Periodontal disease in pediatric rheumatic
               diseases

Fabri, Gisele M.C.; Savioli, Cynthia; Siqueira, José T.; Campos, Lucia M.; Bonfá, Eloisa; Silva, Clovis A.

doi:10.1016/j.rbr.2013.11.004

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Review Articles • Rev. Bras. Reumatol. 54 (4) • Jul-Aug 2014 • https://doi.org/10.1016/j.rbr.2013.11.004 copy

Periodontal disease in pediatric rheumatic diseases

Authorship SCIMAGO INSTITUTIONS RANKINGS

Gingivitis and periodontitis are immunoinflammatory periodontal diseases characterized by chronic localized infections usually associated with insidious inflammation. This narrative review discusses periodontal diseases and mechanisms influencing the immune response and autoimmunity in pediatric rheumatic diseases (PRD), particularly juvenile idiopathic arthritis (JIA), childhood-onset systemic lupus erythematosus (C-SLE) and juvenile dermatomyositis (JDM). Gingivitis was more frequently observed in these diseases compared to health controls, whereas periodontitis was a rare finding. In JIA patients, gingivitis and periodontitis were related to mechanical factors, chronic arthritis with functional disability, dysregulation of the immunoinflammatory response, diet and drugs, mainly corticosteroids and cyclosporine. In C-SLE, gingivitis was associated with longer disease period, high doses of corticosteroids, B-cell hyperactivation and immunoglobulin G elevation. There are scarce data on periodontal diseases in JDM population, and a unique gingival pattern, characterized by gingival erythema, capillary dilation and bush-loop formation, was observed in active patients. In conclusion, gingivitis was the most common periodontal disease in PRD. The observed association with disease activity reinforces the need for future studies to determine if resolution of this complication will influence disease course or severity.

Gingivitis; Periodontitis; Periodontal diseases; Juvenile idiopathic arthritis; Childhood-onset systemic lupus; erythematosus; Juvenile dermatomyositis

Diseases	Country	Number of patients and healthy controls	Clinical and immunological findings
Walton et al., 2000²⁸28 Walton AG, Welbury RR, Thomason JM, Foster HE. Oral health and juvenile idiopathic arthritis: a review. Rheumatology (Oxford). 2000;39:550-5.	UK	Review	Negative impact of poor oral health
Miranda et al., 2003³⁷37 Miranda LA, Fischer RG, Sztajnbok FR, Figueredo CM, Gustafsson A. Periodontal conditions in patients with juvenile idiopathic arthritis. J Clin Periodontol. 2003;30:969-74.	Brazil	32 JIA patients and 24 controls	JIA adolescents presented more periodontal attachment loss than healthy controls
Welbury et al., 2003³⁵35 Welbury RR, Thomason JM, Fitzgerald JL, Steen IN, Marshall NJ, Foster HE.Increased prevalence of dental caries and poor oral hygiene in juvenile idiopathic arthritis. Rheumatology. 2003;42:1445-51.	UK	149 JIA patients and 149 controls	Increased level of poor oral hygiene and dental decay in JIA
Savioli et al., 2004³²32 Savioli C, Silva CA, Ching LH, Campos LM, Prado EF, Siqueira JT. Dental and facial characteristics of patients with juvenile idiopathic arthritis. Rev Hosp Clín Fac Med São Paulo. 2004;59:93-8.	Brazil	26 JIA patients and 13 controls	Gingivitis in JIA patients associated with upper limb disability
Ahmed et al., 2004³¹31 Ahmed N, Bloch-Zupan A, Murray KJ, Calvert M, Roberts GJ, Lucas VS. Oral health of children with juvenile idiopathic arthritis. J Rheumatol. 2004;31:1639-43.	UK	55 patients and 55 controls	Gingivitis score was significantly higher in JIA compared to controls
Miranda et al., 2005⁵⁵55 Miranda LA, Fischer RG, Sztajnbok FR, Johansson A, Figueredo CM, Gustafsson A. Increased interleukin-18 in patients with juvenile idiopathic arthritis and early attachment loss. J Periodontol. 2005;76:75-82.	Brazil	38 JIA patients and 29 controls	Increased serum IL-18 and IL-1p in JIA patients increased susceptibility to PD
Havemose-Poulsen et al., 2005³⁸38 Havemose-Poulsen A, Sørensen LK, Stoltze K, Bendtzen K, Holmstrup P. Cytokine profiles in peripheral blood and whole blood cell cultures associated with aggressive periodontitis, juvenile idiopathic arthritis, and rheumatoid arthritis. J Periodontol. 2005;76:2276-85.	Denmark	10 JIA, 23 RA, 45 aggressive periodontitis patients and 25 controls	Peripheral blood cytokine profile and citokine secretion pattern were showed in by JIA, RA and generalized aggressive periodontitis
Miranda et al., 2006³³33 Miranda LA, Braga F, Fischer RG, Sztajnbok FR, Figueredo CM, Gustafsson A. Changes in periodontal and rheumatological conditions after 2 years in patients with juvenile idiopathic arthritis. J Periodontol. 2006;77:1695-700.	Brazil	18 JIA adolescents and 14 controls	No clinical or laboratory differences in periodontal inflammation were found in JIA patients and controls
Havemose-Poulsen et al, 2006³⁹39 Havemose-Poulsen A, Westergaard J, Stoltze K, Skjødt H, Danneskiold-Samsøe B, Locht H et al. Periodontal and hematological characteristics associated with aggressive periodontitis, juvenile idiopathic arthritis, and rheumatoid arthritis. J Periodontol. 2006;77:280-8.	Denmark	10 JIA, 23 RA, 45 aggressive periodontitis patients and 25 controls	Elevated levels of traditional markers of inflammation were observed in generalized aggressive periodontitis, JIA and RA.
Reichert et al, 2006³⁶36 Reichert S, Machulla HK, Fuchs C, John V, Schaller HG, Stein J. Is there a relationship between juvenile idiopathic arthritis and periodontitis? J Clin Periodontol. 2006;33:317-23.	Germany	78 JIA patients and 75 controls	JIA was not a risk factor for periodontitis
Reichert et al., 2007⁴³43 Reichert S, Stein J, Fuchs C, John V, Schaller HG, Machulla HK. Are there common human leucocyte antigen associations in juvenile idiopathic arthritis and periodontitis? J Clin Periodontol. 2007;34:492-8.	Germany	110 JIA patients (50 of them generalized aggressive periodontitis),102 JIA with chronic periodontitis and 102 controls	HLA-DRB3n was common risk indicator for JIA and chronic periodontitis in females
Havemose-Poulsen et al, 2007⁴⁰40 Havemose-Poulsen A, Sørensen LK, Bendtzen K, Holmstrup P. Polymorphisms within the IL-1 gene cluster: effects on cytokine profiles in peripheral blood and whole blood cell cultures of patients with aggressive periodontitis, juvenile idiopathic arthritis, and rheumatoid arthritis. J Periodontol. 2007;78:475-92.	Denmark	10 JIA, 23 RA, 45 aggressive periodontitis patients and 25 controls	Variation of alleles of the IL-1 gene cluster modified the cytokine profiles of patients with aggressive periodontitis and chronic arthritis
Synodinos et al, 2008²⁹29 Synodinos PN, Polyzois I. Oral health and orthodontic considerations in children with juvenile idiopathic arthritis: review of the literature and report of a case. J Ir Dent Assoc. 2008;54:29-36.	Ireland	Review	Caries and periodontal disease related to diet, disease activity and similar inflammatory process pattern
Leksel et al, 2008³⁴34 Leksell E, Ernberg M, Magnusson B, Hedenberg-Magnusson B. Intraoral condition in children with juvenile idiopathic arthritis compared to controls. Int J Paediatr Dent. 2008;18:423-33.	Sweden	41 JIA patients and 41 controls	JIA patients showed worse periodontal condition compared to controls
Silva et al, 2012⁴⁸48 Silva TL, Braga FS, Sztajnbok FR, Souza AA, Silva FB, Fischer RG et al. Reduction in alveolar bone density of patients with juvenile idiopathic arthritis. Rev Bras Reumatol. 2012;52:38-43.	Brazil	16 JIA patients and 11 controls	Lower alveolar bone density in JIA patients

