Med Oral Patol Oral Cir Bucal. 2018 Jul 1;23 (4):e391-400.

Oral lesions in Sjögren’s syndrome patients

Journal section: Oral Medicine and Pathology doi:10.4317/medoral.22286

Publication Types: Review http://dx.doi.org/doi:10.4317/medoral.22286

Oral lesions in Sjögren’s syndrome: A systematic review

Julia Serrano 1, Rosa-María López-Pintor 1, José González-Serrano 1, Mónica Fernández-Castro 2, Elisabeth

Casañas 1, Gonzalo Hernández 1

1
Department of Oral Medicine and Surgery, School of Dentistry, Complutense University, Madrid, Spain
2
Rheumatology Service, Hospital Infanta Sofía, Madrid, Spain

Correspondence:
Departamento de Especialidades Clínicas Odontológicas
Facultad de Odontología
Universidad Complutense de Madrid
Plaza Ramón y Cajal s/n, 28040 Madrid. Spain
Julia.serrano.valle@gmail.com
Serrano J, López-Pintor RM, González-Serrano J, Fernández-Castro M,
Casañas E, Hernández G. Oral lesions in Sjögren’s syndrome: A system-
atic review. Med Oral Patol Oral Cir Bucal. 2018 Jul 1;23 (4):e391-400.
Received: 18/11/2017 http://www.medicinaoral.com/medoralfree01/v23i4/medoralv23i4p391.pdf
Accepted: 09/05/2018

Article Number: 22291 http://www.medicinaoral.com/

© Medicina Oral S. L. C.I.F. B 96689336 - pISSN 1698-4447 - eISSN: 1698-6946
eMail: medicina@medicinaoral.com
Indexed in:
Science Citation Index Expanded
Journal Citation Reports
Index Medicus, MEDLINE, PubMed
Scopus, Embase and Emcare
Indice Médico Español

Abstract
Background: 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.
Material and Methods: 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).
Results: 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.
Conclusions: OL are common and more frequent in SS patients when compared to a CG. This may be a conse-
quence of low levels of saliva. More studies where these OL and all the possible cofounding factors are taken into
account are needed.

Key words: Sjögren’s syndrome, oral lesions, oral diseases, oral manifestations, oral disorders, systematic re-
view.

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Med Oral Patol Oral Cir Bucal. 2018 Jul 1;23 (4):e391-400. Oral lesions in Sjögren’s syndrome patients

