Lupus (2017) 0, 1–7

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PAPER

Impact of systemic lupus erythematosus on oral health-related

quality of life
JD Corrêa1, LGA Branco1, DC Calderaro2, SMS Mendonça1, DV Travassos3, GA Ferreira2, AL Teixeira4,
LG Abreu5 and TA Silva1
1
Department of Oral Pathology and Surgery, Universidade Federal de Minas Gerais, Belo Horizonte, Brazil; 2Department of Locomotor System,
Universidade Federal de Minas Gerais, Belo Horizonte, Brazil; 3Department of Community and Preventive Dentistry, Universidade Federal de
Minas Gerais, Minas Gerais, Belo Horizonte, Brazil; 4Department of Internal Medicine, Universidade Federal de Minas Gerais, Belo Horizonte,
Brazil; and 5Department of Pediatric Dentistry and Orthodontics, Universidade Federal de Minas Gerais, Belo Horizonte, Brazil

Oral symptoms in systemic lupus erythematosus (SLE) patients are often unexplored and
affect the health-related quality of life. The aims of this study were: (a) to evaluate the oral
health condition of SLE patients compared to control subjects without rheumatic diseases; (b)
to determine the consequences of oral health condition in the quality of life of these two
groups. Individuals with SLE (n ¼ 75) and without SLE (n ¼ 78) (control group), paired for
gender and age, underwent complete oral examination. Sociodemographic and clinical infor-
mation was obtained, and interviews were conducted using the Brazilian version of the oral
health impact profile. The activity and damage of SLE disease were assessed, respectively, by
the systemic lupus erythematosus disease activity index 2000 and the Systemic Lupus
International Collaborating Clinics/American College of Rheumatology damage index for
systemic lupus erythematosus. When we analysed the oral health condition and hygiene
habits of the participants, SLE patients exhibited an increased number of missing teeth despite
their higher frequency of tooth brushing. No significant differences were verified in other
habits and clinical parameters evaluated such as smoking, flossing, salivary flux, periodontitis,
decayed and filled teeth. Patients with SLE presented with worse oral health-related quality of
life than controls (P ¼ 0.011). The significant difference was on individuals’ physical disability
(P ¼ 0.002). The determinant of the negative impact on the oral health-related quality of life
was prosthesis wearing (P < 0.05). Overall, the oral health impact profile score was higher in
individuals with moderate SLE damage compared to SLE individuals with no damage
(P ¼ 0.043). Patients with SLE had a negative impact of oral condition on their quality of
life. The evaluation of the oral health-related quality of life might be useful to monitor the
effects of SLE on oral condition. Lupus (2017) 0, 1–7.

