- Email: [email protected]
A prospective evaluation of dental and periodontal status in patients with suspected Sjögren's syndrome
G Model BONSOI-4190; No. of Pages 2
ARTICLE IN PRESS Joint Bone Spine xxx (2015) xxx–xxx
Available online at
ScienceDirect www.sciencedirect.com
Letter to the Editor A prospective evaluation of dental and periodontal status in patients with suspected Sjögren’s syndrome
a r t i c l e
i n f o
Keywords: Sjögren’s syndrome Sicca syndrome Periodontitis Oral health Xerostomia Salivary pH
Sjögren’s syndrome (SS) is an autoimmune epithelitis [1] characterized by lymphocytic infiltration of the exocrine glands reducing lacrimal and salivary secretion. If the diagnosis is made in the absence of another autoimmune disease, it has been classified as primary SS (pSS). When SS is associated with another autoimmune diseases, it has been termed secondary SS (sSS). The resulting xerostomia increases the development of dental plaque and the likelihood of periodontal disease, a chronic inflammatory process whereby bacteria triggers localized gingival inflammation that leads to the destruction of the bone and connective tissue supporting the teeth [2]. There are many etiologies for xerostomia, such as medication, physiological aging, radiotherapy, graft-versus-host disease, viral infection and systemic disease [3]. Analyses of this complication in SS have however yielded conflicting conclusions [4–7] and, to date, no consensus can be reached as to whether patients with pSS experience more severe oral complications and periodontitis than controls complaining of xerostomia. Our objective was to monitor, in a prospective observational study performed in the single-center Brittany cohort of patients with suspected SS between January 2006 and February 2013, the oral and periodontal status of 31 patients who fulfilled the American-European Consensus Group (AECG) criteria for SS [8] in comparison with 42 patients with subjective sicca complaints. No differences were observed between the two groups that could be attributed to age, gender, smoking status, duration of symptoms or subjective complaints of xerophthalmia (Table 1). Interestingly, the mean number of decayed, missing and filled teeth (DMFT) [9] was significantly higher in SS patients than in non-SS patients. This difference can be put down to the missing tooth score, which was also significantly higher in SS patients than in non-SS patients. The plaque index, gingival index and papillary bleeding
Abbreviations: pSS, primary Sjögren’s syndrome; sSS, secondary Sjögren’s syndrome; AECG, American-European Consensus Group; DMFT, decayed, missing and filled teeth; SD, standard deviation.
Table 1 Comparison of patients with and without Sjögren’s syndrome.
Age (years, mean ± SD) Symptom duration (years, mean ± SD) Female, n (%) Xerophthalmia, n (%)a Xerostomia, n (%)a Schirmer’s test < 5 mm, n (%) Chisholm ≥ 2, n (%) Anti-SSA/SSB, n (%) Smoker, n (%) Steroid use, n (%) Decayed (D) Missing (M) Filled (F) DMFT Number of crowns Plaque index Gingival index Papillary bleeding index Pocket depth UWSF SWSF pH
SS n = 31
No SSn = 42
P value
60.0 ± 12.4 7.5 ± 5.4 29 (93.5) 30 (96.8) 31 (100) 22 (71.0) 26 (83.9) 15 (48.4) 2 (6.5) 7 (22.6) 0.4 (1.6) 8.4 (9.9) 11.6 (7.5) 20.3 (6.4) 3.4 (5.4) 9.8 (4.5) 11.5 (6.8) 7.7 (4.2) 9.7 (10.0) 0.15 (0.18) 0.55 (0.48) 5.8 (1.0)
55.1 ± 16.1 6.6 ± 6.0 39 (92.9) 39 (92.9) 39 (92.9) 11 (26.2) 5 (11.9) 4 (9.5) 5 (11.1) 5 (11.9) 0.1 (0.5) 4.4 (6.7) 11.4 (5.6) 15.9 (7.1) 4.2 (4.6) 6.1 (3.5) 6.1 (4.8) 5.0 (4.2) 5.0 (6.6) 0.28 (0.16) 0.70 (0.46) 6.7 (1.1)
