Abstract
Background. Sjögren’s syndrome (SS) is a common systemic autoimmune disease that affects oral health, and consequently oral health-related quality of life (OHRQoL) due to the involvement of exocrine glands.
Objectives. The present study aimed to evaluate the oral health-related quality of life and oral health indicators in patients with SS in comparison with healthy individuals.
Material and methods. In the case and control groups (45 patients and 45 healthy individuals), questions about demographic data, other systemic disorders, medications, the years of infection, xerostomia, as well as inquiries about the quality of life (Oral Health Impact Profile-14 – OHIP-14) were asked. The patients were evaluated clinically, and oral health indicators, including the plaque index (PI), the gingival index (GI), the sulcus bleeding index (SBI), and the number of decayed, missing and filled teeth (DMFT) were assessed on the Ramfjord teeth. Unstimulated saliva samples from both groups were obtained and weighed. The data was analyzed using IBM SPSS Statistics for Windows, v. 24.0. Quantitative variables were compared between the case and control groups with the use of the independent t test or their non-parametric equivalent (the Mann–Whitney test).
Results. The comparison of the quantitative variables between the study groups showed a statistically significant difference in the OHRQoL scores (p = 0.037) and the unstimulated saliva flow rate (p = 0.002) between the case and control groups. Also, there was a statistically significant difference in the DMFT index between patients with primary and secondary SS in the case group (p = 0.048).
Conclusions. The lower OHRQoL of patients with SS requires more attention and follow-up to solve periodontal and dental problems in this group of patients.
Keywords: oral health-related quality of life, Sjögren’s syndrome, plaque index, gingival index
Introduction
Sjogren’s syndrome (SS) is an autoimmune disease of the exocrine glands that mainly affects the salivary and lacrimal glands.1 This disease affects 3–4% of the adult population and primarily affects middle-aged to older women. The prevalence of this disease in the European population varies from 0.05 to 1%.2, 3 The condition can be divided into primary and secondary SS.4 It can be present alone (primary SS, pSS) or in association with other systemic autoimmune disorders such as lupus, rheumatoid arthritis, and connective tissue diseases (secondary SS, sSS). The clinical presentation of this disease is characterized by dryness of the entire mucosa. Symptoms may range from localized outcomes of the exocrine glands to systemic complications such as vasculitis.5 Although the etiology of this disease is still unknown, the current hypothesis supports an autoimmune reaction within the exocrine glands, which triggers the uptake of salivary gland and lacrimal cell nuclear factors. Over the years, this pathological process leads to lymph node destruction and disruption or even total loss of saliva and tears.6 SS can affect the overall quality of life related to general health.1 Fatigue, pain, and systemic manifestations are the predominant complications of this disease that affects the health-related quality of life.7 Quality of life is a multidimensional and broad concept that means a person’s understanding of their life situation according to culture and value systems, expectations, standards, and life experiences that affect the state of physical, mental, social communication, and personal beliefs.8 Quality of life is a valuable indicator used to measure health status in research.9 Oral health-related quality of life (OHRQoL) includes a part of the quality of life affected explicitly by oral health.10
Decreased salivation in patients with pSS can have a significant negative effect on oral health.11 Oral symptoms of SS are mainly due to decreased salivary flow.12 Xerostomia can be severe and can lead to discomfort and problems with speech, eating, swallowing, changes in taste, candidiasis of the mouth, tooth decay, and periodontal problems.13 In these patients, oral issues play a critical role in OHRQoL.14 Numerous studies have linked decreased salivation to oral problems.15, 16 A few studies have reported taste and smell disorders in patients with early SS.17 However, the effect of oral symptoms of SS on OHRQoL is not yet fully understood.18 Health interventions are increasingly being used to assess the impacts of oral disorders.19 A comprehensive approach to measuring OHRQoL combines the use of general and specific oral criteria with specific conditions.20 Oral Health Impact Profile (OHIP) is currently one of the most comprehensive measures of the effect of oral status on health-related quality of life.21 Assessing patient-based health status is essential to measuring health. Oral diseases are prevalent and have physical, social, economic, and psychological consequences on patients. Many of these patients’ quality of life is impaired, and various aspects of their lives, such as chewing food and speech, can be affected.22 The OHIP was developed by Slade and Spencer in 1994 and is an advanced OHRQoL tool that is used internationally.23 The main OHIP consists of 49 items that can be long and time-consuming. In 1997, Slade developed a short form with 14 questions called the OHIP-14 that was found to have good reliability, accuracy, and credibility.24 These fourteen items of the OHIP fall into seven aspects: functional limitations, physical pain, mental discomfort, physical disability, mental disability, social disability, and disability.23
Therefore, considering the significant effects of SS on general health and oral health, the lack of a similar study in Iran, and to measure of some variables that have not been studied so far, this study aims to evaluate the OHRQoL of patients with SS referred to the Touba Clinic in Sari in 2020. The null hypothesis is that there is a difference between SS patients and healthy individuals when looking at periodontal indices, Decayed, Missing, and Filled Teeth (DMFT) index, xerostomia, hyposalivation, and OHRQoL.
