Skip to main content
Top
Published in: Pediatric Rheumatology 1/2018

Open Access 01-12-2018 | Research article

Clinical features of children with enthesitis-related juvenile idiopathic arthritis / juvenile spondyloarthritis followed in a French tertiary care pediatric rheumatology centre

Authors: Maxime Goirand, Sylvain Breton, Frédéric Chevallier, Ngoc-Phoi Duong, Florence Uettwiller, Isabelle Melki, Richard Mouy, Carine Wouters, Brigitte Bader-Meunier, Chantal Job-Deslandre, Pierre Quartier

Published in: Pediatric Rheumatology | Issue 1/2018

Login to get access

Abstract

Background

Childhood-onset spondyloarthropathies usually start with enthesitis and peripheral arthritis. However, axial disease may develop afterward. Patients are most often classified, following revised (Edmonton 2011) ILAR criteria, as enthesitis-related arthritis, psoriatic arthritis, or unclassified juvenile idiopathic arthritis, particularly in cases of psoriasis in the patient or a first-degree relative. In adults, peripheral spondyloarthritis is classified by ASAS criteria.

Methods

We retrospectively studied patients with childhood-onset spondyloarthropathies followed for more than one year in our referral centre. We did not exclude patients with a personal or familial history of psoriasis.

Results

We included 114 patients followed between January 2008 and December 2015 for a median of 2.5 years (IQR = 2.3). Sixty-nine per-cent of patients fulfilled the revised ILAR classification criteria for enthesitis-related arthritis, and 92% the ASAS criteria for peripheral spondyolarthritis (p <  0.001). Axial disease and sacroiliitis were rare at disease onset. However, they appeared during follow-up in 63% and 47% of cases respectively, after a median disease duration of 2.6 (IC 95% [2.2–4.4]) and 5.3 years (IC 95% [4.1–7.7]), respectively. Multivariable analysis showed that familial history of spondyloarthritis was associated with the presence of sacroiliitis and active disease at the latest follow-up (OR = 3.61 [1.5–8.7], p <  0.01 and 2.98 [1.2–7.3], p = 0.02, respectively).

