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Year : 2020  |  Volume : 23  |  Issue : 2  |  Page : 159-164

Oral health related qualıty of lıfe and dısease severıty ın autoımmune bullous dıseases

1 Seydisehir State Hospital, Dermatology Clinic, Seydisehir, Konya, Turkey
2 Ondokuz Mayis University, Faculty of Medicine, Department of Dermatology, Samsun, Antalya, Turkey
3 Ondokuz Mayis University, Faculty of Dentistry, Department of Dentomaxillofacial Radyology, Samsun, Antalya, Turkey
4 Ondokuz Mayis University, Faculty of Dentistry, Department of Periodontology, Samsun, Antalya, Turkey
5 Kepez State Hospital, Dermatology Clinic, Antalya, Turkey
6 Akdeniz University, Faculty of Medicine, Biostatistics and Medical Informatics Department, Antalya, Turkey
7 Department of Health Management, Marmara University Faculty of Health Sciences, İstanbul, Turkey
8 Akdeniz University, Faculty of Medicine, Department of Dermatology and Venereology, Antalya, Turkey

Date of Submission18-Apr-2019
Date of Acceptance10-Sep-2019
Date of Web Publication7-Feb-2020

Correspondence Address:
Dr. A Bilgic
Seydisehir State Hospital, Dermatology Clinic, Seydisehir, Konya
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Source of Support: None, Conflict of Interest: None

DOI: 10.4103/njcp.njcp_216_19

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Background: There is an increased risk of long-term dental and periodontal disease in autoimmune bullous diseases (AIBD). Aims: In this cross-sectional study, we aimed to determine whether the oral health-related quality of life status (OHRQoL) was associated with disease severity and activity in patients with AIBD. Subjects and Methods: 67 patients with AIBD were enrolled in this study. Autoimmune Bullous Skin Disorder Intensity Score (ABSIS) was used to evaluate the disease severity. The score was categorized as a significant course (≥17) and moderate course (<17). Oral health impact profile-14 (OHIP-14) questionnaire was filled to assess the OHRQoL. Self-reported oral health status and oral lesion related pain score were also evaluated in the study group. Results: OHIP-14 score was significantly higher in active patients (42.28 ± 13.66) than inactive patients (29.08 ± 12.25) (P = 0.004) and it was correlated with the pain score (6.33 ± 2.78; r = 0.409, P = 0.013). Furthermore, OHIP-14 score was higher in patients with a significant disease course (45.18 ± 15.08) (P = 0.010) than in patients with a moderate course (36.09 ± 9.73). Conclusions: OHRQoL may be useful in the disease management and treatment. Since it can be affected by both presence of oral erosions and disease severity, a collaboration between dermatologists and dentists could be crucial to the disease management in AIBD.

Keywords: Autoimmune bullous diseases, bullous pemphigoid, health related quality of life, oral health, pemphigus vulgaris

How to cite this article:
Bilgic A, Aydin F, Sumer P, Keskiner I, Koc S, Bozkurt S, Mumcu G, Alpsoy E, Uzun S, Akman-Karakas A. Oral health related qualıty of lıfe and dısease severıty ın autoımmune bullous dıseases. Niger J Clin Pract 2020;23:159-64

How to cite this URL:
Bilgic A, Aydin F, Sumer P, Keskiner I, Koc S, Bozkurt S, Mumcu G, Alpsoy E, Uzun S, Akman-Karakas A. Oral health related qualıty of lıfe and dısease severıty ın autoımmune bullous dıseases. Niger J Clin Pract [serial online] 2020 [cited 2021 Jun 12];23:159-64. Available from:

   Introduction Top

Autoimmune bullous disorders (AIBD) cover a wide variety of diseases such as pemphigus vulgaris (PV), bullous pemphigoid (BP), their subtypes and paraneoplastic pemphigus (PNP), cicatricial pemphigoid (CP), linear IgA dermatosis, epidermolysis bullosa acquisita (EBA). Erythematous and erosive areas with vesiculobullous lesions in oral tissues are common findings in AIBD and referred as desquamative gingivitis, when occurred in gingiva.[1] It is a matter of discussion in the literature whether desquamative gingivitis could have an impact on increasing the risk of periodontal tissue disruption (periodontitis) in patients with AIBD. AIBD patients may also have difficulty to continue efficient and effective oral hygiene practices (effective tooth brushing, etc.) due to the discomfort caused by oral lesions. These factors can prevent patients to visit their dentists for their regular check-ups. This results in ineffective oral hygiene applications and plaque accumulation. This figure may cause increased risk of long-term dental and periodontal disease in PV.[2] Increase in microbial plaque accumulation and gingival inflammation was demonstrated in patients with mucous membrane pemphigoid. Periodontal disease progression was influenced by the increase in disease duration poorly.[3] Oral lesions can affect all oral functions such as communication, social interaction and psychosocial well-being negatively.[4],[5],[6],[7],[8],[9] In the available literature, OHRQoL and oral health was examined in patients with ulcerative lichen planus, recurrent aphthous stomatitis, Behcet's disease and some AIBD.[2],[9],[10],[11],[12],[13],[14],[15] Since disease severity could also affect the presence of oral ulcer/erosions, the aim of this study was to evaluate the association between OHRQoL and disease severity in patients with AIBD.