Material and methods
The present study is a case-control study of patients referred to the Touba Clinic in Sari, India, in 2020. The Research Ethics Committee of Mazandaran University of Medical Sciences approved this study (Ethics Code: IR.MAZUMS.REC.1398.6148). The sample size was estimated using the results of a study by Meijer et al.4 In their study, the mean and standard deviations were 59.2 ±26.0 in the case group and 74.8 ±25.8 in the control group, respectively. Considering these results, a 95% confidence level, an 80% test power, two test ranges, and using the comparison formula between means and using the G*power software, the sample size was estimated to be 90 people (45 people in the case group and 45 in the control group).
The inclusion criteria included people with primary or secondary SS diagnosed using the American-European Consensus Group criteria5 with an age range of 30–80 years who had at least 20 teeth in their mouth and no history of periodontal treatment in the past three months. The exclusion criteria included patients who are illiterates, patients who were unable to complete the questionnaire, and patients with chronic gastrointestinal diseases, organ transplantation, diabetes mellitus, infectious diseases (hepatitis, HIV), seizure disorder or neuropathy, heart failure, drug users, pregnant women, smokers, and alcoholics.25 The control group was selected from patients referred to the Sari Dental School clinic. In addition to the mentioned inclusion and exclusion criteria, age and gender were considered for the case group. Also, the control group was negative for diabetes based on fasting blood sugar (FBS) test results in the month before the start of the study.
Data collection
The purpose of the research and its steps were initially explained to all participants, and after obtaining written consent, patients were assured that their information would remain confidential. This study’s data collection method used a question-and-answer session, a questionnaire, patient records, and a clinical oral examination by a periodontist. Demographic information for the patients (age, gender) and information related to the patient (duration of illness, medications) were recorded in the patient’s files. To determine the presence of xerostomia, patients were asked 9 questions, and those who answered 9 to 5 questions positively were diagnosed with xerostomia.25
Unstimulated saliva flow rate
To assess the unstimulated saliva flow rate (USFR), individuals were asked to avoid drinking, eating, and smoking for at least 2 h before sampling. Patients with partial dentures were asked to remove them from their mouths. While collecting unstimulated saliva samples, individuals were asked to sit and reduce their mouth movement and not swallow or suck. Saliva was then collected from the floor of their mouths for 60 s. They were then asked to spit it in a pre-weighed tube for five consecutive minutes. The saliva samples were stored in the freezer at −70°C until assayed. The amount of unstimulated saliva was measured by the weighting method and expressed in milliliters per minute. A USFR <0.1 mL/min was considered to indicate hyposalvation.26
Oral health-related quality of life
To assess OHRQoL in this study, the OHIP-14 questionnaire was used, and the validity and reliability of the Persian version were confirmed27 and included the seven subgroups: functional limitation, physical pain, mental discomfort, physical disability, mental disability, social disability, and disability. Each subgroup consisted of 2 questions. Two methods were considered to evaluate the responses. The additive17 method in which test options were scored as never = 0, seldom = 1, sometimes = 2, most often = 3, in the majority of cases = 4. The OHIP-14 scores could range between 0 and 56, and the lower the score, the better the quality of life for the patient. In another evaluation method called simple count (SC), the score given for “never” and “seldom” options is zero, and the score given for sometimes, most often, and in the majority of cases is one. This method was used because some people do not understand the real difference between the questionnaire options. The OHIP-14 score ranges from zero to 14 using the SC method, and again the lower the score, the higher quality of life in the patient.27