Conclusion

Axial involvement developed in most patients within five years. Revised Edmonton criteria were less sensitive than ASAS criteria to classify patients as having childhood-onset spondyloarthropathies. The main risk factor for both sacroiliitis and persistent active disease was a familial history of spondyloarthritis.
Appendix
Available only for authorised users
Literature
1.
go back to reference Ravelli A, Martini A. Juvenile idiopathic arthritis. Lancet Lond Engl. 2007;369:767–78.CrossRef Ravelli A, Martini A. Juvenile idiopathic arthritis. Lancet Lond Engl. 2007;369:767–78.CrossRef
2.
go back to reference Petty RE, Southwood TR, Manners P, Baum J, Glass DN, Goldenberg J, et al. International league of associations for rheumatology classification of juvenile idiopathic arthritis: second revision, Edmonton, 2001. J Rheumatol. 2004;31:390–2.PubMed Petty RE, Southwood TR, Manners P, Baum J, Glass DN, Goldenberg J, et al. International league of associations for rheumatology classification of juvenile idiopathic arthritis: second revision, Edmonton, 2001. J Rheumatol. 2004;31:390–2.PubMed
3.
go back to reference Weiss PF. Diagnosis and treatment of enthesitis-related arthritis. Adolesc Health Med Ther. 2012;2012:67–74.CrossRefPubMed Weiss PF. Diagnosis and treatment of enthesitis-related arthritis. Adolesc Health Med Ther. 2012;2012:67–74.CrossRefPubMed
4.
go back to reference Tubergen AV, Weber U. Diagnosis and classification in spondyloarthritis : identifying a chameleon. Nat Rev Rheumatol. 2012;8:253–61.CrossRefPubMed Tubergen AV, Weber U. Diagnosis and classification in spondyloarthritis : identifying a chameleon. Nat Rev Rheumatol. 2012;8:253–61.CrossRefPubMed
5.
go back to reference Burgos-Vargas R. The assessment of the spondyloarthritis international society concept and criteria for the classification of axial spondyloarthritis and peripheral spondyloarthritis: a critical appraisal for the pediatric rheumatologist. Pediatr Rheum Online J. 2012;10:14.CrossRef Burgos-Vargas R. The assessment of the spondyloarthritis international society concept and criteria for the classification of axial spondyloarthritis and peripheral spondyloarthritis: a critical appraisal for the pediatric rheumatologist. Pediatr Rheum Online J. 2012;10:14.CrossRef
6.
go back to reference Flatø B, Hoffmann-Vold A-M, Reiff A, Førre Ø, Lien G, Vinje O. Long-term outcome and prognostic factors in enthesitis-related arthritis: a case-control study. Arthritis Rheum. 2006;54:3573–82.CrossRefPubMed Flatø B, Hoffmann-Vold A-M, Reiff A, Førre Ø, Lien G, Vinje O. Long-term outcome and prognostic factors in enthesitis-related arthritis: a case-control study. Arthritis Rheum. 2006;54:3573–82.CrossRefPubMed
7.
go back to reference Stone M, Warren RW, Bruckel J, Cooper D, Cortinovis D, Inman RD. Juvenile-onset ankylosing spondylitis is associated with worse functional outcomes than adult-onset ankylosing spondylitis. Arthritis Rheum. 2005;53:445–51.CrossRefPubMed Stone M, Warren RW, Bruckel J, Cooper D, Cortinovis D, Inman RD. Juvenile-onset ankylosing spondylitis is associated with worse functional outcomes than adult-onset ankylosing spondylitis. Arthritis Rheum. 2005;53:445–51.CrossRefPubMed
8.
go back to reference Rudwaleit M, van der Heijde D, Landewé R, Listing J, Akkoc N, Brandt J, et al. The development of assessment of SpondyloArthritis international society classification criteria for axial spondyloarthritis (part II): validation and final selection. Ann Rheum Dis. 2009;68:777–83.CrossRefPubMed Rudwaleit M, van der Heijde D, Landewé R, Listing J, Akkoc N, Brandt J, et al. The development of assessment of SpondyloArthritis international society classification criteria for axial spondyloarthritis (part II): validation and final selection. Ann Rheum Dis. 2009;68:777–83.CrossRefPubMed
9.
go back to reference Rudwaleit M, van der Heijde D, Landewé R, Akkoc N, Brandt J, Chou CT, et al. The assessment of SpondyloArthritis international society classification criteria for peripheral spondyloarthritis and for spondyloarthritis in general. Ann Rheum Dis. 2011;70:25–31.CrossRefPubMed Rudwaleit M, van der Heijde D, Landewé R, Akkoc N, Brandt J, Chou CT, et al. The assessment of SpondyloArthritis international society classification criteria for peripheral spondyloarthritis and for spondyloarthritis in general. Ann Rheum Dis. 2011;70:25–31.CrossRefPubMed
10.
go back to reference Katsicas, MM, Russo RAG. Classification of juvenile spondylarthropathies according to ASAS criteria. Katsicas, MM, Russo RAG. Classification of juvenile spondylarthropathies according to ASAS criteria.
11.
go back to reference Landais P, Messiaen C, Rath A, Le Mignot L, Dufour E, Ben Said M, et al. CEMARA an information system for rare diseases. Stud Health Technol Inform. 2010;160:481–5.PubMed Landais P, Messiaen C, Rath A, Le Mignot L, Dufour E, Ben Said M, et al. CEMARA an information system for rare diseases. Stud Health Technol Inform. 2010;160:481–5.PubMed
12.