Key words: Systemic lupus erythematosus; oral health; quality of life

Introduction
dryness, soreness, oral ulcers, mucositis, glossitis
and periodontal disease.3–5 These oral symptoms
Systemic lupus erythematosus (SLE) is an auto- may influence the appearance and interpersonal
immune, chronic inflammatory disease, with an relationships, with reflections on economic, social
estimated incidence of 8.7 per 100,000 individuals and psychological aspects of the patients, leading to
each year in Brazil.1 SLE clinical manifestations impairment of quality of life.6
affect skin, joints, kidneys, lungs, nervous system Health-related quality of life (HRQoL) is gen-
and other organs.2 Furthermore, most SLE erally poorer in patients with SLE than in the
patients suffer from oral complaints such as general population.7 Several studies have shown
that patients’ HRQoL depends on treatment effi-
The first two authors contributed equally to this publication.
cacy and on psychosocial factors such as quality
Correspondence to: TA Silva, Universidade Federal de Minas Gerais, of social relationships.7,8 The oral health impact
Avenida Antonio Carlos 6627, Pampulha, Belo Horizonte 31270-901,
Brazil.
profile (OHIP) was introduced to measure sub-
Email: silva.tarcilia@gmail.com jects’ perceptions of the social impact of oral dis-
Received 4 January 2017; accepted 13 June 2017 orders on their wellbeing.9 There is little
! The Author(s), 2017. Reprints and permissions: http://www.sagepub.co.uk/journalsPermissions.nav 10.1177/0961203317719147
 Lupus and Oral health-related quality of life
JD Corrêa et al.
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information about the oral health-related quality SLE group and the control group were equal was
of life (OHRQoL) among individuals with rheum- rejected with a power of 87.5%. This means that
atic diseases,6,10,11 with no data regarding SLE. the statistical power with our sample size was
Thus, the aims of this study were: (a) to evaluate higher than 80%.
the oral health condition of SLE patients com-
pared to control subjects without rheumatic dis- Ethical issues
eases; (b) to determine the consequences of oral
The present study was approved by the Ethics
health condition in the quality of life of these
Committee on Human Research of the
two groups.
Universidade Federal de Minas Gerais (UFMG)
(protocol number CAAE 03128012.0.0000.5149/
2012). Individuals were asked regarding their will-
Methods ingness to participate or otherwise. If they agreed
to participate, a written informed consent form was
Participants, setting, period of recruitment and elig- signed.
ibility criteria
The present cross-sectional study was conducted Assessment of SLE disease activity and disease
in Belo Horizonte, Brazil, between 2013 and damage
2014. SLE patients with a regular follow-up at Medical records of SLE patients were reviewed in
the Rheumatology Outpatient Clinic of the order to collect information about the disease.
Medical School Hospital of Universidade Federal Disease activity was established according to the
de Minas Gerais were included in this study systemic lupus erythematosus disease activity
(n ¼ 75). The control group (n ¼ 75) consisted of index 2000 (SLEDAI 2k).12 Disease damage was
subjects without known rheumatic diseases, ran- classified using the Systemic Lupus International
domly assigned from a population of workers of Collaborating Clinics/American College of
the public health services or family and friends of Rheumatology damage index for SLE (SDI). This
SLE patients, with demographic, social and edu- tool evaluates non-reversible cumulative damage in
cational backgrounds similar to the SLE group. 12 domains according to the organ system
The exclusion criteria were: use of any medication involved.13 It was categorised as follows: SDI
with the exception of oral contraceptives, those score equal to 0 denotes no damage; SDI score of
who had been submitted to any dental treatment 1 to 3 indicates moderate damage and SDI score
within the last 6 months or had used antibiotics in higher than 3 denotes severe damage.14
the last 3 months.
The eligibility criteria for inclusion in the SLE OHRQoL evaluation instrument
group were as follows: age 18 years or greater;
diagnosis of SLE and the presence of at least The dependent variable assessed was the OHRQoL
eight teeth. Individuals with other rheumatic dis- of individuals with SLE and controls. Data were
eases, except for secondary Sjögren’s syndrome; collected through the long form of the oral health
those who had been submitted to any dental treat- impact profile (OHIP-49),15 which was developed
ment within the last 6 months; individuals with in Australia and cross-culturally adapted for use
chronic renal insufficiency requiring dialysis or in the Brazilian population.16 The OHIP-49 con-
kidney transplantation; acute or chronic infectious sists of 49 questions distributed across seven sub-
conditions at the time of the study; diagnosis scales: functional limitation (nine items), physical
of neoplasia within the last 5 years; pregnant indi- pain (nine items), psychological discomfort (five
viduals and those during breastfeeding were items), physical disability (nine items), psycho-
excluded. logical disability (six items), social disability (five
The sample power calculation was performed items) and handicap (six items). Each question
using the power and sample size calculation pro- has five response options: ‘never’ 0, ‘hardly
gram (PS, version 3.0; Nashville, TN, USA). ever’ 1, ‘sometimes’ 2, ‘fairly often’ 3, ‘very
When analysing means and standard deviations of often’ 4. The overall score is obtained by adding
overall OHIP scores for the SLE group and the up the scores of the 49 questions and ranges from
control group, the true difference in the mean 0 to 196. Scores for each of the seven subscales can
values between the SLE group and control group also be obtained independently. Superior scores
was 20.52 and the standard deviation was 40.18. denote higher negative impact on individuals’
The null hypothesis that the mean values of the OHRQoL.
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Assessment of oral outcomes the Bonferroni correction was used and P values
less than 0.007 were considered statistically
Dental caries were diagnosed using the decayed,
significant.
missing and filled teeth index according to the
Finally, multivariable linear regression analysing
World Health Organization.17 Both groups were
the OHRQoL of participants of both groups was
submitted to periodontal examination of the full
carried out. The clinical variables along with the
mouth using a periodontal probe (Hu-Friedy,
PCP 15; North Carolina University, Chicago, IL, sociodemographic and the oral behaviour variables
USA). Two trained and calibrated examiners (JDC were incorporated into the model. The sociodemo-
and SMSM) performed the periodontal examin- graphic and oral behaviour variables were incorpo-
ation. Periodontitis was defined as two or more rated into the model based on statistical
interproximal sites with clinical attachment level significance (P < 0.20). For the final model, the
(CAL) of 3 mm or greater, and two or more inter- level of significance was set at 5% (P < 0.05).
proximal sites with probing depth (PD) of 4 mm or
greater (not on same tooth) or one site with PD of
5 mm or greater.18 Results
For sialometry assessment, participants were
asked to stay 30 minutes without eating or drink- Table 1 shows the demographic and socioeconomic
ing. For unstimulated sialometry, participants were characteristics of participants. The gender distribu-
instructed to spit the saliva that accumulated in the tion was similar in both groups. The mean age for
mouth for 5 minutes in a tube. For stimulated sia- individuals of the SLE group was 38.03 years
lometry, the procedure was similar and participants ($9.80) and for individuals of the control group it
were instructed to chew a mechanic sialogogue was 41.31 years ($14.20). The level of education
during saliva collection. and the family income were not different between
SLE and control subjects.
Sociodemographic and oral hygiene variables When we analysed the oral condition and hygiene
The following sociodemographic and oral hygiene habits of the participants, we found that SLE
variables were collected: gender, age ("39 years; patients exhibited an increased number of missing
>39 years), schooling ("10 years of education; teeth despite their higher frequency of tooth brush-
#11 years of education), smoking (no; yes), tooth- ing (Table 2). No significant differences were verified
brushing ("2 times/day; #3 times/day) and flossing in habits such as smoking or flossing frequency.
(<1 times/day; #1 times/day). Family income was Similar clinical parameters such as prosthesis
evaluated in terms of the Brazilian monthly min- wearing, decayed teeth, filled teeth or periodontitis
imum wage (BMMW) which corresponded to were detected comparing the two groups.
US$300.00 at the time of the study and was defined
as the income of all economically active members of Table 1 Sociodemographic characteristics of participants of
that family ("1 BMMW; >1 BMMWs "3; >3 the SLE and control groups
BMMWs "5; >5 BMMWs). SLE, Control,
N (%) N (%) P value
Statistical analysis
Gender
Statistical analysis was carried out using the statis- Female 68 (90.7) 62 (79.5) 0.053a
tical package for the social sciences software (SPSS Male 07 (9.3) 16 (20.5)
for Windows, version 22.0; SPSS, Chicago, IL, Age (years)
"39 46 (61.3) 35 (44.9) 0.041a
USA). Descriptive analysis was performed. The >39 29 (38.7) 43 (55.1)
responses to categorical questions for each group Schooling (years of education)
were compared using the chi-square test. The "10 26 (34.7) 22 (28.2) 0.389a
responses to continuous variables for each group #11 49 (65.3) 56 (71.8)
Family income (BMMW)
were compared using the Mann–Whitney test.
"1 BMMW 08 (10.7) 06 (7.7) 0.356a
The Mann–Whitney test was also used to evaluate >1 BMMWs "3 44 (58.7) 41 (52.6)
differences in the subscale and overall OHIP scores >3 BMMWs "5 18 (24.0) 19 (24.4)
between the SLE group and the control group and >5 BMMWs 05 (6.6) 12 (15.3)
between the different SLEDAI 2K SDI categories SLE: systemic lupus erythematosus; BMMW: Brazilian monthly min-
in the SLE group. For the overall score, the level of imum wage.
significance was set at P < 0.05. For the subscales, a
Chi-square test.