Introduction two independent researchers (JS, JGS). The search strat-

Sjögren’s syndrome (SS) is one of the most frequent au- egy used was: (“Sjögren syndrome” OR “Sjögren’s syn-
toimmune rheumatic diseases. It affects 0.5-1% of the drome”) AND (“oral manifestations” OR “oral lesions”
population, occurring more middle-aged women than OR “mucosal lesions” OR “oral diseases” OR “oral
in men, with a ratio of 9:1 (1). Although it can appear at pathology” OR “oral mucosal alterations” OR “oral re-
any age, it usually arises between the fourth and sixth percussions”) according to each database (Fig. 1). Fur-
decade of life. SS is a systemic exocrinopathy of un- thermore, an additional hand search was performed to
known aetiology, which mainly affects the lacrimal and find potential eligible studies as reference lists of review
salivary glands giving rise to dry eyes and hyposaliva- articles and relevant studies.
tion. It may manifest as primary SS (pSS), which occurs -Study selection
as an isolated disease, or as secondary SS (sSS) when it •Inclusion criteria. Full-text articles were included re-
appears simultaneously with other autoimmune disease gardless of time period of study and year of publication.
(1-3). There have been many classification criteria sug- Types of studies. The studies included had to be (a) orig-
gested for pSS (4,5). Nowadays, the most widely used is inal articles published in scientific journals, (b) cross-
the one proposed by the American-European Consen- sectional or cohort studies, (c) comparative studies (SS
sus Group in 2002 (6). Other diagnosis criteria also ac- group and CG), if available, (d) only in humans, and (e)
cepted are the ones proposed by the American College written in English language.
of Rheumatology and the Sjögren’s International Col- Types of population. Individuals with SS that could
laborative Clinical Alliance for pSS (7). have pSS and sSS (no restriction for SS diagnosis clas-
Saliva has an important role in preserving oral health. sification criteria was applied). CG population had to be
Therefore, hyposalivation (or hyposialia) frequently healthy patients.
increases the risk for different oral problems such as Outcomes. We considered oral alterations, oral manifes-
tooth decay, periodontal disease or fungal infections tations and oral repercussions as OL. Neither xerosto-
(8-13). Tongue alterations and non-specific ulceration mia nor hyposialia were included as OL. In addition, we
have also been reported (9,14). The association between did not include dental lesions or periodontal disease. We
SS and oral lesions of autoimmune aetiology as lichen considered oral candida lesions when clinical changes,
planus, recurrent aphtous stomatitis, pemphigus vulgar- such as angular cheilitis, atrophic glossitis, erythema-
is and mucous membrane pemphigoid remains unclear tous candidiasis, pseudomembranous candidiasis, or
(15). median rhomboid glossitis were described. We did not
This is the first systematic review that unifies all the oral consider only positive cultures as OL. The studies must
lesions (OL) -non-xerostomia and/or hyposalivation- evaluate the presence of oral mucosal lesions and spec-
shown in the SS patients. The objective of the present ify the number and/or percentage in the SS group, and
study was to evaluate which OL are the most frequent the CG, if available.
in SS patients and compare them with a control group •Exclusion criteria. (a) Those articles published in a
(CG). Knowing this, future dental protocols could be language other than English, and (b) review articles,
carried out, with the aim of improving SS patient’s oral experimental studies, case reports, commentaries and
health and quality of life. letters to the Editor.
-Data collection and extraction
Material and Methods Two independent researchers (JS and JGS) compared
This systematic review was conducted according to the search results to ensure completeness and then du-
Preferred Reporting Items for Systematic Reviews and plicates were removed. Both reviewers individually
Meta-Analyses Protocols (PRISMA-P) 2015 statement screened all full title and abstract of the identified ar-
(16). ticles. Differences in eligible studies were resolved by
-Focused question discussion with a third reviewer (RMLP). Relevant
Based on the PRISMA guidelines, 2 focused PICO full-text articles were obtained, and checked for eligi-
(population, intervention, comparison, and outcome) bility using the following standard abstraction forms:
questions were constructed: 1) Which are the most fre- first authors, journal, country in which was conducted,
quent OL (non-xerostomia and/or hyposalivation) in SS title of the paper, type of study, recruitment of patients,
patients? 2) Do SS patients have a higher prevalence of sample characteristics (population, age, and gender of
these OL when compared to a CG? SS patients and CG, when available), type of SS, diag-
-Search Strategy nosis criteria for SS, and oral mucosal diseases diagno-
A comprehensive search of the scientific literature was sis criteria (Table 1, 1 continue). In Table 2, 2 continue,
conducted without date restriction until September 1st we reported the prevalence of the different OL in SS
2017, in the following databases: PubMed/MEDLINE, patients and CG and, the statistical signification if there
Scopus, Web of Science and The Cochrane Library by was CG, and it was available.

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Fig. 1. Flow diagram of the literature search, according to the Preferred Report-
ing Items for Systematic Reviews and Meta-Analyses (PRISMA).

-Quality Assessment (when available), were recorded in Table 2, 2 continue.