   Methods Top


In the study, 67 patients (F/M: 40/27; mean age 53.48 ± 15.27 years) with AIBD (63 PV and 4 BP) and 35 healthy subjects (F/M: 20/15; 54.86 ± 7.1 years) attending two Universities Dermatology and Venerology Outpatient Clinics were included in compliance with the principles of the Declaration of Helsinki. The study was approved by the local ethics committee (13.11.2007/588). Systemic corticosteroid (CS) therapy (Methylprednisolone at 0.5 mg to 1.0 mg/kg/day, usually not more than a total dose of 60 mg daily) was started as the mainstay therapy of AIBD during new diagnosis and relapses. CSs dose was decreased by 8 mg every 2 or 4 weeks if clinical improvement continued, or no relapse was seen. When patients achieved 16 mg/day methylprednisolone dose, tapering was lessened to 4 mg every month. The dose of immunosuppressive agents (mainly azathioprine, mycophenolate mofetil, etc.) would have reduced and stopped if patient stayed in a 6 month-remission period after ceasing CS therapy. Local and intralesional CS therapy is used in combination with systemic therapies to provide faster pain relief and healing process for active lesions in a limited area.[16]

Control subjects were enrolled from the patients who visited the dermatology clinic during the study period and who did not have AIBD. Control subjects did not have any inflammatory disorder and a relation with the patient's family.

Data was collected by a structured form including demographic properties (age, disease duration, previous therapies, frequency of flares of oral lesions, healing time of oral lesions, the duration after the last flare), disease severity scores in terms of Autoimmune Bullous Skin Disorder Intensity Score (ABSIS) and Oral Health Impact Profile with 14 items (OHIP-14), generic quality of life questionnaires (SF-36), self-reported oral health status and pain score due to oral lesions. The term of frequency of flares of oral lesions was accepted as defined by Murrell et al., as having 3 or more new lesions in a month that do not heal spontaneously within 1 week, or by the extension of established lesions, in a patient who has achieved disease control.[17] Patients with a definitive diagnosis of AIBD based on typical clinical, histopathological and immunofluorescence analysis were enrolled in this study. The clinical disease severity scores of patients were determined in terms of ABSIS as described by Pfutze et al., which is a specific tool showing disease activity according to a standard scoring scheme.[18] The suggested cut-off values differentiating moderate, significant and the extensive pemphigus were 17 and 53 for ABSIS as defined in the recent study of Boulard et al.[19] Since extensive disease was so limited, we only used cut-off values of 17 for ABSIS for comparisons. Patients who were pregnant, who have chronic inflammatory diseases, psychiatric disorders, cancer and other oral mucosal disorders were excluded from the study.

Patient reported outcome measures

Oral health-related quality of life status was evaluated by OHIP-14.[10],[20],[21],[22] A 5-point Likert-type scale was used in scoring each item of the OHIP-14. Total OHIP-14 scores ranged from 0 (no impact) to 56 (all the oral health problems were experienced very often). High scores indicated a poor oral quality of life.[20] The Turkish version of OHIP-14 was found to be valid and reliable in a previous study by Mumcu et al.[22] Self-reported oral health status was also evaluated by a 5-point Likert- type scale. Responses were coded as: 1 = very bad, 2 = bad, 3 = moderate, 4 = good, 5 = Very good. Then, the self-reported oral health status of patients was categorized as good (very good/good) or poor (very bad/bad/neutral) for the analysis. In addition, pain score due to oral lesions was assessed by using a visual analogue scale with 100 mm (0 = no pain and 100 = very severe pain). The other quality of life questionnaire was 36 item Short Form (SF-36) as a generic quality of life measure. The SF-36 assesses health-related quality of life with 36 items in 8 subgroups regarding physical functioning, role physical, bodily pain, general health, vitality, social functioning, role emotional and mental health. These scales are scored from 0 to 100 following a standard algorithm.[23] The SF -36 questionnaire was translated into Turkish and validated by Kocyigit et al.[24] High scores indicated a better health-related quality of life.[23],[24] Following the initial dermatological examination, the patients were asked to complete these questionnaires.