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Table 2 Oral behaviours and clinical variables of participants Table 3 Comparison of oral health-related quality of life
of the SLE group and the control group between the SLE group and the control group
SLE, Control, SLE Control
N (%) N (%) P value Median Median
(mode) (mode) P value
Smoking
No 59 (78.7) 58 (74.4) 0.530b Function limitation 14.0 (0) 9.00 (0) 0.022a
Yes 16 (21.3) 20 (25.6) Physical pain 12.0 (0) 9.00 (0) 0.033a
Tooth-brushing Psychological discomfort 8.0 (0) 2.00 (0) 0.015a
"2 times/day 16 (21.3) 33 (42.3) 0.005b Physical disability 4.0 (0) 1.00 (0) 0.002a
#3 times/day 59 (78.7) 45 (57.7) Psychological disability 3.0 (0) 0.00 (0) 0.020a
Flossing Social disability 0.00 (0) 0.00 (0) 0.014a
<1 times/day 26 (34.7) 33 (42.3) 0.332b Handicap 0.00 (0) 0.00 (0) 0.018a
#1 times/day 49 (65.3) 45 (57.7) Overall score 43.00 (0) 22.00 (0) 0.011b
Prothesis wearing
No 61 (81.3) 59 (75.6) 0.392b
SLE: systemic lupus erythematosus.
a
Yes 14 (18.7) 19 (24.3)
Bonferroni correction; significant at the level P < 0.007.
b
Sialometry (unstimulated)
Mann–Whitney test; significant at the level P < 0.05.
"0.3 ml/min 09 (12.0) 03 (3.8) 0.064b
#0.4 ml/min 66 (88.0) 74 (96.2)
Sialometry (stimulated)
<1.5 ml/min 23 (30.7) 21 (27.6) 0.682b disease activity (SLEDAI) no significant differences
#1.5 ml/min 52 (69.3) 55 (72.3) of OHRQoL were detected (P > 0.05).
DMFT 13.65 (6.48)a 15.14 (7.40)a 0.160c
Table 5 shows the findings of the multivariable
Decayed teeth 1.76 (2.71)a 0.63 (0.95)a 0.013c
Missing teeth 3.73 (3.85)a 4.09 (4.63)a 0.997c linear regression for individuals with SLE and for
Filled teeth 8.33 (5.34)a 9.36 (5.53)a 0.273c individuals of the control group. In multivariate
Periodontitis regression, the only predictor of worse OHRQoL
No 24 (32.0) 37 (47.4) 0.051b was prosthesis wearing (P < 0.05) in the SLE group.
Yes 51 (68.0) 41 (52.6)