The Joanna Briggs Institute Prevalence Critical Ap- A meta-analysis was not possible to carry out due to the
praisal Tool (JBI) for Studies Reporting Prevalence differences between the selected papers: different types
Data (17) was used to evaluate the methodological qual- of SS, different SS diagnosis criteria, lack of agreement
ity of the selected studies (Table 3). in OL diagnosis, and absence of healthy CG in some of
A study was considered to have a low quality assess- the studies.
ment if a 0-5 criteria was met, and high quality assess-
ment if studies met 5-10 criteria. Two reviewers (JS and Results
JGS) conducted independently a critical appraisal, com- -Study selection
paring and discussing afterwards their results. If the The search strategy yielded 467 results, of which 310
two reviewers disagreed on the final critical appraisal, a remained after removing duplicates. We screened all
third reviewer (RMLP) was required. the titles, excluding those written in any language other
-Categorization of Studies than English, and those that were out of scope of re-
In order to clarify the results, we categorized the stud- view, obtaining a total of 56 eligible publications. Then,
ies in different groups: 1) studies which determine the two independent researchers (JS and JGS) reviewed all
prevalence of any type of OL, 2) studies which only de- the titles and abstracts, and excluded those that were
termine the prevalence of Candida albicans lesions and reviews, case reports or did not specify oral disorders.
3) studies which determine the prevalence of OL of au- Due to the study populations in the papers carried out
toimmune aetiology. by Soto-Rojas (14,18) were exactly the same (with the
-Data items and synthesis of results same result data) we considered both publications as
The prevalence of oral mucosal lesions from the in- only one article in order to unify the oral manifesta-
cluded studies was presented as a percentage. This tions. The same resolution was taken for those carried
percentages and their statistical significance, when out by Rhodus (19,20). Thirty-six studies, which did not
available, shown along with the number of SS and CG
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Table 1. Study characteristics.

Author Type of Patients Sample Mean Gender Type of SS Oral mucosal evaluation
Journal study recruited at (Denture age (F %) SS Classification
Country wearers) (years) criteria

(1) Studies which determine the prevalence of any type of oral lesions
Pedersen et al; 1999 Cross- School of SS 16 (4) SS 61.5 SS 87.5% pSS 16 Examination, mirror test and
Oral Diseases sectional Dentistry, CG 27 Aged CG CG 92.5% European oral smears
Norway University of (2) 50 classification
Copenhagen, Young criteria (1993)
Dental CG 24
Department,
Rigshospitalet
Patinen et al; 2004 Cross- - CD+SS CD+SS 100% pSS 40 WHO recommendation
Oral Diseases sectional 20 (-) 61 AECG (2002) (1987)
Finland SS 20 (-) SS 62

Koseki et al; 2004 Cross- Ichikawa General SS 54 SS - Not determined. Calibration trial between the
Oral Diseases sectional Hospital, Tokyo (0) 58.09±10 Fox criteria examiner and patients and
Japan Dental College CG 51 .61 (1986) which selective medium Candida
(0) CG fixed the AECG Color
50.98±15 (2002)
.03
Márton et al; 2006 Cross- University of SS 49 SS 55±11 SS 93.8% pSS 49 Visual examination
Oral Diseases sectional Debrecen (26) CG 90.6% according to a standard
Hungary CG: Hajdú-Bihar CG AECG (2002) procedure (Langlais et al.,
County Dental CG 43 49±15 1984)
Service (13)
Fox et al; 2008 Cross- Nine (1) 277 (- (1) (1) 90% pSS 1502
Journal of the American sectional rheumatology and ) 62±12.6 (2) 93% AECG (2002) -
Dental Association USA oral medicine (2) 1225 (2) CG 92%
centers (-) 61±12.7
CG 606 CG
(-) 61±12.2
Olate et al; 2014 Cross- University of La 35 (-) 53.9±15 - Not determined.
International Journal of sectional Frontera, Hernán Based on clinical -
Clinical and Chile Henríquez No CG and biopsy criteria
Experimental Medicine Aravena Hospital

Blochowiak et al; 2016 Cross- - 40 (-) 28.25 94.5% pSS 22 sSS 18

Advances in sectional AECG (2002) -
Dermatology and Poland No CG
Allergology

(2) Studies which only determine the prevalence of Candida albicans oral lesions
Tapper-Jones et al; Cross- Welsh National SS 16 SS 57 SS 87.5% pSS 5 sSS 11 Examination, quantitative
1980 sectional School of (11) CG 57 CG 87.5% Bloch et al criteria imprint culture technique
Journal of Clinical United Medicine Dental CG 16 (1965)
Pathology Kingdom School (11)

