Influence of periodontal treatment on rheumatoid arthritis: a systematic review and meta-analysis☆

Calderaro, Débora Cerqueira; Corrêa, Jôice Dias; Ferreira, Gilda Aparecida; Barbosa, Izabela Guimarães; Martins, Carolina Castro; Silva, Tarcília Aparecida; Teixeira, Antônio Lúcio

doi:10.1016/j.rbre.2016.11.011

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Review articles • Rev. Bras. Reumatol. 57 (3) • May-Jun 2017 • https://doi.org/10.1016/j.rbre.2016.11.011 copy

Influence of periodontal treatment on rheumatoid arthritis: a systematic review and meta-analysis^☆ ☆ Study conducted at Universidade Federal de Minas Gerais, Faculdade de Odontologia e Faculdade de Medicina, Departamento do Aparelho Locomotor, Belo Horizonte, MG, Brazil.

Authorship SCIMAGO INSTITUTIONS RANKINGS

ABSTRACT

Objective:

To evaluate the influence of periodontal treatment on rheumatoid arthritis activity.

Methods:

MEDLINE/PUBMED, The Cochrane Library, Clinical Trials, SciELO and LILACS were searched for studies published until December 2014. Included articles were: prospective studies; including patients older than 18 years, diagnosed with periodontitis and rheumatoid arthritis submitted to non-surgical periodontal treatment; with a control group receiving no periodontal treatment; with outcomes including at least one marker of rheumatoid arthritis activity. Methodological quality of the studies was assessed using PEDro scale. Quantitative data were pooled in statistical meta-analysis using Review Manager 5.

Results:

Four articles were included. Non-surgical periodontal treatment was associated with a significant reduction of DAS28 (OR: -1.18; 95% CI: -1.43, -0.93; p < 0.00001). Erythrocyte sedimentation rate, C-reactive protein, patient's assessment of rheumatoid activity using visual analogical scale, tender and swollen joint counts showed a trend toward reduction (not statistically significant).

Conclusions:

The reduction of DAS 28 in patients with rheumatoid arthritis after periodontal treatment suggests that the improvement of periodontal condition is beneficial to these patients. Further randomized controlled clinical trials are necessary to confirm this finding.

Keywords:
Periodontal-systemic disease interactions; Periodontitis; Rheumatoid arthritis; Meta-analysis

PEDro scale item	Al-Katma et al., 2007²⁵25 Al-Katma K, Bissada NF, Bordeaux JM, Sue J, Askari AD. Control of periodontal infection reduces the severity of active rheumatoid arthritis. JCR. 2007;13:134-7.	Pinho et al., 2009²⁶26 Pinho MN, Oliveira RDR, Novaes JRAB. Relationship between periodontitis and rheumatoid arthritis and the effect of non-surgical periodontal treatment. Braz Dent J. 2009;20:355-64.	Ortiz et al., 2009²⁷27 Ortiz P, Bissada NF, Palomo L, Han YW, Al-Zahrani MS, Panneerselvam A, et al. Periodontal therapy reduces the severity of active rheumatoid arthritis in patients treated with or without tumor necrosis factor inhibitors. J Periodontol. 2009;80:535-40.	Okada et al., 2013²⁹29 Okada M, Kobayashi T, Ito S, Yokoyama T, Abe A, Murasawa A, et al. Periodontal treatment decreases levels of antibodies to Porphyromonas gingivalis and citrulline in patients with rheumatoid arthritis and periodontitis. J Periodontol. 2013;84:e74-84.
Eligibility criteria specified	1	1	1	1
Random allocation	1	0	1	1
Concealed allocation	0	0	0	0
Groups similar at baseline	1	1	1	1
Subject blinding	0	0	0	0
Therapist blinding	0	0	0	0
Assessor blinding	1	0	0	0
Less than 15% dropouts	0	1	1	1
Intention-to-treat analysis	1	1	1	1
Between-group statistical comparisons	1	0	1	1
Point measures and variability data	1	1	1	1

Total	7	5	7	7

Article	Study design	Subjects	Losses	Follow-up time	RA outcomes	Results
Al-Katma et al., 2007²⁵25 Al-Katma K, Bissada NF, Bordeaux JM, Sue J, Askari AD. Control of periodontal infection reduces the severity of active rheumatoid arthritis. JCR. 2007;13:134-7.	IS, C, R, U B^a a Rheumatologist blinded to periodontal treatment. Patients: those submitted to non-surgical periodontal treatment. Controls: Those not submitted to periodontal treatment.	All: RA + P N = 38 Patients: n = 19 Controls: n = 19	Controls: n = 7^b b Four: absence to evaluations; three: changes in medications for RA. Patients: n = 2^c c One: absence to evaluations; one: inability to maintain good level of oral hygiene.	8 Wk	TJC SJC DAS 28 Global VAS ESR	Improvement of DAS 28 in 13/17 patients (76.4%) and 2/12 controls (16.7%) Improvement of VAS in 10/17 patients (58.8%) and 2/12 controls (16.7%) Greater reduction of DAS 28 and ESR in patients than controls

Ortiz et al., 2009²⁷27 Ortiz P, Bissada NF, Palomo L, Han YW, Al-Zahrani MS, Panneerselvam A, et al. Periodontal therapy reduces the severity of active rheumatoid arthritis in patients treated with or without tumor necrosis factor inhibitors. J Periodontol. 2009;80:535-40.	I, C, U RND BND	All: RA + P N = 20 Patients: n = 10 Controls: n = 10	No losses	6 Wk	TJC SJC Global VAS ESR DAS 28	Improvement of DAS 28, decrease in number of SJC, and global VAS in patients, when compared to controls