SLE: systemic lupus erythematosus; DMFT: decayed, missing, filled

tooth. Discussion
a
Mean (standard deviation).
b
Chi-square test.
c
Mann–Whitney test. To our knowledge, this is the first study assessing
the effect of oral conditions on SLE patients’ qual-
ity of life. The main findings of this study are: (a)
Unstimulated salivary flux was slightly diminished SLE patients presented with worse OHRQoL than
in SLE patients but no significance was observed controls with the main impact upon individuals’
(Table 2). It is important to mention that none of physical disability; (b) prosthesis wearing was inde-
the SLE patients reported the use of any saliva sub- pendently associated with worse OHRQoL; (c) the
stitute or stimulant. comparison among SDI categories showed that
Table 3 displays the results of the comparison of SLE patients with moderate damage had worse
OHRQoL between the SLE and control groups. OHRQoL than those with no damage.
The individuals of the SLE group presented with Chronic diseases such as SLE affect not only
a higher OHIP overall score compared to the indi- patients’ physical health, but also their behaviour,
viduals of the control group (P ¼ 0.011). Therefore, social and psychological aspects.19 Therefore, it is
the OHRQoL was more deteriorated among indi- important to consider disease activity and damage
viduals of the SLE group. The significant domain as well as subjective parameters, such as the
affected was individuals’ physical disability (phys- HRQoL, during the follow-up of affected individ-
ical disability subscale, P ¼ 0.002). uals. HRQoL is a measure of a patient’s physical
Table 4 presents the comparison of OHRQoL and functional health.20 Studies have reported that
between the different categories of SLEDAI 2K SLE patients have a reduced HRQoL comparable
and SDI in the SLE group. Individuals with a mod- to their counterparts with severe medical diseases,
erate damage (SDI score of 1–3) had a worse such as AIDS, rheumatoid arthritis and dia-
OHRQoL, demonstrated by a significant higher betes.19–21 As poor quality of life is a determinant
overall OHIP score than individuals with no of reduced treatment compliance,7 the 2010
damage (SDI score equal to 0) (P ¼ 0.043). European League Against Rheumatism guidelines
Comparing SLE patients with different scores of for monitoring patients with SLE recommended
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Table 4 Median (mode) of overall and subscale OHIP scores according to SLEDAI and SDI categories
Function Physical Psychological Physical Psychological Social Overall
limitation pain discomfort disability disability disability Handicap score
Median Median Median Median Median Median Median Median
(mode) (mode) (mode) (mode) (mode) (mode) (mode) (mode)