MacFarlane et al; 1984 Cross- Glasgow Dental SS 10 (9) SS 62 SS 90% Not determined Clinical changes in the
Microbios sectional Hospital and CG 10 CG 62 CG 90% Bloch et al criteria tongue (Bertran 1967)
United School (9) (1965)
Kingdom
Hernández et al; 1989 Cross- Sjögren’s 246 (66) 52 87.8% pSS 166 sSS 80 Specific observation of
Oral Surgery Oral sectional syndrome Clinic Bloch et al Candida lesions
Medicine Oral Pathology USA of the University No CG Criteria (1965)
of California
Lundström et al; 1995 Cross- University 40 (15) 59 92.5% pSS 40 Clinical oral examination,
Clinical and sectional Hospital, Copenhagen evaluation of subjective oral
Experimental Sweden Linköping No CG criteria 1986 symptoms
Rheumatology
Soto-Rojas et al; 1998 Cross- National Institute SS 50 (-) pSS pSS 95.2% pSS 21 sSS 29 WHO recommendation
Journal of Rheumatology sectional of Nutrition CG 31 (-) 56.9±11 sSS 96.5% Keratoconjunctivit (1987)
Mexico Salvador Zubirá sSS CG 93.5% is sicca, minor
47.4±13 salivary gland
CG biopsy,
49.8±10 abnormalities in
sialography
/scintigraphy
Kindelan et al; 1998 Cross- Charles Clifford 28 (10) pSS 56.9 pSS 81.2% pSS 16 sSS 12
Oral Surgery Oral sectional Dental Hospital, No CG sSS 56.6 sSS 91.6% European -
Medicine Oral Pathology United Oral Medicine classification
Kingdom Clinic criteria of 1993

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Table 1 continue. Study characteristics.

Rhodus et al; 1999 Cross- University of SS 27 (0) 56.3 pSS 100% pSS 9 sSS 18 -
ENT Journal sectional Minnesota, Oral CG 14 sSS 5.8% San Diego criteria
USA Medicine Clinic (0) CG 92.8%
Leung et al; Cross- SS: SS 51 (-) pSS 51.4 pSS 92.3% pSS 26 sSS 25 Clinical and mycological
2004 sectional Rheumatology CG29 (-) sSS sSS 96% AECG (2002) examinations by the same
International Dental China clinic, Queen 43.33 CG 93.1% examiner. Mucositis as
Journal Mary Hospital CG 44.0 Spijkervet et al. (1989)
CG: Prince Philip
Dental Hospital
Ergun et al; 2010 Cross- SS: Istambul SS 47 SS 53.27 - pSS 14 sSS 23 Clinical, mycological
Medicina Oral Patología sectional University, (10) CG 54.27 Modified examinations by the same
Oral Cirugía Bucal Turkey Faculty of CG 37 internationally examiner
Medicine (12) agreed-on criteria
CG: - for SS (2004)
Yan et al; 2011 Cross- Stomatological 30 (-) 48.6 100% pSS 30 Clinical, mycological
Journal of Rheumatology sectional Hospital of Pekin No CG AECG (2002) examinations by the same
China University examiner

(3) Studies which determine the prevalence of oral lesions of autoimmune aetiology
Likar-Manookin et al; Cohort Carolinas Medical 155 (-) 57.9±12. 90.3% pSS 155 Clinical, histopathological
2013 study Center, Baylor No CG 5 AECG (2002) examination. All oral lesions
Oral Diseases USA College of were documented
Dentistry,
University of
Florida
Group, SS=Sjogren syndrome, pSS=Primary SS, sSS=Secondary SS, CD=Celiac Patients, F=female, AECG=American-Europe-
CG=Control
an Consensus Group, (1)=Identified by their physician, (2)=Sjögren’s syndrome foundation patients.