0.28 0.32 1 0.63 0.26 <0.01 <0.01 <0.01 0.69 0.32 0.71 0.04 0.88 0.01 0.24 <0.01 <0.02 0.02 0.08 <0.01 0.15 <0.01
SS, Sjögren’s syndrome patients fulfilling AECG criteria (28 primary and 3 secondary with 1 rheumatoid arthritis, 1 mixed connective tissue disease, 1 undifferentiated connective tissue disease). No SS, patients with sicca syndrome who do not fulfil AECG criteria (29 idiopathic sicca syndrome, 4 drug-induced sicca syndrome, 1 poorly controlled type 2 diabetes mellitus, 8 other systemic autoimmune diseases [rheumatoid arthritis, n = 2; systemic lupus erythematosus, n = 2, undifferentiated connective tissue disease, n = 4]). DMFT: decayed, missing and filled teeth; UWSF: unstimulated whole saliva; SWSF: stimulated whole saliva; SD: standard deviation. Xerophthalmia and xerostomia referred to patients’ subjective complaints. Schirmer’s test was considered abnormal if ≤5 mm in 5 min. Unstimulated whole salivary flow was considered abnormal if ≤0.1 mL/min. Salivary gland biopsies were graded according to Chisholm and Masson. Mann-Whitney and Chi2 tests were used, as appropriate, to compare SS and non-SS patients. P values < 0.05 were considered significant. a Refers to patients complaints.
index [10] were higher in SS patients than in non-SS patients. Although SS patients presented a slightly higher pocket depth, the difference was not, however, significant when compared to non-SS patients. The salivary pH was significantly lower in SS patients compared to non-SS patients. Interestingly, we only observed significant negative correlations between salivary pH and periodontal conditions in SS patients (Spearman Rho coefficient –0.44 with plaque index, P = 0.03; –0.42 with gingival index, P = 0.04; –0.38 with papillary bleeding index, P = 0.07; and –0.40 with pocket depth, P = 0.05). Thus, SS patients with salivary pH < 6 (n = 13) displayed higher periodontal indices than those with salivary pH ≥ 6 (n = 17) (Table 2), whereas these two groups were comparable in terms of age, disease duration, salivary flow, Chisholm’s score and DMFT. These results
http://dx.doi.org/10.1016/j.jbspin.2015.02.015 1297-319X/© 2015 Société franc¸aise de rhumatologie. Published by Elsevier Masson SAS. All rights reserved.
Please cite this article in press as: Le Gall M, et al. A prospective evaluation of dental and periodontal status in patients with suspected Sjögren’s syndrome. Joint Bone Spine (2015), http://dx.doi.org/10.1016/j.jbspin.2015.02.015
G Model
ARTICLE IN PRESS
BONSOI-4190; No. of Pages 2
Letter to the Editor / Joint Bone Spine xxx (2015) xxx–xxx
2
Table 2 Low pH is a marker of periodontal disease severity in SS patients. pH < 6 n = 13 Age (years) Disease duration (years) UWSF (mL/min) SWSF (mL/min) Chisholm score Decayed (D) Missing (M) Filled (F) DMFT Number of crowns Plaque index Gingival index Papillary bleeding index Pocket depth
60.9 8.0 0.19 0.61 3.00 0.8 11.8 10.1 22.6 2.7 12.4 15.8 9.8 14.3
± ± ± ± ± ± ± ± ± ± ± ± ± ±
12.8 5.1 0.24 0.42 1.08 2.5 11.7 8.8 6.6 5.9 3.9 6.2 4.7 8.4
References
pH ≥ 6 n = 17
P value
59.0 ± 12.6 7.4 ± 5.6 0.13 ± 0.14 0.52 ± 0.53 3.41 ± 0.87 0.1 ± 0.2 6.2 ± 7.9 12. ± 6.1 18.5 ± 6.1 4.1 ± 5.3 7.9 ± 3.9 8.7 ± 5.9 6.5 ± 3.7 5.7 ± 8.7
0.90 0.62 0.91 0.39 0.30 0.65 0.28 0.28 0.08 0.30 0.01 0.02 0.08 0.01
Data are expressed as means ± standard deviation. Mann-Whitney test was used to compare patients. P values < 0.05 were considered significant. UWSF: unstimulated whole saliva; SWSF: stimulated whole saliva; DMFT: decayed, missing and filled teeth.