Periodontal indices
Finally, the patients were clinically examined by a periodontist. The DMFT, the plaque index (PI), the gingival index (GI), and the sulcus bleeding index (SBI) were performed on the Ramfjord teeth (teeth numbers 3, 9, 12, 19, 25, and 28), and if one of these teeth were missing, the lateral tooth was used.28
Statistical analysis
To analyze the data, all the recorded information was entered into the IBM SPSS Statistics for Windows software, v. 25.0 (IBM Corp., Armonk, USA). The normality of quantitative variables was assessed using the Kolmogorov–Smirnov and Shapiro–Wilk tests. The variables were described as mean and standard deviation (M ±SD), minimum and maximum, and as number and percentage (n (%)). The normally distributed variables were compared using the independent t tests, whereas abnormal parameters were compared using a non-parametric comparative test (the Mann–Whitney test), and for multiple groups, the non-parametric Kruskal–Wallis H comparison test was performed. To examine the correlation relationships, normal data utilized the Pearson correlation method, whereas abnormal data used the Spearman method. Also, for the comparison of variables between the groups, the χ2 test and Fisher’s exact test were used. Finally, to rank and prioritize abnormal data, the Friedman ranking method was used. The criterion in which all cases reached statistical significance was a p-value <0.05, except for the normality and equality of variance.
After obtaining a license from the esteemed vice-chancellor of research at the university, the ethics committee began the process in Sari using the ethics code IR.MAZUMS.REC.1398.488 and obtained approval from the competent authorities. This research started by obtaining patient consent after explaining the potential advantages and disadvantages of the study, the goals of the project, the voluntary nature of the study, the possibility of leaving the study at any time, and the process of keeping the patients’ information and identity confidential.
Results
A total of 90 people (45 in the case group and 45 in the control group) participated in this study. In the case group, 19 patients (42%) had pSS, and 26 patients (58%) had sSS (22 patients with rheumatoid arthritis and 4 patients with scleroderma). There were 40 women (88%) and 5 men (12%) in both groups. The mean age of the case group was 50.62 ±7.82 years, and the control group was 50.62 ±7.82 years, which had a similar distribution that was not statistically significant (p = 0.999). The mean age in the case group with pSS was 47.68 ±8.42 years. The case group with sSS was 52.77 ±6.73 years, which was not statistically significant based on a non-parametric comparison test (Mann–Whitney; p = 0.373). The disease duration in the case group varied from 4 months to 20 years. The period of the disease had a significant relationship with the patient’s age (p = 0.027) but had no statistical association with any other measured indicators. It should be noted that in the case group, 17 people (38%, 8 people with pSS, and 9 people with sSS), and in the control group, 6 people (13%) had hyposalivation. Examination of the 9-item xerostomia questionnaire revealed that 20 patients (45%) in the case group (8 patients with pSS and 9 patients with sSS) and only 4 patients (90%) in the control group had xerostomia.