Oral health assessment

The dental and periodontal status of 27 active patients and 35 controls were examined on the same day with their dermatological examinations. Oral health was evaluated by periodontal indices including the plaque index (PI), gingival index (GI), probing depth (PD), and clinical attachment loss (CAL).[25],[26] Plaque index defines the thickness of microbial plaque accumulation at the gingival area, gingival index evaluates the severity of gingivitis, PD and CAL assess the state of periodontal health. Williams periodontal probe (Hu-Friedy, Chicago, IL, USA) was used to do all probings and 6 sites (buccal, lingual, mesio-lingual, mesio- buccal, disto-lingual and distobuccal) for each tooth were documented. A previously calibrated examiner performed all clinical assessments. Calibration of probing pocket depth and clinical attachment loss was achieved by the examination of 2 patients twice, 24 h apart, before the beginning of the study. Calibration was accepted if measurements at baseline and at 24 h were within 0.5 mm at a 90% confidence level.

Statistical analysis

Continuous variables are presented as a mean ± standard deviation, while categorical variables are given as percentages. The Kolmogorov-Smirnov test was used to verify the normality of the distribution of continuous variables. Statistical analysis of clinical data between two groups consisted of unpaired t-tests for parametric data and Mann Whitney U test analysis for nonparametric data. Correlations were assessed with Spearman correlation coefficients and the Chi-square test was used for categorical variables. Cronbach-alpha values for internal reliability were observed to be very high for OHIP-14 (0.933) and SF-36 (0.898) in the study. Analyses were performed with PASW 18 (SPSS/IBM, Chicago, IL, USA,) software, and two-tailed P value of less than 0.05 was considered statistically significant.

   Results Top

The mean duration of AIBD was 65.22 ± 70.44 months. In the study group, the duration after the last flare, the frequency of flares and healing time of oral lesions were 3.88 ± 8.35, 2.42 ± 3.84, 0.78 ± 0.88 months, respectively [Table 1]. Significant correlation was observed between the healing time of oral lesions and age (53,48 ± 15,27) (r = 0.56, P = 0.037). The mean ABSIS of patients was 26.43 ± 28.49. Scores of OHIP-14, self-reported oral health status and oral lesion related pain were 40 ± 14.28, 2.87 ± 0.52 and 6.33 ± 2.78, respectively [Table 1]. OHIP-14 score was correlated with ABSIS (r = 0.344, P = 0.013), the pain-score due to oral lesions (r = 0.409, P = 0.013) and self-reported oral health status (r = −0.374, P = 0.019). Fifty-five patients (82.1%) with AIBD had active disease in dermatological and oral examinations whereas the others were inactive ones (n = 12, 17.9%). The OHIP-14 score was significantly higher in active patients (42.38 ± 13.66) than inactive ones (29.08 ± 12.25) (P = 0.004). Moreover, it was also higher in patients whose self-reported oral health status was poor compared to good ones [Table 1]. Among SF-36 subgroup scores, the lowest score was observed in SF-36 General health subscale (50.18 ± 21.45), whereas the highest score was seen in SF-36 Physical functioning (70.62 ± 29.23) in patients with AIBD [Table 1]. Patients were categorized according to the cut-off point (moderate: <17 vs significant: ≥17) of ABSIS. The OHIP-14 score was lower in patients with the moderate course (36.09 ± 9.73) than the significant course (45.18 ± 15.08) (P = 0.034). Moreover, scores of SF-36 bodily pain and vitality were lower in significant course compared to those of moderate course (P = 0.015; P = 0.010, respectively) [Table 2]. Periodontal health could be evaluated almost 49,1% of active patients (n = 27; moderate course: 14 vs significant course: 13 according to ABSIS score). The mean PI and GI were significantly higher in patients with AIBD (PI: 2.19 ± 0.57, GI: 1.91 ± 0.42) than that in healthy controls (PI: 1.67 ± 0.40, GI: 1.53 ± 0.27), respectively (P < 0.001, both for PI and GI). No statistically significant difference was observed in the number of teeth, PD and CAL between patients with AIBD (17.96 ± 7.69; 2.36 ± 0.61; 3.26 ± 1.17, respectively) and HC (18.17 ± 6.14; 2.25 ± 0.41; 2.72 ± 0.54, respectively (P > 0.05) [Table 3]. There was no correlation between the OHIP-14 score and periodontal scores and the number of natural teeth (P > 0.05).
Table 1: Disease Related Factors, Oral Involvement and Quality of Life Status in AIBD

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Table 2: OHIP-14 and SF-36 Scores in AIBD patients According to Disease Severity

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Table 3: Scores of Periodontal indices According to Active Patients with AIBD and Healthy Control Group