suggest that low salivary pH could be a marker of periodontal disease severity in SS patients regardless of salivary flow rate. This study suggests that patients with SS have increased DMFT score and more severe periodontal conditions compared to non-SS patients. These conditions are most probably due to the combined effect of impaired salivary gland functions and reduced saliva buffer capacity. SS patients should therefore be convinced of the necessity of preventing dental and periodontal conditions through regular surveillance and care. Disclosure of interest The authors declare that they have no conflicts of interest concerning this article. All authors have substantial contributions to conception and design of, or acquisition of data or analysis and interpretation of data. They have also participated to the drafting of the article or its revising. Finally, all authors have approved the submitted version. Acknowledgments We are grateful to Dr. Emmanuel Nowak (INSERM CIC 0502, Brest, France) for helping with the statistical analysis and to Alice Philippe, Jérémy Santucci, Aurélie Hacquard and Sébastien Beuzit for their operational assistance. We would also like to thank Geneviève Michel and Simone Forest for typing this letter.
[1] Moutsopoulos HM. Sjogren’s syndrome: autoimmune epithelitis. Clin Immunol Immunopathol 1994;72:162–5. [2] Williams RC. Periodontal disease. N Engl J Med 1990;322:373–82. [3] Cornec D, Saraux A, Jousse-Joulin S, et al. The differential diagnosis of dry eyes, dry mouth, and parotidomegaly: a comprehensive review. Clin Rev Allergy Immunol 2014, http://dx.doi.org/10.1007/s12016-014-8431-1. [4] Antoniazzi RP, Miranda LA, Zanatta FB, et al. Periodontal conditions of individuals with Sjogren’s syndrome. J Periodontol 2009;80:429–35. [5] Kuru B, McCullough MJ, Yilmaz S, Porter SR. Clinical and microbiological studies of periodontal disease in Sjogren syndrome patients. J Clin Periodontol 2002;29:92–102. [6] Ergun S, Cekici A, Topcuoglu N, et al. Oral status and Candida colonization in patients with Sjogren’s Syndrome. Med Oral Patologia Oral Cirugia Bucal 2010;15:e310–5. [7] Boutsi EA, Paikos S, Dafni UG, Moutsopoulos HM, Skopouli FN. Dental and periodontal status of Sjogren’s syndrome. J Clin Periodontol 2000;27:231–5. [8] Vitali C, Bombardieri S, Jonsson R, et al. Classification criteria for Sjogren’s syndrome: a revised version of the European criteria proposed by the American-European Consensus Group. Ann Rheum Dis 2002;61:554–8. [9] World Health Organization. Oral health surveys: basic methods. 4th ed. Geneva; 1997. [10] Ramfjord SP. The Periodontal Disease Index (PDI). J Periodontol 1967;38 Suppl.:602–10.