SLEDAI
0 15.0 (16) 12.5 (9) 7.0 (0) 4.0 (0) 3.0 (0) 0.0 (0) 0.5 (0) 39.0 (17)
1 13.0 (0) 12.5 (0) 9.0 (0) 3.0 (0) 3.5 (0) 0.0 (0) 0.0 (0) 41.0 (0)
P valuea 0.809 0.733 0.638 0.394 0.873 0.619 0.407 0.998
SLEDAI
0 15.0 (16) 12.5 (9) 7.0 (0) 4.0 (0) 3.0 (0) 0.0 (0) 0.5 (0) 39.0 (17)
2 16.0 (2) 12.0 (0) 6.0 (0) 7.0 (0) 0.0 (0) 0.0 (0) 2.0 (0) 50.0 (2)
P valuea 0.961 0.921 0.634 0.392 0.496 0.664 0.468 0.98
SDI
0 12.0 (0) 12.0 (0) 4.0 (0) 3.0 (0) 1.0 (0) 0.0 (0) 0.0 (0) 40.0 (2)
1 15.0 (16) 13.0 (3) 10.0 (20) 4.0 (0) 8.0 (0) 0.0 (0) 1.0 (0) 53.0 (17)
P valuea 0.094 0.238 0.041 0.287 0.043 0.055 0.112 0.043
SDI
0 12.0 (0) 12.0 (0) 4.0 (0) 3.0 (0) 1.0 (0) 0.0 (0) 0.0 (0) 40.0 (2)
2 13.0 (13) 4.0 (18) 9.0 (0) 4.0 (0) 4.0 (0) 0.0 (0) 0.0 (0) 25.0 (3)
P valuea 0.842 0.818 0.368 0.604 0.385 0.548 0.815 0.668
a
Mann–Whitney test.
For the subscales, Bonferroni correction was applied; significant at the level P < 0.007.
For the overall score, significant at the level P < 0.05.
OHIP: oral health impact profile; SLEDAI: systemic lupus erythematosus disease activity index; SDI: Systemic Lupus International Collaborating
Clinics/American College of Rheumatology damage index for systemic lupus erythematosus.
SLEDAI 0: no disease activity; SLEDAI 1: moderate disease activity; SLEDAI 2: severe disease activity.
SDI 0: no damage; SDI 1: moderate damage; SDI 2: severe damage.

