Primary Sjögren’s syndrome (pSS) is a chronic and progressive systemic autoimmune disease that typically affects the tear and salivary glands, among other organs. Characterístically it causes lymphoplasmacytic glandular infiltration that leads to the progressive destruction of the same, with the resulting reduction in immunomediated secretion and the appearance of ocular dryness (xerophthalmia) and oral dryness (xerostomia), although it also affects other mucus membranes and internal organs.1

Due to its chronic and progressive nature, this disease has a major impact at a physical level as well as socially and psychologically, increasing patient morbidity. The oral dysfunction leads to an alteration in taste, speech and diet, as well as pain, depression, fatigue and sleep alterations caused by the deterioration in the overall state of health of the patient.2

There is currently no standardised protocol for referral and multidisciplinary collaboration in the treatment and management of dry mouth in l patients with pSS. The aim of the EPOX-pSS study was to obtain a more precise and complete characterisation of the oral state of patients with pSS, and the impact of their oral health on their quality of life. We describe the clinical characteristics of dry mouth, its associated complications, accumulated damage, the severity of dry mouth syndrome and patient quality of life in connection with oral health.

Of a total of 67 patients recruited in 13 hospitals, 61 who fulfilled all of the inclusion criteria were studied. 52.5% of these patients had pathological oral signs (non-stimulated salivary flow/sialography/scintigraphy of the salivary glands), 90.2% of them were antiRo/antiLa+, 91.8% were ANA + and 54% of the subject had systemic involvement. Demographic data, the variables associated with EA 2002 classification criteria, and the clinical and serological manifestations of the disease are shown in Table 1.

91.8% of the patients described xerostomia, 60.7% of the patients suffered hyposialia confirmed by NSSF and in 55.7% it was confirmed by SSF. Thirty five patients (57.4%) had lesions of the oral mucosa. The most frequent lesion was oral candidiasis (11.5%), and of the lesions associated with candida, 71.3% were candidiasis subprosthesis. 8.2% of the patients had a fissured tongue, and 13.1% had traumatic lesions. The CAOD index was 16.97 ± 7.93. Patient-perceived xerostomia recorded by the xerostomia AVS was 46.68 ± 14.4; the results corresponding to each one of the questions are described in Table 3. Oral health-related quality of life recorded by the total OHIP-14 index was 23.13 ± 13, where the dimensions with the highest scores were physical pain (4.72 ± 2.2) and psychological discomfort (4.23 ± 3). The scores for each dimension are shown in Table 4. The percentage of patients who use each one of the elements for managing xerostomia is shown in Table 5.

In the association analysis we found that the 32 patients with pathological oral signs obtained an OHIP-14 score significantly higher (26.78 ± 14) than the score for the patients without pathological oral signs (19.1 ± 13.4) (P = .03). This was also the case for both patients with peripheral nervous system involvement vs. those without this alteration (33.5 ± .7 vs. 22.7 ± 14, P = .001). The seronegative patients (6 antiRo/antiLa patients and 5 ANA subjects) tended to have a higher OHIP-14 score than those who were seropositive (antiRo/antiLa 32.8 vs. 22, P = .07; ANA 34 vs. 22.1; P = .07). Although it did not attain statistical significance, the patients with oral lesions obtained an OHIP-14 index score that was lower than that for those without such lesions (21.74 ± 13.96 vs. 25 ± 14.48; P = .81) (Table 6).

In this work we present a cohort of pSS patients with xerostomia in a very high percentage of cases (91.8%), hyposialia detected by the NSSF in more than half of the individuals, with a high intensity of oral dryness according to the xerostomia AVS, complications such as glossodynia, dysphagia and dysgeusia in a third of the patients and oral lesions in more than half of the subjects. This group also had a high rate of dental deterioration and a negative impact on quality of life in connection with oral health, as shown in the CAOD and OHIP-14 indices, respectively.