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   Discussion Top

Some dermatologic diseases such as lichen planus, lupus erythematosus, erythema multiforme, PV and some pemphigoid lesions present with oral manifestations. The impact of oral mucosal diseases on daily life is easily monitored by using patient- based outcome measures (PROMs) in the disease management.[4],[5],[10],[22],[27] Since they reflect psychosocial changes, functional status and control of symptoms,[28] OHRQoL as a PROM is commonly used to understand patients' conditions in oral medicine,[4],[22],[29] and to assess the efficacies of treatment protocols in clinical practice.[27],[30],[31],[32],[33],[34] Close associations were seen among oral involvement and OHRQoL in patients with AIBD in the present study. Impaired OHRQoL was observed in active patients and patients with significant disease course. As related to them, poor OHRQoL was associated with oral lesion related pain and poor self-reported oral health status. Oral mucosa involvement with painful ulcerations and erosions could be the initial symptoms of PV.[35] Oral diseases affect oral functions, communication, social interaction and psychosocial well-being negatively.[4],[5],[6],[7],[8],[9] Therefore these results could be predicted due to painful oral lesions and/or erosions in this patient group.[35],[36] Similarly, poor OHRQoL was seen in patients with ulcerative lichen planus, recurrent aphthous stomatitis and Behcet's disease.[4],[10],[11],[12],[22] In a study from the UK, 200 patients regarding 100 oral lichen planus, 42 recurrent aphthous stomatitis and 58 vesiculobullous diseases (mucous membrane pemphigoid or pemphigus vulgaris) had poor OHIP-14 score suggesting the impact of oral lesions in these patients.[36] OHIP-14 score was also found to be high in AIBD patients compared to that of Behcet's disease.[22] In this frame, OHRQoL status could be different according to oral lesion pattern regarding activity and healing time of oral lesions.[22] Microbial plague accumulation and gingival inflammation were found to be high in patients with AIBD compared to controls in the present study. Patients could be afraid of causing new oral lesions or aggravating lesions with oral hygiene applications.[12] Moreover, they are less likely to visit the dentist due to the discomfort caused by painful oral lesions.[2] As predicted, lesions may lead to ineffective oral hygiene measures and allow plaque accumulation that causes gingival inflammation and may enhance the risk of attachment loss in AIBD.[2],[12],[13],[14],[15] Impaired oral health in PV patients was previously revealed by using CPITN index by Akman et al.[2] Periodontal health could be related with clinical severity of PV.[14] Furthermore, PV might also act as a trigger for the development and/or progression of periodontitis as damaged oral mucosa might increase presenting antigenic epitopes to activate the autoimmune response.[2] Furthermore, the increase in gingival index scores in AIBD patients should be evaluated with caution due to the similarities of erythema resulting from the AIBD morphology and plaque-induced inflammation.[3]

Oral hygiene therapy and professional recommendations could be helpful to reduce gingival inflammation and to improve patient-related outcomes in AIBD.[12] It is suggested that increased inflammatory mediators and acute-phase proteins due to periodontitis may have an impact on the development of several systemic diseases.[37],[38],[39] Inflammatory changes related to autoantibodies resulted in the periodontal tissue breakdown. This may be another reason in periodontitis in AIBD patients. In addition, immunosuppressive drugs that are frequently used in the treatment of AIBD have potential to diminish immune response and may lead to bacterial-elicited inflammatory tissue damage.[3],[40]

The evaluation of health-related quality of life status is seen increasingly in health care because the effects of treatment protocols on symptoms are easily monitored.[41] Scores of OHIP-14, SF-36 Bodily pain and SF-36 Vitality as PROMs were poor in patients with significant group (ABSIS score ≥17) compared to those of moderate group (ABSIS <17). Since oral involvement is commonly seen in this patient group, these results could be predicted due to connections of oral and general health. Moreover, SF-36 scores could be associated with clinical severity in clinical practice of PV as predicted.[42] In the present study, oral health, OHRQoL status and its related factors were evaluated in patients with AIBD. OHRQoL status was found to be related with both disease severity and disease activity in the study group. This is crucial information for the disease management of patients with AIBD by the collaborations of dermatologist and dentists.

However, the study has some limitations. Firstly, the study design was cross-sectional and study subjects from only two university hospitals were enrolled in this study. Secondly, oral health could be examined in almost half of the group. Therefore the results should be evaluated within the limitations of the study. Consequently, the severity of oral involvement in patients with AIBD could play a role in the prediction of disease course.

Since OHRQoL was affected by both activity of oral lesions and disease severity, it might be helpful for dermatologists in the clinical decision- making process of treatment protocols. AIBD patients should be informed about oral health problems and encouraged to go for dental follow-up visits. Therefore, the collaboration between dermatologists and dentists may contribute to the disease management in AIBD.

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Conflicts of interest

There are no conflicts of interest.

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  [Table 1], [Table 2], [Table 3]


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