Table 5 Linear regression model evaluating the impact of oral that HRQoL should be assessed at every scheduled
conditions on the quality of life of individuals of SLE and the appointment.22
control group Oral health is an essential part of general health
SLE group Control group and significantly influences individuals’ quality of
life. The OHIP-49 is a questionnaire that evaluates
! Standard ! Standard
coefficient error coefficient error dysfunction, discomfort and disability attributed to
oral conditions.16 In this study the OHIP-49 was
Gender used and the data obtained showed that SLE
Female; male 0.070 17.55 –0.155 9.21
patients presented with worse OHRQoL. Similar
Age (years)
"39; >39 0.214 13.11 –0.031 9.64 results have been shown for patients with other
Toothbrushing rheumatic diseases such as Sjögren’s syndrome,
"2 times/day; 0.008 13.61 –0.157 7.58 fibromyalgia, rheumatoid arthritis and systemic
#3 times/day
sclerosis.6,11
Sialometry (unstimulated)
"0.3 ml/min; 0.009 19.49 –0.020 19.30
The domain of OHRQoL affected in SLE
#0.4 ml/min patients was physical disability and this was prob-
Sialometry (stimulated) ably caused by prosthesis wearing. Previous studies
<1.5 ml/min; –0.092 12.79 0.09 8.34
#1.5 ml/min
have demonstrated that the need for dental pros-
Prothesis wearing thesis or the current use of dental prosthesis pro-
No; Yes –0.300 16.86a –0.048 11.69 duced detrimental effects on OHRQoL.23,24 Despite
DMFT the general improvement in OHRQoL shortly after
Decayed teeth –0.407 5.88 –0.053 0.88
rehabilitation with partial dentures, a long-term
Missing teeth 0.438 6.17 0.206 3.94
Filled teeth 0.541 6.37 0.282 1.35
opposite effect can be observed. Furthermore,
Periodontitis 0.577 6.04 0.229 1.00 whether prosthesis replaces few teeth or the entire
No; Yes 0.122 12.29 0.114 8.46 arch of teeth needs observation. One important
a
P < 0.05.
aspect of our sample was the use of a minimum
SLE: systemic lupus erythematosus; DMFT: decayed, missing, filled number of teeth as inclusion criteria, resulting in
teeth. the exclusion of 62 SLE patients.5 This fact may
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have underestimated the impact of the prosthesis In conclusion, SLE has a negative impact on the
wearing in OHRQoL in our study. individuals’ OHRQoL. As SLE is a complex dis-
The negative effects on OHRQoL of individuals ease, a wide range of factors regarding its onset and
wearing partial dentures might be explained by the progression remains underappreciated and poorly
development of dental caries and/or periodontal understood. The OHRQoL might be useful to
disease on the remaining teeth over time. Previous evaluate the effects of SLE on the oral condition
studies25,26 have shown that SLE patients are more and to monitor the consequences reflected by the
affected by periodontitis. Our data demonstrated impairment in patients’ quality of life. The results
that SLE patients tended to be more affected by presented here highlighted that SLE requires an
periodontitis, but the difference was not significant. interdisciplinary intervention for its care, with
In addition, complications such as ill-fitting, dis- dental assistance and follow-up for patients, to
comfort of the new prosthesis and inflammation improve the quality of life of the affected popula-
of the supported mucosa could have negatively tion, as the psychosocial aspects may contribute to
impacted OHRQoL.27 Regarding function, the complexity of the development and exacerba-
instability of the prosthesis, problems with speech tion of SLE symptoms.
and a feeling of having something in the mouth also
had a negative impact on the patients.27 Prosthesis
wearing can also affect the patients’ diet, causing Declaration of conflicting interests
pain when chewing and leading to the avoidance of
some kinds of food. These complications may
explain the impact on SLE individuals’ physical The authors declared no potential conflicts of inter-
function that was observed in the present study. est with respect to the research, authorship, and/or
Despite the fact that no difference in prosthesis publication of this article.
wearing was found between SLE patients and
healthy subjects, it seems to disturb SLE patients
more. This fact is probably related to the SLE oral Funding
symptoms, e.g. hyposalivation.28 In fact, previous
studies have found that about 79% of SLE patients The authors disclosed receipt of the following
suffered from hyposalivation.28 Despite no signifi- financial support for the research, authorship,
cant changes in sialometry being detected compar- and/or publication of this article: Fundação de
ing the groups, we observed that unstimulated Amparo a Pesquisa do Estado de Minas Gerais
saliva is very close to the inferior limit in SLE (grant/award number APQ-01138-15).
patients. Although sialometry is the best way to
diagnose hyposalivation, it does not necessarily
reflect the self-reported dry mouth sensation or xer- References
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