The results of the analyzed quantitative variables in this study, as presented in Table 1, show that the mean DMFT index in the case group was 10.29 ±4.70. In the control group, it was 10.24 ±4.78, which was not statistically significant (p = 0.965). PI, GI, and SBI were also examined in the case and control groups, and the results showed that the mean PI in the case group was 1.33 ±0.44 and 1.37 ±0.39 in the control group, which was not significantly different (p = 0.646). The mean GI in the case group was 6.93 ±1.43 and 7.67 ±1.87 in the control group, which was not significantly different (p = 0.206). Also, the mean SBI in the case group was 0.93 ±1.42 and 1.53 ±1.77 in the control group, which was not statistically significant despite the apparent difference (p = 0.210). Saliva samples collected from the two groups after weighing showed that the mean USFR per minute in the case group was 0.93 ±0.99. The USFR per minute in the control group was 1.36 ±0.99, in which the difference was statistically significant (p = 0.002). It should be noted that 17 patients in the case group (38%) and 6 in the control group (13%) had hyposalivation (Table 1).
Table 2 summarizes the results of the correlation relationships between the quantitative variables. These results show that in the case group, there were significant correlations between PI with GI and SBI with coefficients of r = 0.397 and r = 0.305, respectively. There is also a stronger positive correlation between GI and SBI (r = 0.89).
Examination of Pearson correlations in the control group also shows that there is a significant and negative correlation between patient age and USFR (r = 0.40). There is also a relationship between age and PI (r = 0.38). There is a significant correlation (p = 0.32) between PI and GI with a 95% accuracy. As in the case group, there is a strong correlation (r = 0.93) between the GI and SBI variables (Table 2).
In the study of OHRQoL as a dependent variable with the independent quantitative variables using Pearson correlation coefficient analysis, we observed that additive oral health impact profile (ADD_OHIP14) and simple-count oral health impact profile (SC-OHIP14) in the case group had a positive and significant correlation with PI (r = 0.31 and r = 0.35, respectively). But in the control group, this correlation was not statistically significant. Other quantitative data, such as GI, SBI, and DMFT did not show a significant relationship with oral quality of life variables collected in the questionnaire (Table 3).
Comparative evaluation of patients
with primary and secondary SS
Quantitative indices in patients with primary
and secondary SS
The analyzed results of SS patients in the two groups of pSS and sSS in Table 4 showed that the mean ADD_OHIP-14 in pSS patients was 21.00 ±10.30. In sSS, it was 18.50 ±13.93, and the mean SC_OHIP14 in pSS was 7.21 ±1.08. In sSS, it was 6.15 ±4.01, which did not show a statistically significant difference (p = 0.493 and p = 0.392, respectively). Also, PI, GI, and SBI indices between primary and secondary Sjogren’s were examined. The mean PI in pSS was 1.342 ±0.37, and in sSS was 1.314 ±0.495 (p = 0.829). The mean GI was 1.123 ±0.156 in pSS and 1.212 ±0.304 in sSS (p = 0.660). The mean SBI in pSS was 0.114 ±0.125, and in sSS was 0.186 ±0.292 (p = 0.980). Also, the mean USFR values were not statistically significant between the two groups of Sjogren’s patients (p = 0.260). However, the mean DMFT in primary Sjogren’s patients was 12.05 ±4.65, and in secondary patients, it was 9.31 ±4.15, which was statistically significant (p = 0.048) (Table 4).
Comparison of the quantitative indices in SS patients with regard to gender
The results showed no statistically significant difference in ADD-OHIP14, SC-OHIP14, age, GI, SBI, and DMFT in men and women with SS, but this difference was statistically significant for PI (p = 0.045). A comparison of the mean USFR in Sjogren’s patients also showed that the mean in women was higher than in men (p = 0.026) (Table 5).