The incidence of xerostomia in the general population is estimated to stand at around 20% in individuals over the age of 60 years old, and it is an important indicator of pSS.8 In patients with pSS the prevalence of xerostomia is far higher than it is in the general population, as is shown by the results of our cohort (91.8%). The intensity of the oral symptoms perceived by patients in this study was detected using an AVS for xerostomia, giving a total average score of 46.69. A recent study published by Fernández-Martínez et al.9 and undertaken in patients with pSS found total AVS scores similar to ours, although somewhat lower (41.5), while the scores in their healthy control group amounted to 10. Other works use different scales to express the degree of xerostomia in patients with pSS, such as the study by Tashbayev et al.10 in Oslo, which evaluated the SXI-D (Summated Xerostomia Inventory-Dutch Version). They included 34 patients with pSS and a control group of 32 healthy patients. They found significantly more severe oral dryness in the patients with pSS compared with the healthy control group (average score: 12.1 vs. 5.94). The CODS (Clinical Oral Dryness Score index) ≥ 5 was reached by 62% of the patients with pSS, compared to 0% of those in the healthy control group.

One of the pSS classification criteria is the reduction in the flow of saliva.3 The majority of experts agree that a NSSF < .1 mL/min. and a SSF < .7 mL/min.11 is abnormal, and these values have been taken into account in this work. More than half of the patients in our cohort had hyposalia (60.7% of NSSF and 55.7% of SSF). The percentage of patients with reduced NSSF in our study is lower than the figures published in other works, such as the one by Enger et al.12 in Norway, who reported a reduced NSSF in 81% of 177 patients whose pSS was evaluated, or the study by López-Jornet and Camacho-Alonso13 in Spain, which found a reduced NSSF in 90.91% of the cases in their cohort (33 patients with pSS and 11 with secondary Sjögren syndrome [SS]). These variations may be due to the time of evolution and treatment being received by the patients for their disease. It is also possible that the time of day saliva flow was measured may have an influence, as this is often not specified in studies.

Saliva has important functions, not only as a lubricant, but also as an agent which protects against infections, caries and alterations to the oral mucosa. Although in itself it is not a disease, xerostomia may also affect patients’ quality of life.14,15 It sometimes does not manifest until 50% of the normal volume of saliva has been lost, and it usually appears when multiple glands are affected. Prolonged oral dryness leads to difficulties in speech, mastication and deglutition,16 reducing the retention of removal removable dentures17 and causing oral lesions. In our cohort 32.8% of the patients had glossodynia, 39.3% had dysphagia and 34.4% has dysgeusia. In the above-mentioned study by Enger et al.,12 49% of the patients described a reduction in their sense of taste, 33.8% had repeated fungal infections and 64% were hoarse. Due to their oral dryness, 35% feared going out to eat dinner during celebrations, 62% said they ate slowly, 85% had to get up at night and 72% mentioned speech difficulty.

We used the OHIP-14 index in our study to measure quality of life in connection with oral health. This index is often used in odontology to evaluate oral alterations and how different odontological treatments influence patient quality of life. It was developed by Slade and Spencer in 199718 to discover whether oral condition is an important part of different aspects of people’s lives, such as social functions, psychological and biological factors, discomfort, dysfunction and disability. In our case the scores amounted to 23.13. Previous studies also used this tool, such as the work by Enger et al.,12 who reported an average OHIP-14 index score of 12.7. These authors also found that patients with pSS and high levels of this index scored less in the 5 SF-36 subscales (general health questionnaires). In 2017 Rusthen et al.19 observed that patients with pSS (31 patients) had a significantly lower smell and taste scores than the controls (33 individuals), greater dysgeusia, ageusia and hypogeusia, anosmia or hypoanosmia, burning tongue and halitosis. The OHIP-14 average was significantly higher in patients with pSS (16.2 vs. 2.7) and it is positively associated with dysgeusia, halitosis and burning tongue, which indicates that oral involvement has a marked impact on pSS patients’ general quality of life. These authors did not analyse, like us, variations in the OHIP-14 score depending on different characteristics of patients with pSS. In our cohort we found a significantly greater negative impact on oral health-associated quality of life measured by OHIP-14 in patients with hyposialia revealed by the NSSF test and/or glandular involvement according to 2002 EA classification criteria in sialography or scintigraphy of the salivary glands. We also found a significantly higher OHIP-14 score in patients with peripheral nervous system involvement.