Pinho et al., 2009²⁶26 Pinho MN, Oliveira RDR, Novaes JRAB. Relationship between periodontitis and rheumatoid arthritis and the effect of non-surgical periodontal treatment. Braz Dent J. 2009;20:355-64.	I, C, U RND BND	All: RA + P N = 30 Patients: n = 15 Controls: n = 15	No losses	6 Mo	ESR CRP DAS 28	No significant differences of ESR and CRP

Okada et al., 2013²⁹29 Okada M, Kobayashi T, Ito S, Yokoyama T, Abe A, Murasawa A, et al. Periodontal treatment decreases levels of antibodies to Porphyromonas gingivalis and citrulline in patients with rheumatoid arthritis and periodontitis. J Periodontol. 2013;84:e74-84.	I, C, U RND BND	All: RA + P N = 55 Patients: n = 26 Controls: n = 29	No losses	8 Wk	DAS28-CRP CRP TJC SJC Global VAS	Decrease in DAS28-CRP No significant differences for TJC, SJC, VAS, CRP, RF

Outcome	OR [95% CI]	I²; p-value	Number of patients (periodontal treatment/no treatment)	Number of studies (References)
DAS 28	-1.18 [-1.43, -0.93]	0%; <0.00001	27/22	2 (Al-Katma et al.²⁵25 Al-Katma K, Bissada NF, Bordeaux JM, Sue J, Askari AD. Control of periodontal infection reduces the severity of active rheumatoid arthritis. JCR. 2007;13:134-7.; Ortiz et al.²⁷27 Ortiz P, Bissada NF, Palomo L, Han YW, Al-Zahrani MS, Panneerselvam A, et al. Periodontal therapy reduces the severity of active rheumatoid arthritis in patients treated with or without tumor necrosis factor inhibitors. J Periodontol. 2009;80:535-40.)
CRP	-0.16 [-0.64, 0.33]	77%; 0.53	41/44	2 (Okada et al.²⁹29 Okada M, Kobayashi T, Ito S, Yokoyama T, Abe A, Murasawa A, et al. Periodontal treatment decreases levels of antibodies to Porphyromonas gingivalis and citrulline in patients with rheumatoid arthritis and periodontitis. J Periodontol. 2013;84:e74-84.; Pinho et al.²⁶26 Pinho MN, Oliveira RDR, Novaes JRAB. Relationship between periodontitis and rheumatoid arthritis and the effect of non-surgical periodontal treatment. Braz Dent J. 2009;20:355-64.)
ESR	-6.68 [-28.57, 15.21]	97%; 0.55	32/27	2 (Al-Katma et al.²⁵25 Al-Katma K, Bissada NF, Bordeaux JM, Sue J, Askari AD. Control of periodontal infection reduces the severity of active rheumatoid arthritis. JCR. 2007;13:134-7.; Pinho et al.²⁶26 Pinho MN, Oliveira RDR, Novaes JRAB. Relationship between periodontitis and rheumatoid arthritis and the effect of non-surgical periodontal treatment. Braz Dent J. 2009;20:355-64.)
TJC	-2.97 [-8.76, 2.82]	97%; 0.31	43/41	2 (Al-Katma et al.²⁵25 Al-Katma K, Bissada NF, Bordeaux JM, Sue J, Askari AD. Control of periodontal infection reduces the severity of active rheumatoid arthritis. JCR. 2007;13:134-7.; Okada et al.²⁹29 Okada M, Kobayashi T, Ito S, Yokoyama T, Abe A, Murasawa A, et al. Periodontal treatment decreases levels of antibodies to Porphyromonas gingivalis and citrulline in patients with rheumatoid arthritis and periodontitis. J Periodontol. 2013;84:e74-84.)
SJC	-2.53 [-5.89, 0.83]	96%; 0.14	43/41	2 (Al-Katma et al.²⁵25 Al-Katma K, Bissada NF, Bordeaux JM, Sue J, Askari AD. Control of periodontal infection reduces the severity of active rheumatoid arthritis. JCR. 2007;13:134-7.; Okada et al.²⁹29 Okada M, Kobayashi T, Ito S, Yokoyama T, Abe A, Murasawa A, et al. Periodontal treatment decreases levels of antibodies to Porphyromonas gingivalis and citrulline in patients with rheumatoid arthritis and periodontitis. J Periodontol. 2013;84:e74-84.)
Global VAS	-1.56 [-8.14, 5.02]	84%; 0.84	43/41	2 (Al-Katma et al.²⁵25 Al-Katma K, Bissada NF, Bordeaux JM, Sue J, Askari AD. Control of periodontal infection reduces the severity of active rheumatoid arthritis. JCR. 2007;13:134-7.; Okada et al.²⁹29 Okada M, Kobayashi T, Ito S, Yokoyama T, Abe A, Murasawa A, et al. Periodontal treatment decreases levels of antibodies to Porphyromonas gingivalis and citrulline in patients with rheumatoid arthritis and periodontitis. J Periodontol. 2013;84:e74-84.)

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[1] *Corresponding author. E-mail: dccalderaro@gmail.com, dccalderaro@hotmail.com (D.C. Calderaro).

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Influence of periodontal treatment on rheumatoid arthritis: a systematic review and meta-analysis☆ ☆ Study conducted at Universidade Federal de Minas Gerais, Faculdade de Odontologia e Faculdade de Medicina, Departamento do Aparelho Locomotor, Belo Horizonte, MG, Brazil.

ABSTRACT

Objective:

Methods:

Results:

Conclusions:

Influence of periodontal treatment on rheumatoid arthritis: a systematic review and meta-analysis^☆ ☆ Study conducted at Universidade Federal de Minas Gerais, Faculdade de Odontologia e Faculdade de Medicina, Departamento do Aparelho Locomotor, Belo Horizonte, MG, Brazil.