Malo Le Gall a Divi Cornec b,c,d Jacques-Olivier Pers a,c,∗,d Alain Saraux b,c,d Sandrine Jousse-Joulin b,c,d Béatrice Cochener e Anne-Marie Roguedas-Contios f Valérie Devauchelle-Pensec b,c,d Sylvie Boisramé a a Odontology, CHRU de Brest, 29609 Brest cedex, France b Rheumatology, CHRU de Brest, 29609 Brest cedex, France c EA2216, Inserm ESPRI, ERI29, laboratoire d’immunologie, université de Brest, 29609 Brest cedex, France d LabEx IGO, 29609 Brest cedex, France e Ophthalmology, CHRU de Brest, Brest cedex, France f Dermatology, CHRU de Brest, Brest cedex, France ∗ Corresponding author. EA2216, Inserm ESPRI, ERI29, laboratoire d’immunologie, université de Brest, 29609 Brest cedex, France. E-mail address: [email protected] (J.-O. Pers)
Accepted 17 February 2015 Available online xxx
Please cite this article in press as: Le Gall M, et al. A prospective evaluation of dental and periodontal status in patients with suspected Sjögren’s syndrome. Joint Bone Spine (2015), http://dx.doi.org/10.1016/j.jbspin.2015.02.015
ARTICLE IN PRESS Joint Bone Spine xxx (2015) xxx–xxx
Available online at
ScienceDirect www.sciencedirect.com
Letter to the Editor A prospective evaluation of dental and periodontal status in patients with suspected Sjögren’s syndrome
a r t i c l e
i n f o
Keywords: Sjögren’s syndrome Sicca syndrome Periodontitis Oral health Xerostomia Salivary pH
Sjögren’s syndrome (SS) is an autoimmune epithelitis [1] characterized by lymphocytic infiltration of the exocrine glands reducing lacrimal and salivary secretion. If the diagnosis is made in the absence of another autoimmune disease, it has been classified as primary SS (pSS). When SS is associated with another autoimmune diseases, it has been termed secondary SS (sSS). The resulting xerostomia increases the development of dental plaque and the likelihood of periodontal disease, a chronic inflammatory process whereby bacteria triggers localized gingival inflammation that leads to the destruction of the bone and connective tissue supporting the teeth [2]. There are many etiologies for xerostomia, such as medication, physiological aging, radiotherapy, graft-versus-host disease, viral infection and systemic disease [3]. Analyses of this complication in SS have however yielded conflicting conclusions [4–7] and, to date, no consensus can be reached as to whether patients with pSS experience more severe oral complications and periodontitis than controls complaining of xerostomia. Our objective was to monitor, in a prospective observational study performed in the single-center Brittany cohort of patients with suspected SS between January 2006 and February 2013, the oral and periodontal status of 31 patients who fulfilled the American-European Consensus Group (AECG) criteria for SS [8] in comparison with 42 patients with subjective sicca complaints. No differences were observed between the two groups that could be attributed to age, gender, smoking status, duration of symptoms or subjective complaints of xerophthalmia (Table 1). Interestingly, the mean number of decayed, missing and filled teeth (DMFT) [9] was significantly higher in SS patients than in non-SS patients. This difference can be put down to the missing tooth score, which was also significantly higher in SS patients than in non-SS patients. The plaque index, gingival index and papillary bleeding
Abbreviations: pSS, primary Sjögren’s syndrome; sSS, secondary Sjögren’s syndrome; AECG, American-European Consensus Group; DMFT, decayed, missing and filled teeth; SD, standard deviation.
Table 1 Comparison of patients with and without Sjögren’s syndrome.
Age (years, mean ± SD) Symptom duration (years, mean ± SD) Female, n (%) Xerophthalmia, n (%)a Xerostomia, n (%)a Schirmer’s test < 5 mm, n (%) Chisholm ≥ 2, n (%) Anti-SSA/SSB, n (%) Smoker, n (%) Steroid use, n (%) Decayed (D) Missing (M) Filled (F) DMFT Number of crowns Plaque index Gingival index Papillary bleeding index Pocket depth UWSF SWSF pH
SS n = 31
No SSn = 42
