary Sjögren's syndrome had significantly higher mean candida densities compared with patients with secondary Sjögren's syndrome.

title: The oral ecology of patients with severe Sjogren's syndrome.
abstract: An investigation of the commensal microflora, salivary flow rate, pH, and the degree of atrophy of the oral mucosa in ten patients with severe Sjogren's syndrome and ten control subjects, revealed a number of differences. The numbers of Streptococcus salivarius, Neisseria pharyngis, Veillonella species and Micrococcus mucilagenosus isolated from patients with Sjogren's syndrome were significantly reduced, while the numbers of Candida spp. and Staphylococcus aureus were significantly increased when compared with control subjects. In addition the salivary pH of the Sjogren's group was significantly reduced and the degree of mucosal atrophy increased compared with controls.

title: Primary Sjögren's syndrome: salivary gland function and clinical oral findings.
abstract: To evaluate salivary gland function, saliva composition and oral findings in patients with primary Sjögren's syndrome (pSS) subdivided into patients with and without focus score > or = 1 (FS) and/or antibodies to SSA/SSB (AB) as well as in healthy controls.



Unstimulated (UWS) and chewing stimulated (SWS) whole saliva, and stimulated parotid saliva (SPS) were collected in 16 patients fulfilling the European classification criteria for pSS subdivided into those with FS and/or AB (n = 8) and those without FS and AB (n = 8), and in age-matched (n = 14) and young healthy controls (n = 13). UWS and SWS were analysed for Na+ and K+. SPS was analysed for Na+, K+, statherin, and proline-rich proteins (PRPs). Sicca symptoms, DMFT/DMFS, plaque (PI) and gingival (GI) scores, periodontal pocket depth (PPD), and mucosal status were recorded.



The young healthy controls had lower UWS as compared to the aged controls (P = 0.03). However, the aged controls had higher DMFT/DMFS (P < 0.001) and PI, GI and PPD (P < 0.01). Patients with FS and/or AB generally had lower saliva secretory rates than patients without FS and/or AB (P = 0.01 for UWS and SPS) and age-matched healthy controls (P = 0.001). There was no significant difference in the content of Na+ and K+, statherin and PRPs between groups. Patients with FS and/or AB had the highest frequency of oral mucosal changes and higher DMFT/DMFS than patients without FS and/or AB and healthy controls (P < 0.01). However, PI, GI, and PPD did not differ significantly.



Patients with FS and/or AB had lower salivary secretory rates, higher DMFT/DMFS, and more oral mucosal changes than patients without FS and/or AB. Additionally, data suggest that salivary gland function in healthy individuals do not decrease with age.

title: Multiple Oral Candida Infections in Patients with Sjögren’s Syndrome — Prevalence and Clinical and Drug Susceptibility Profiles
abstract: To determine the prevalence of oral candidiasis and multiple oral Candida infections in patients with primary Sjögren’s syndrome (SS), and the clinical and drug susceptibility profile.  Thirty patients with primary SS were enrolled in our study. The diagnosis of oral candidiasis was based on the clinical manifestation, and confirmed by a concentrated rinse culture. Candida spp. assessment was accomplished using standard methods: Sabouraud dextrose agar with 50 mg/l chloramphenicol and CHROMagar were used for the rapid screening of clinical species, followed by the API 20C system for further species identification. In vitro antifungal drug susceptibility of Candida isolates was determined by the minimal inhibitory concentrations.  In our study, 87% (26/30) of subjects had oral candidiasis, in which 42% (11/26) had multiple Candida spp. infection. Although C. albicans remains the predominant isolate, other rare species such as C. tropicalis, C. glabrata, C. parapsilosis, and C. krusei were present, alone or in combination. Chronic atrophic candidiasis is the most common clinical type of oral candidiasis in patients with SS. The susceptibilities of the 44 Candida isolates to 7 antifungal agents varied dramatically. The resistance to azoles was remarkable, and the phenomenon of cross-resistance between itraconazole and fluconazole was observed.  Patients with primary SS carry a high risk of oral candidiasis and a high frequency of multiple Candida infections. The azole resistance patterns of Candida spp. support the necessity for drug susceptibility testing as a routine procedure for patients with oral Candida infections.

title: A descriptive study of the oral status in subjects with Sjögren's syndrome.
abstract: Sjögren's Syndrome (SS) is an autoimmune pathology of varying prevalence. Its involvement in exocrine glands requires that greater attention be paid to patients' oral health. A cross-sectional study was designed to assess the oral health of subjects with SS in constant medical follow-ups. Variables such as the presence of periodontal infections, decay and alterations in the oral mucosa were analyzed, and the individual's salivary flow was measured. The data were analyzed descriptively and with the chi-squared test, considering p<0.05 as statistically significant. 35 subjects of both sexes were studied, aged between 25 and 82 years, with an age average of 53.9 years; they presented on average 7.9 years after the initial diagnosis. The subjects reported a dental check-up every 6 months in only 9% of cases, whereas the rest had one every 1 or 2 years. All the subjects recounted presenting with dry mouth and associated significantly the ingestion of fluids and teeth brushing to improve the sensation of dryness. The salivary flow was objectively seen to be compromised, showing a significant reduction in those with more time since diagnosis of the disease; more than 90% of subjects exhibited periodontal inflammation and a high level of caries. The mucosa presented a low level of pathology. In conclusion, education in oral health is imperative for subjects with this pathology and more frequent check-ups may be useful in decreasing the levels of oral pathology.

title: Oral health condition and saliva flow in southern Chinese with Sjögren's syndrome.
abstract: To investigate the oral health condition and saliva flow of southern Chinese patients with Sjögren's syndrome (SS).



51 SS patients (26 primary and 25 secondary cases) and 29 controls took part in this cross-sectional study. Stimulated whole and parotid saliva flow rates, pH, and buffer capacity, and xerostomia, oral mucosal lesions, oral hygiene status, dental and periodontal conditions, prosthetic status were assessed and compared between groups.



Stimulated whole saliva (SWS) flow was reduced in primary and secondary SS cases (p<0.001), pH and buffer capacity were also reduced in the primary SS group (p<0.05). SS patients had a greater prevalence of xerostomia than controls (p<0.001). Primary SS patients had a higher mean DMFT, more missing teeth, and more prostheses than secondary SS cases and controls (p<0.05). SWS flow correlated negatively with the number of filled teeth in both SS groups (p<0.05) and the number of decayed teeth in the primary SS group (p<0.05).



Despite good oral hygiene and regular dental check-ups, the oral health of southern Chinese with primary SS was significantly compromised compared with secondary SS cases and controls, most probably due to the combined effect of impaired salivary gland function and poorer saliva buffer capacity.