fulfil the eligibility criteria, were excluded (Appendix This is in accordance with what we found when com-
1). Finally, 18 articles were included in our systematic pared to a CG. The types of OL which were significant-
review (3,9,11-15,19,21-30) (Fig. 1). ly more common in SS are: angular cheilitis, (14,28)
-Study characteristics atrophic glossitis (9,28), grooves or fissuration of the
Seventeen of the eighteen selected articles were cross- tongue (9,14), clinical manifestation of candidiasis (14),
sectional studies and the other one was a cohort study. erythematous candidiasis (28) and atrophic mucosa
They were published between 1980 and 2016. A total of (28). Oral manifestations, with its respective percentag-
3290 patients were studied: 2426 were SS patients (of es, both in SS and CG patients are recorded in Table 2.
which known: 2111 had pSS and 216 sSS), 3 of the stud- -Risk of bias in individual studies
ies did not specify the type of SS (MacFarlane et al., 10 Using the predetermined 10 domains for the method-
SS patients; Koseki et al., 54 SS patients; and Olate et ological quality assessment according to the JBI (17), we
al., 35 SS patients), and 864 patients were CG (Table 1). determined ten of the selected papers (3,11,12,14,21,22,
The mean age of the subjects ranged from 28.25-62 25,26,29,30) to have a low quality assessment and eight
years in the SS group and 24-62 years in the CG (Table of them (9,13,15,19,23,24,27,28) to have a high quality
1). assessment. Table 3 shows a more detailed description
Regarding to gender, in the SS patients the female per- of the articles included.
centage ranged from 81.2% to 100%, and in the CG -Risk of bias within studies
from 87.5% to 100%. Three articles did not specify the We detected some sources of information bias. First
gender of the sample (12,28,30). of all, different diagnosis criteria for SS have been
We did not consider the CG in Patinen et al. study, since used along the years. Second of all, some studies did
they were celiac patients; neither in Kindelan et al. not specify how the oral mucosal evaluation was car-
study (since they were xerostomic controls), nor Yan et ried out (3,13,19,24,30). Six studies (3,11,23,24,29,30)
al. (because they had oral candidiasis) (Table 1). did not compare the outcomes with a healthy CG and
-Main findings three studies did not specify the gender of the sample
The most frequent OL among SS patients was angular nor the CG (12,28,30). In addition, three studies did not
cheilitis, reported in fifteen of the eighteen selected pa- determine the type of SS studied (12,22,30). The studies
pers. Atrophic glossitis was also common, reported in did not take into account the presence of confounding
ten of the selected papers. Candida manifestations and factors as smoking and alcohol habits, other diseases or
recurrent or chronic oral ulcerations in eight of them; drugs intake, and eight of them did not report if the pa-
and grooves or fissuration of the tongue were reported tients wore dentures (3,13-15,26,27,29,30).
in seven papers. None of the selected papers reflected -Risk of bias across studies
the total prevalence within the SS or the CG patients Due to the fact that only articles published in English
(Table 2). were reviewed, bias due to language publication could
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Table 2. Oral manifestations in SS and CG.