Investigating the effect of the duration of the disease
Examination of the correlations between the studied quantitative variables and the duration of SS in Table 6 shows that there is a significant relationship between the studied indices ADD_OHIP14, SC_OHIP14, PI, GI, SBI, and USFR in patients with SS in relation to the duration of the disease. Still, there was a correlation with patient age (r = 0.33) which was also obvious (p = 0.027). Also, the mean DMFT in Sjogren’s patients had a positive and significant relationship with the disease’s duration (Table 6)
Effect of different drug therapies on the quantitative indices in SS patients
In this study, 100% of people used hydroxychloroquine and adjuvant drugs such as folic acid, calcium, and omega-3, 33% of patients were treated with methotrexate or prednisolone in addition to the above, and 11% of patients also used bromhexine. The results of a comparative analysis of the quantitative indices mean and the three types of prescribed drug treatments: (1) immunosuppressives with supplements and sialagogue; (2) immunosuppressives with supplements; and (3) immunosuppressive drugs with supplements and anti-rheumatic drugs using non-parametric multi-group comparisons with 95% accuracy showed that there was no significant differences or preferences between the mean of the variables ADD_OHIP14, SC_OHIP14, PI, GI, SBI, USFR, and DMFT (Table 7).
Discussion
The present study compared OHRQoL in patients with primary and secondary SS and healthy individuals. Based on the study results, PI, GI, SBI, and DMFT indices did not show a statistically significant difference between the two groups. USFR was significantly different between patients with SS and healthy individuals (p = 0.002).
The results of many studies have linked SS to poor periodontal status for more than three decades,28, 29 with PI, GI, and bleeding on probing (BOP) indices higher in Sjogren’s patients than in healthy patients. In a meta-analysis of 512 studies examining PI, GI, probing pocket depth (PPD), clinical attachment loss (CAL),30 and DMFT in patients with SS, only 10 studies were eligible for the meta-analysis. Four studies showed a statistically significant difference in the GI between patients and healthy individuals,12, 31, 32, 33 and 5 studies reported PLI in Sjogren’s patients higher than controls.32, 33, 34, 35, 36 The final results of the meta-analysis between 163 patients with SS and 164 healthy individuals did not show a statistically significant difference in the PI and GI in these two groups.37 Some studies have reported a higher risk of periodontal involvement in patients with SS than in healthy individuals.28, 31 In contrast, other studies have not reported an increase in periodontal involvement in Sjogren’s patients.32, 33, 35, 36
Finally, the meta-analysis results in 2019 showed that despite the higher rates of periodontal disease in Sjogren’s patients compared to healthy individuals, the statistical difference between the two groups was not significant.37
In another review study on the relationship between SS and a patient’s periodontal status, 17 studies were reviewed, with only 8 studies being included in the meta-analysis.33 The PI and GI were higher than in healthy individuals in 4 studies of Sjogren’s patients, and the BOP in the case group was higher than in the control group.38 A meta-analysis of 303 patients with primary and secondary SS with 288 healthy individuals showed that the GI was statistically significant in primary and secondary SS compared to the control group. The meta-analysis reported differences in the results related to PI, GI, BOP, and PPD due to differences in the examiners used in the different studies. This means that these indicators are subjective, and each examiner may use different pressures to examine these indicators. Even one examiner may not have the same examination pressure on periodontal tissues during the study.38 Good oral hygiene and less severe disease are cited in a study to explain the lack of significant association between SS and periodontal disease.39
Also, there was no significant relationship between periodontal involvement in Sjogren’s patients and healthy individuals due to long-term use of drugs such as NSAIDs, DMARDs, and immunosuppressive drugs, which can effectively treat periodontal inflammatory responses.40
In our study, the lack of a significant relationship between GI, PI, and SBI indices between the case and control groups and the reasons mentioned in the above examinations can also be related to the inclusion or exclusion criteria of the participants. Destructive and influential factors on the periodontium, especially smoking, and diabetes were among the participants’ exclusion criteria in our study. To accurately evaluate the effect of the disease on the periodontal status, we applied strict criteria in selecting individuals for the two groups, which some studies neglected.12, 41
In this study, the DMFT index did not show a statistically significant relationship between the two groups. In Antoniazzi’s study, a tooth missing in patients with pSS was not statistically significant compared to the healthy control group.31 The results of a meta-analysis mentioned DMFT in the group of Sjogren’s patients to be higher than in the control group. It should be noted that one of the possible reasons for this result in comparison with our study is the role of smoking and its use which was reported in 7 studies of this meta-analysis.12, 31, 33, 35, 36, 37, 42 Despite the lack of a significant relationship between the DMFT index between case and control groups in our study, there was a statistically significant difference in DMFT between primary and secondary SS compared to patients with primary and secondary SS (p = 0.048).