P value
60.0 ± 12.4 7.5 ± 5.4 29 (93.5) 30 (96.8) 31 (100) 22 (71.0) 26 (83.9) 15 (48.4) 2 (6.5) 7 (22.6) 0.4 (1.6) 8.4 (9.9) 11.6 (7.5) 20.3 (6.4) 3.4 (5.4) 9.8 (4.5) 11.5 (6.8) 7.7 (4.2) 9.7 (10.0) 0.15 (0.18) 0.55 (0.48) 5.8 (1.0)
55.1 ± 16.1 6.6 ± 6.0 39 (92.9) 39 (92.9) 39 (92.9) 11 (26.2) 5 (11.9) 4 (9.5) 5 (11.1) 5 (11.9) 0.1 (0.5) 4.4 (6.7) 11.4 (5.6) 15.9 (7.1) 4.2 (4.6) 6.1 (3.5) 6.1 (4.8) 5.0 (4.2) 5.0 (6.6) 0.28 (0.16) 0.70 (0.46) 6.7 (1.1)
0.28 0.32 1 0.63 0.26 <0.01 <0.01 <0.01 0.69 0.32 0.71 0.04 0.88 0.01 0.24 <0.01 <0.02 0.02 0.08 <0.01 0.15 <0.01
SS, Sjögren’s syndrome patients fulfilling AECG criteria (28 primary and 3 secondary with 1 rheumatoid arthritis, 1 mixed connective tissue disease, 1 undifferentiated connective tissue disease). No SS, patients with sicca syndrome who do not fulfil AECG criteria (29 idiopathic sicca syndrome, 4 drug-induced sicca syndrome, 1 poorly controlled type 2 diabetes mellitus, 8 other systemic autoimmune diseases [rheumatoid arthritis, n = 2; systemic lupus erythematosus, n = 2, undifferentiated connective tissue disease, n = 4]). DMFT: decayed, missing and filled teeth; UWSF: unstimulated whole saliva; SWSF: stimulated whole saliva; SD: standard deviation. Xerophthalmia and xerostomia referred to patients’ subjective complaints. Schirmer’s test was considered abnormal if ≤5 mm in 5 min. Unstimulated whole salivary flow was considered abnormal if ≤0.1 mL/min. Salivary gland biopsies were graded according to Chisholm and Masson. Mann-Whitney and Chi2 tests were used, as appropriate, to compare SS and non-SS patients. P values < 0.05 were considered significant. a Refers to patients complaints.
index [10] were higher in SS patients than in non-SS patients. Although SS patients presented a slightly higher pocket depth, the difference was not, however, significant when compared to non-SS patients. The salivary pH was significantly lower in SS patients compared to non-SS patients. Interestingly, we only observed significant negative correlations between salivary pH and periodontal conditions in SS patients (Spearman Rho coefficient –0.44 with plaque index, P = 0.03; –0.42 with gingival index, P = 0.04; –0.38 with papillary bleeding index, P = 0.07; and –0.40 with pocket depth, P = 0.05). Thus, SS patients with salivary pH < 6 (n = 13) displayed higher periodontal indices than those with salivary pH ≥ 6 (n = 17) (Table 2), whereas these two groups were comparable in terms of age, disease duration, salivary flow, Chisholm’s score and DMFT. These results
http://dx.doi.org/10.1016/j.jbspin.2015.02.015 1297-319X/© 2015 Société franc¸aise de rhumatologie. Published by Elsevier Masson SAS. All rights reserved.
Please cite this article in press as: Le Gall M, et al. A prospective evaluation of dental and periodontal status in patients with suspected Sjögren’s syndrome. Joint Bone Spine (2015), http://dx.doi.org/10.1016/j.jbspin.2015.02.015
G Model
ARTICLE IN PRESS
BONSOI-4190; No. of Pages 2
Letter to the Editor / Joint Bone Spine xxx (2015) xxx–xxx
2
Table 2 Low pH is a marker of periodontal disease severity in SS patients. pH < 6 n = 13 Age (years) Disease duration (years) UWSF (mL/min) SWSF (mL/min) Chisholm score Decayed (D) Missing (M) Filled (F) DMFT Number of crowns Plaque index Gingival index Papillary bleeding index Pocket depth
60.9 8.0 0.19 0.61 3.00 0.8 11.8 10.1 22.6 2.7 12.4 15.8 9.8 14.3
± ± ± ± ± ± ± ± ± ± ± ± ± ±
12.8 5.1 0.24 0.42 1.08 2.5 11.7 8.8 6.6 5.9 3.9 6.2 4.7 8.4
References
pH ≥ 6 n = 17
P value
59.0 ± 12.6 7.4 ± 5.6 0.13 ± 0.14 0.52 ± 0.53 3.41 ± 0.87 0.1 ± 0.2 6.2 ± 7.9 12. ± 6.1 18.5 ± 6.1 4.1 ± 5.3 7.9 ± 3.9 8.7 ± 5.9 6.5 ± 3.7 5.7 ± 8.7
0.90 0.62 0.91 0.39 0.30 0.65 0.28 0.28 0.08 0.30 0.01 0.02 0.08 0.01
Data are expressed as means ± standard deviation. Mann-Whitney test was used to compare patients. P values < 0.05 were considered significant. UWSF: unstimulated whole saliva; SWSF: stimulated whole saliva; DMFT: decayed, missing and filled teeth.