Study Oral manifestations in SS and CG
Tapper-Jones et al; 1980 Angular cheilitis: SS 18.7% pSS 20% sSS 18.1% CG 0
Atrophic glossitis: SS 37.5% pSS 40% sSS 36.3% CG 0
Macfarlane et al; 1984 Angular cheilitis: SS 50% CG 0
Atrophic glossitis: SS 90% CG 0
Hernández et al; 1989 Angular cheilitis: SS 20%
Atrophic glossitis: SS 44%
Grooves/ Fissuration of the tongue: SS 52%
Dorsal tongue erythema: SS 32%
Patchy erythema (nonlingual): SS 26%
Removable white plaques: SS 1%
Lundström et al; 1995 Angular cheilitis: pSS 35%
Oral candidiasis: pSS 75%
Recurrent or chronic ulcerations: pSS 40%
Oral lichenoid lesions: pSS 18%
Herpes labialis: pSS 2.5%
Soto-Rojas et al; 1998 Angular cheilitis: pSS 24% sSS 24% CG 0 (pSS vs CG p=0.017; sSS vs CG p=0.012)
Atrophic glossitis: pSS 62% sSS 76% CG 16%
Oral candidiasis: pSS 71% sSS 76% CG 23% (pSS vs CG p<0.01; sSS vs CG p<0.001)
Grooves/ Fissuration of the tongue: pSS 62% sSS 76% CG 16% (pSS vs CG p=0.001; sSS vs CG p<0.001)
Removable white plaques: pSS 4.76% sSS 6.8%
Kindelan et al; 1998 Angular cheilitis: pSS 6.2% sSS 16.6%
Atrophic glossitis: pSS 6.2%
Oral candidiasis: pSS 18.75% sSS 25%
Denture stomatitis: pSS 6.2% sSS 8.3%
Dorsal tongue erythema: sSS 8.3%
Erythematous candidiasis: sSS 8.3%
Pedersen et al; 1999 Angular cheilitis: pSS 18.7% CG 0
Atrophic glossitis: pSS 68.7% CG 0
Oral candidiasis: pSS 18.7% CG 0
Recurrent or chronic ulcerations: pSS 25% CG 0
Denture stomatitis: pSS 12.5% CG 0
Mucosal friction: pSS 62.5% CG 0
Rhodus et al; 1999 Oral candidiasis: SS 48% CG 0
Angular cheilitis: SS 81% CG 0
Removable white plaques: SS 14% CG 0
Patinen et al; 2004 Recurrent or chronic ulcerations: SS 30% CD+SS 30%
Oral lichenoid lesions: SS 35% CD+SS 15%
Leukoplakia: SS 25% CD+SS 5%
Koseki et al; 2004 Angular cheilitis: SS 44.5% CG 2.6%
Atrophic glossitis: SS 16.7% CG 13.5%
Grooves/ Fissuration of the tongue: SS 33.3% CG 2.7%
Shiny tongue: SS 16.7% CG 0
Strawberry tongue: SS 5.6% CG 0
Leung et al; Angular cheilitis: pSS 11.5% sSS 12% CG 0
2004 Atrophic glossitis: pSS 7.6% sSS 8% CG 0
Removable white plaques: pSS 3.8% sSS 4% CG 0
Erythematous candidiasis: pSS 3.8% sSS 4% CG 0
Márton et al; 2006 Angular cheilitis: SS 2.04% CG 4.6%
Atrophic glossitis: SS 34.7% CG 9.3% (p< 0.01)
Denture stomatitis: SS 20.4% CG 4.6%
Grooves/ Fissuration of the tongue: SS 40.8% CG 4.6% (p<0.01)
Median rhomboid glossitis: SS 6.1% CG 11.6%
Geographic tongue: SS 2.04% CG 4.6%
Black hairy tongue: SS 16.3% CG 4.6%
Atrophic mucosa: SS 10.2% CG 2.32%
Fox et al; 2008 Recurrent or chronic ulcerations: PhysR-Pss 41% SFS-PSS 46% (p<0.05)
Ergun et al; 2010 Angular cheilitis SS 21.6% CG 0 (p=0.005)
Atrophic glossitis SS 48.6% CG 10.8% (p<0.001)
Recurrent or chronic ulcerations: SS 35.13% CG 0
Erythematous candidiasis: SS 62.16% CG 13.5% (p=0.000)
Atrophic mucosa: SS 75.7% CG 8.1% (p=0.0001)
Yan et al; 2011 Angular cheilitis: pSS 6.66%
Oral candidiasis: pSS 87%
Denture stomatitis: pSS 3.33%
Median rhomboid glossitis: pSS 6.6%
Dorsal tongue erythema: pSS 33.3%
Likar-Manookin et al; Oral candidiasis: 29.9%
2013 Recurrent or chronic ulcerations:
Recurrent aphtous stomatitis: 3.9%
Chronic Ulcerative Stomatitis: 0.6%
Lichen planus: 7.1%
Olate et al; 2014 Angular cheilitis: 14%
Oral candidiasis: 3%

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Table 2 continue. Oral manifestations in SS and CG.