Kalk noted that the submandibular and sublingual salivary flow rate in SS was lower than usual.43 This result was consistent with our study and some studies that reported higher DMFT in patients with pSS due to decreased salivary gland function and decreased salivary buffering capacity compared to sSS.12, 39, 41 Hyposalivation can also be another cause of higher DMFT in pSS. In our study, 42% of people with pSS had hyposalivation, while 34% of people with sSS showed decreased salivary gland function.
The study of oral health variables related to the quality of life in Sjogren’s patients with healthy individuals showed that ADD-OHIP-14 (p = 0.037) and SC-OHIP-14 (p = 0.025) were statistically significantly different between the two groups. Participants in all 7 subgroups and 14 questions showed a statistically significant difference. The effects of SS on an individual’s quality of life have been evaluated in various studies.19, 44, 45 In these articles, the patient’s quality of life with SS was lower than that of healthy individuals in the community, especially regarding severe limitations in the physical functioning of SS patients.39, 46
Rusthen examined the effects of salivation, halitosis, chemosensory function, burning sensation of the tongue (BST), and OHRQoL in people with pSS and healthy individuals. The results showed that the case group had a lower mean OHRQOL in the following 4 subgroups of physical limitation, functional limitation, psychological limitation, and social limitation than in the control group. Stimulated and unstimulated salivary flow rates were significantly lower in Sjogren’s patients with a higher prevalence of dysgeusia, BST, and halitosis in SS, which is a sign of salivary and chemosensory dysfunction.25 Enger evaluated systemic health effects on the OHRQoL in patients with pSS and a healthy group. In this study, higher oral distress in Sjogren’s patients led to decreased OHRQoL, which had significant effects on health-related quality of life. Patients with SS in this study had a significant difference from the control group in all 14 questions. The biggest differences were seen in the subgroups of physical pain, psychological distress, and functional limitation.
Enger noted that xerostomia plays a crucial role in causing oral complications, increasing tooth decay, and leading to frequent dental visits in Sjogren’s patients. It was also mentioned in this study that oral distress has significant effects on a patient’s physical and mental health, and the powerful impact on their self-esteem, self-confidence, and social relationships is undeniable. Therefore, the main focus on oral health aspects in patients with SS is strongly recommended to improve their systemic health.12
This study is the first study to evaluate the effect of periodontal indices, DMFT, and USFR on OHRQoL in patients with SS. Despite the limited number of patients, especially patients with pSS, we used strict inclusion criteria to evaluate the effect of the disease on oral health care. We suggest that more multicenter studies be conducted with a larger sample size over a more extended period of time in the future. Another limitation of the present study was that periodontal variables such as the CAL and PPD were not measured in these patients because normal periodontal conditions or mild gingivitis were observed in the small sample size of the patients with SS we examined. It is suggested that these periodontal factors be examined in future studies.
Conclusions
In our study to evaluate OHRQoL as a dependent variable concerning the quantitative variables studied, including PI, GI, SBI, DMFT, and USFR, only the PLI in the case group was statistically significant and had a positive correlation with OHRQoL. According to the results, in addition to regular examinations and the drug treatment of patients with SS, regular oral examinations are recommended to check for dry mouth and prevent its consequences, such as dental caries and periodontal disease.
Ethics approval and consent to participate
The study was approved by the Research Ethics Committee at Mazandaran University of Medical Sciences, Sari, Iran (IR.MAZUMS.REC.1398.6148). Written informed consent was obtained from all participants prior to the commencement of the study.
Data availability
The datasets generated and/or analyzed during the current study are available from the corresponding author on reasonable request.
Consent for publication
Not applicable.