suggest that low salivary pH could be a marker of periodontal disease severity in SS patients regardless of salivary flow rate. This study suggests that patients with SS have increased DMFT score and more severe periodontal conditions compared to non-SS patients. These conditions are most probably due to the combined effect of impaired salivary gland functions and reduced saliva buffer capacity. SS patients should therefore be convinced of the necessity of preventing dental and periodontal conditions through regular surveillance and care. Disclosure of interest The authors declare that they have no conflicts of interest concerning this article. All authors have substantial contributions to conception and design of, or acquisition of data or analysis and interpretation of data. They have also participated to the drafting of the article or its revising. Finally, all authors have approved the submitted version. Acknowledgments We are grateful to Dr. Emmanuel Nowak (INSERM CIC 0502, Brest, France) for helping with the statistical analysis and to Alice Philippe, Jérémy Santucci, Aurélie Hacquard and Sébastien Beuzit for their operational assistance. We would also like to thank Geneviève Michel and Simone Forest for typing this letter.
[1] Moutsopoulos HM. Sjogren’s syndrome: autoimmune epithelitis. Clin Immunol Immunopathol 1994;72:162–5. [2] Williams RC. Periodontal disease. N Engl J Med 1990;322:373–82. [3] Cornec D, Saraux A, Jousse-Joulin S, et al. The differential diagnosis of dry eyes, dry mouth, and parotidomegaly: a comprehensive review. Clin Rev Allergy Immunol 2014, http://dx.doi.org/10.1007/s12016-014-8431-1. [4] Antoniazzi RP, Miranda LA, Zanatta FB, et al. Periodontal conditions of individuals with Sjogren’s syndrome. J Periodontol 2009;80:429–35. [5] Kuru B, McCullough MJ, Yilmaz S, Porter SR. Clinical and microbiological studies of periodontal disease in Sjogren syndrome patients. J Clin Periodontol 2002;29:92–102. [6] Ergun S, Cekici A, Topcuoglu N, et al. Oral status and Candida colonization in patients with Sjogren’s Syndrome. Med Oral Patologia Oral Cirugia Bucal 2010;15:e310–5. [7] Boutsi EA, Paikos S, Dafni UG, Moutsopoulos HM, Skopouli FN. Dental and periodontal status of Sjogren’s syndrome. J Clin Periodontol 2000;27:231–5. [8] Vitali C, Bombardieri S, Jonsson R, et al. Classification criteria for Sjogren’s syndrome: a revised version of the European criteria proposed by the American-European Consensus Group. Ann Rheum Dis 2002;61:554–8. [9] World Health Organization. Oral health surveys: basic methods. 4th ed. Geneva; 1997. [10] Ramfjord SP. The Periodontal Disease Index (PDI). J Periodontol 1967;38 Suppl.:602–10.
Malo Le Gall a Divi Cornec b,c,d Jacques-Olivier Pers a,c,∗,d Alain Saraux b,c,d Sandrine Jousse-Joulin b,c,d Béatrice Cochener e Anne-Marie Roguedas-Contios f Valérie Devauchelle-Pensec b,c,d Sylvie Boisramé a a Odontology, CHRU de Brest, 29609 Brest cedex, France b Rheumatology, CHRU de Brest, 29609 Brest cedex, France c EA2216, Inserm ESPRI, ERI29, laboratoire d’immunologie, université de Brest, 29609 Brest cedex, France d LabEx IGO, 29609 Brest cedex, France e Ophthalmology, CHRU de Brest, Brest cedex, France f Dermatology, CHRU de Brest, Brest cedex, France ∗ Corresponding author. EA2216, Inserm ESPRI, ERI29, laboratoire d’immunologie, université de Brest, 29609 Brest cedex, France. E-mail address: [email protected] (J.-O. Pers)
Accepted 17 February 2015 Available online xxx
Please cite this article in press as: Le Gall M, et al. A prospective evaluation of dental and periodontal status in patients with suspected Sjögren’s syndrome. Joint Bone Spine (2015), http://dx.doi.org/10.1016/j.jbspin.2015.02.015