Recurrent or chronic ulcerations:
Ulcers 3%
Aphtae 31%
Denture stomatitis: 26%
Removable white plaques: 0%
Erythematous candidiasis: 3%
Blochowiak et al; 2016 Angular cheilitis: pSS 18.2% sSS 22.2%
Non-specific ulceration: pSS 9.1% sSS 22.2%
Small Apthae: pSS 13.6% sSS 11.1%
Sutton’s apthae: pSS 4.5% sSS 0
Grooves/ Fissuration of the tongue: pSS 4.5% sSS 0
Denture stomatitis: pSS 4.5% sSS 0
Geographic tongue: pSS 0 sSS 11.1%
CG=Control Group, SS=Sjogren syndrome, pSS=Primary SS, sSS=secondary SS, CD=Celiac Patients.

not be ruled out. Even though we searched four data- The association between SS and OL of autoimmune
bases, we cannot guarantee that some related papers aetiology remains unclear. Likar-Manookin et al. con-
might not have been identified. Additionally, not all OL ducted the first study of autoimmune oral diseases in
were classified in the same way, and not all the studies pSS. This study observed that 12.3% of pSS patients
specified if such lesions were reported by a calibrated presented autoimmune OL such as lichen planus (7.1%)
(or always the same) examiner. and recurrent aphtous stomatitis (3.9%). Chronic or re-
current ulceration seem to be common among SS pa-
Discussion tients: Lundström and Lindström reported a prevalence
-Summary of evidence of 40%, which is in accordance with Fox et al. (43%);
SS is known to be one of the most common rheumat- Ergun et al. (35.1% of oral ulcerations in the SS group
ic diseases. To date, there is not a global overview of vs 0% in the CG); Pedersen et al. (25%); and Patinen
which are the most common OL in these patients, nei- et al. (30%). Olate et al. differentiate between ulcers
ther if they appear more frequently in SS than in healthy (3%) and aphtae, with a higher prevalence: 31%; and
population. Blochowiak et al. classify them in non-specific ulcer-
-Main findings ation (9.1% pSS, 22.2% sSS), small aphtae (13.6% pSS,
We identified 18 studies reporting prevalence of oral 11.1% sSS), and Sutton’s aphtae (4.5% pSS, 0% sSS). In
mucosal lesions in SS, 10 of them compared to a healthy these papers the possible aetiology of these ulcerations
CG. We found surprising the young age of the patients. was not given (Table 2, 2 continue).
This is due to Pedersen et al. study consider a young Less frequently reported were oral lichenoid lesions (18-
CG, with a mean age of 24, and Blochowiak et al., a 35%) (11,26), herpes labialis (2.5%) (11) and oral muco-
study group with a mean age of 28.5. The rest of the sal friction (62%) (25).
papers, have a mean age around 50-60 years, which is -Secondary data
more in accordance with the mean age of this disease The increased prevalence of OL in SS may be due to
(Table 1). the impaired salivary gland function in these patients
In this systematic review, OL were more common among (25). Proper levels of saliva allow for lubrication of the
SS patients compared to non-SS patients. Angular cheili- mucosa, enhance healing of damage tissues, and play
tis was the most frequent OL in SS patients, followed by an essential role in local immunity (10,15,19). Addition-
atrophic glossitis; candida lesions; ulcers and grooves or ally, Pedersen et al. found that oral mucosal changes
fissuration of the tongue (Table 2, 2 continue). occurred more frequently in patients with the lowest
When compared to a CG, the types of OL that appeared salivary flow rates.
more frequently in SS with a statistical signification It seems to be an inverse relationship between the rate
were also angular cheilitis; (14,28) clinical manifesta- of salivary flow and the presence of candidiasis: low
tion of candidiasis; (14) erythematous candidiasis;(28) levels of saliva are related to the presence of candidiasis
atrophic mucosa; (28) atrophic glossitis (9,28) and (12,15,29,30). Kindelan et al. and Yan et al. found a sig-
grooves or fissuration of the tongue (9,14). These two nificant inverse relationship between unstimulated sali-
last tongue alterations are characteristic signs of oral vary flow and Candida infection. Pseudomembranous
mucosal desiccation (9). candidiasis or removable white plaques was reported by
Geographic tongue was reported in two of the includ- five authors (18,19,23,27,30). We found interesting the
ed papers (3,9). Less frequent tongue alterations were fact that among SS patients pseudomembranous candi-
shiny tongue, strawberry tongue (12), and black hairy diasis was not common, with a prevalence range in the
tongue (9) (Table 2, 2 continue). These tongue condi- cited articles of 0%-6.8%. Denture wearing is one of the
tions, despite the discomfort that they cause, uncom- major predisposing factors for oral candidiasis, since
monly require treatment. the fitting surface of the denture is the main reservoir