Diseases	Country	Number of patients and healthy controls	Clinical and immunological findings
JDM
Ghali et al., 1999⁶⁰60 Ghali FE, Stein LD, Fine JD, Burkes EJ, McCauliffe DP. Gingival telangiectases: an underappreciated physical sign of juvenile dermatomyositis. Arch Dermatol. 1999;135:1370-4.	USA	5 JDM patients	Gingival telangiectases
Marton et al., 2005⁵⁸58 Márton K, Hermann P, Dankó K, Fejérdy P, Madléna M, Nagy G. Evaluation of oral manifestations and masticatory force in patients with polymyositis and dermatomyositis. J Oral Pathol Med. 2005 Mar;34:164-9.	Hungary	34 JDM patients	Gingival telangiectases
Savioli et al., 2010⁵⁹59 Savioli C, Silva CA, Fabri GM, Kozu K, Campos LM, Bonfá E et al. Gingival capillary changes and oral motor weakness in juvenile dermatomyositis. Rheumatology. 2010;49:1962-70.	Brazil	26 JDM patients and 22 controls	Unique gingival pattern associated with cutaneous disease
C-SLE
Fernandes et al., 2007⁶⁴64 Fernandes EG, Savioli C, Siqueira JT, Silva CA. Oral health and the masticatory system in juvenile systemic lupus erythematosus. Lupus. 2007;16:713-9.	Brazil	48 C-SLE patients and 48 children	C-SLE patients had inadequate oral hygiene, gingivitis and temporomandibular joint dysfunction
Figueredo et al., 2008⁶⁵65 Figueredo CM, Areas A, Sztajnbok FR, Miceli V, Miranda LA, Fischer RG et al. Higher elastase activity associated with lower IL-18 in GCF from juvenile systemic lupus patients. Oral Health Prev Dent. 2008;6:75-81.	Brazil	16 C-SLE patients and 14 controls	Increased elastase activity suggested hyperactivity of neutrophils

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[1] * Corresponding author. E-mail: clovis.silva@hc.fm.usp.br (C.A. Silva).