A series of clinical signs are associated with hyposialia, including the presence of dry cracked lips and a cracked, saburral and erythematous tongue. Other frequent findings are stringy saliva, angular cheilitis, traumatic lesions and aphthae.20 A recent systematic review undertaken by our work group on the prevalence of oral lesions in patients with SS21 concluded that patients with SS suffer more oral lesions than patients without this disease. It was also found that the most common types of oral lesion described in the literature in patients with SS were cheilitis angular, atrophic glossitis, recurring oral ulcers and cracks in the back of the tongue. In our cohort 57.4% of the patients had oral lesions, the most frequent of which were candidiasis, a cracked tongue and traumatic lesions, so that our results agree with those of the majority of studies.

One of the main complications of hyposialia is an increase in the caries index. This is due to the dissolving of hard dental tissue by dental plaque acids. The higher the caries index is shows greater loss of teeth and a larger number of replaced teeth.22,23 The average CAOD of the patients with pSS in our study was 16.97, so that more than half of their teeth were missing, with cavities or replaced, showing a higher degree of dental deterioration. Le Gall et al.24 found a somewhat greater number than ours in 31 patients with pSS. The CAOD in their cohort amounted to 20.3, which was significantly higher than in the control group. The study by Pedersen et al.25 contains a dental evaluation and caries index, with the DMFS index (Decayed, Missing, and Filled Surfaces); the patients with pSS (20 patients) had a significantly higher DMFS score than the healthy controls (20 individuals). Other authors, Olate et al.,26 use the COPD index (the total of permanent teeth with caries, missing or filled, including the said extractions, in the total number of individuals examined). They obtain a score of 7 (which is considered to be high) in their 35 patients with SS. These variations in the CAOD index may be due to time over which the disease has evolved and patient hygiene. If we make comparisons with a healthy adult population, some studies in India and Nepal show how the CAOD varies from 4.49 to 5.1 in populations aged from 20 to 56 years old.27,28

One of the limitations of this work is the size of its sample. Given that it did not reach the expected number, all of the researchers taking part were asked to prolong the period for patient inclusion that had been set. The expected number of patients was not attained after prolonging the said period, either. We believe that the problem with recruitment has been due to the complication it involved for patients, as they had to travel to a hospital other than their own, after having made an appointment themselves on a day other than the date when they visited their rheumatologist. Another limitation of this study is the lack of a record of other comorbidities, such as arterial hypertension or diabetes mellitus, as these may have influenced the appearance of oral alterations such as xerostomia and/or hyposialia and the presence of oral lesions.

In our cohort of patients with pSS in habitual clinical practice a high proportion of patients were found to have xerostomia (91.8%) and hyposalia was detected in 61% of individuals. Half of the subjects had oral lesions, the most frequent of which were candida infections, alterations to the tongue and traumatic lesions. Normal everyday life was also deteriorated by the appearance of difficulty in speech and in the diet of the patients. The appearance of caries and the loss of teeth gave rise to a high CAOD index. Alteration of oral health in these patients with pSS had a negative impact on their social, psychological and biological functions, as well as on their quality of life, as shown by the OHIP-14. The impact was greater when patients had hyposialia and/or glandular involvement detected by sialography and/or scintigraphy of the salivary glands, and in patients with peripheral nervous system involvement. We therefore believe that the availability of this homogeneous group of patients may facilitate the standardised use of different tools to diagnose and evaluate xerostomia in patients with pSS, as this would lead to greater uniformity in the clinical and therapeutic multidisciplinary management of pSS in odontology and rheumatology departments.

This projects was financed by the SORCOM (Sociedad Madrileña de Reumatología)-MSD grant, 2015.

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  The patients with pSS developed oral lesions and dental deterioration.

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  Oral health has a negative impact on the quality of life for patients with pSS.

The authors have no conflict of interests to declare.