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 Table 3. Risk of bias according to the JBI.
Tapper Mac Farlane Hernández Lundstrom Soto Kindelan Pedesen Rhodus Patinen Koseki Leung et Márton Fox et Ergun et Yan et Likar- Olate et Blochowiak
Jones et et al; 1984 et al; 1989 et al; 1995 Rojas et al; 1998 et al; et al; et al; et al; al; 2004 et al; al; al; 2010 al; 2011 Manookin al; 2014 et al; 2016
al; 1980 et al; 1999 1999 2004 2004 2006 2008 et al; 2013
1998

1. Was the sample Y U Y Y U Y Y Y Y U Y Y Y Y Y Y U U

representative of
the target
population?

2. Were study U Y Y U U Y U U U U U U Y U Y Y U U
participants
recruited in an
appropriate way?
Med Oral Patol Oral Cir Bucal. 2018 Jul 1;23 (4):e391-400.

3. Was the U U Y U U Y U U U U U U U U U U U U
sample size
adequate?

4. Were the study Y U Y N Y Y Y Y Y U Y Y Y Y U Y U N

subjects and
setting described
in detail?

5. Is the data U Y U Y Y U U U U U Y Y Y Y U U Y N
analysis
conducted with
sufficient
coverage of the

e398
identified sample?
6. Were objective, U Y U U Y Y U Y U U U Y U Y Y U U U
standard criteria
used for
measurement of
the condition?
7. Was the U U U U U U U Y U U U U U Y Y U U U
condition
measured
reliably?

8. Was there Y Y Y Y Y U Y Y Y Y Y Y Y Y U Y U N
appropriate
statistical
analysis?

9. Are all the U U U U U U U U U U Y U U U U U U Y

important
confounding
factors/subgroups
/differences
identified and
accounted for?
10. Were U U U Y U U Y U Y U Y Y Y U U Y U Y
subpopulation
identified using
objective criteria?

Y=Yes, N=No, U=Unclear, N/A=Not applicable.

Oral lesions in Sjögren’s syndrome patients
Med Oral Patol Oral Cir Bucal. 2018 Jul 1;23 (4):e391-400. Oral lesions in Sjögren’s syndrome patients

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Author contributions
JS did the search analysis, designed the methodology, reviewed all
the selected studies, extracted the data and wrote the paper. JG con-
tributed to the methodology, data collection and extraction. RMLP
solved differences with eligible studies and contributed to the con-
ceptualization and writing of the original draft. MF, LC and GH
helped with the supervision, review and writing of the final version
of this paper.

Funding
This work was not supported by other organizations.

Conflict of interest
The authors declare that they have no conflict of interest.

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