go back to reference Landis JR, Koch GG. The measurement of observer agreement for categorical data. Biometrics. 1977;33:159–74.CrossRefPubMed Landis JR, Koch GG. The measurement of observer agreement for categorical data. Biometrics. 1977;33:159–74.CrossRefPubMed
15.
go back to reference Pagnini I, Savelli S, Matucci-Cerinic M, Fonda C, Cimaz R, Simonini G. Early predictors of juvenile sacroiliitis in enthesitis-related arthritis. J Rheumatol. 2010;37:2395–401.CrossRefPubMed Pagnini I, Savelli S, Matucci-Cerinic M, Fonda C, Cimaz R, Simonini G. Early predictors of juvenile sacroiliitis in enthesitis-related arthritis. J Rheumatol. 2010;37:2395–401.CrossRefPubMed
16.
go back to reference Weiss PF, Klink AJ, Behrens EM, Sherry DD, Finkel TH, Feudtner C, et al. Enthesitis in an inception cohort of enthesitis-related arthritis. Arthritis Care Res. 2011;63:1307–12.CrossRef Weiss PF, Klink AJ, Behrens EM, Sherry DD, Finkel TH, Feudtner C, et al. Enthesitis in an inception cohort of enthesitis-related arthritis. Arthritis Care Res. 2011;63:1307–12.CrossRef
17.
go back to reference Sarma PK, Misra R, Aggarwal A. Outcome in patients with enthesitis related arthritis (ERA): juvenile arthritis damage index (JADI) and functional status. Pediatr Rheum Online J. 2008;6:18.CrossRef Sarma PK, Misra R, Aggarwal A. Outcome in patients with enthesitis related arthritis (ERA): juvenile arthritis damage index (JADI) and functional status. Pediatr Rheum Online J. 2008;6:18.CrossRef
18.
go back to reference Burgos-Vargas R, Vázquez-Mellado J, Pacheco-Tena C, Hernández-Garduño A, Goycochea-Robles MV. A 26 week randomised, double blind, placebo controlled exploratory study of sulfasalazine in juvenile onset spondyloarthropathies. Ann Rheum Dis. 2002;61:941–2.CrossRefPubMedPubMedCentral Burgos-Vargas R, Vázquez-Mellado J, Pacheco-Tena C, Hernández-Garduño A, Goycochea-Robles MV. A 26 week randomised, double blind, placebo controlled exploratory study of sulfasalazine in juvenile onset spondyloarthropathies. Ann Rheum Dis. 2002;61:941–2.CrossRefPubMedPubMedCentral
19.
go back to reference Minden K, Niewerth M, Listing J, Biedermann T, Bollow M, Schöntube M, et al. Long-term outcome in patients with juvenile idiopathic arthritis. Arthritis Rheum. 2002;46:2392–401.CrossRefPubMed Minden K, Niewerth M, Listing J, Biedermann T, Bollow M, Schöntube M, et al. Long-term outcome in patients with juvenile idiopathic arthritis. Arthritis Rheum. 2002;46:2392–401.CrossRefPubMed
20.
go back to reference Aggarwal A, Hissaria P, Misra R. Juvenile ankylosing spondylitis--is it the same disease as adult ankylosing spondylitis? Rheumatol Int. 2005;25:94–6.CrossRefPubMed Aggarwal A, Hissaria P, Misra R. Juvenile ankylosing spondylitis--is it the same disease as adult ankylosing spondylitis? Rheumatol Int. 2005;25:94–6.CrossRefPubMed
21.
go back to reference Burgos-Vargas R, Pacheco-Tena C, Vázquez-Mellado J. A short-term follow-up of enthesitis and arthritis in the active phase of juvenile onset spondyloarthropathies. Clin Exp Rheumatol. 2002;20:727–31.PubMed Burgos-Vargas R, Pacheco-Tena C, Vázquez-Mellado J. A short-term follow-up of enthesitis and arthritis in the active phase of juvenile onset spondyloarthropathies. Clin Exp Rheumatol. 2002;20:727–31.PubMed
22.
go back to reference Ramanathan A, Srinivasalu H, Colbert RA. Update on juvenile spondyloarthritis. Rheum Dis Clin N Am. 2013;39:767–88.CrossRef Ramanathan A, Srinivasalu H, Colbert RA. Update on juvenile spondyloarthritis. Rheum Dis Clin N Am. 2013;39:767–88.CrossRef
23.
go back to reference Burgos-Vargas R. The assessment of the spondyloarthritis international society concept and criteria for the classification of axial spondyloarthritis and peripheral spondyloarthritis: a critical appraisal for the pediatric rheumatologist. Pediatr Rheum Online J. 10:2012, 14. BioMed Central Ltd Burgos-Vargas R. The assessment of the spondyloarthritis international society concept and criteria for the classification of axial spondyloarthritis and peripheral spondyloarthritis: a critical appraisal for the pediatric rheumatologist. Pediatr Rheum Online J. 10:2012, 14. BioMed Central Ltd
24.
go back to reference Tse SML, Laxer RM. New advances in juvenile spondyloarthritis. Nat Rev Rheumatol. 2012;8:269–79. Nature Publishing GroupCrossRefPubMed Tse SML, Laxer RM. New advances in juvenile spondyloarthritis. Nat Rev Rheumatol. 2012;8:269–79. Nature Publishing GroupCrossRefPubMed
25.
go back to reference Lin C, MacKenzie JD, Courtier JL, Gu JT, Milojevic D. Magnetic resonance imaging findings in juvenile spondyloarthropathy and effects of treatment observed on subsequent imaging. Pediatr Rheum Online J. 2014;12:25.CrossRef Lin C, MacKenzie JD, Courtier JL, Gu JT, Milojevic D. Magnetic resonance imaging findings in juvenile spondyloarthropathy and effects of treatment observed on subsequent imaging. Pediatr Rheum Online J. 2014;12:25.CrossRef
26.
go back to reference Roussou E, Ciurtin C. Clinical overlap between fibromyalgia tender points and enthesitis sites in patients with spondyloarthritis who present with inflammatory back pain. Clin Exp Rheumatol. 2012;30:24–30.PubMed Roussou E, Ciurtin C. Clinical overlap between fibromyalgia tender points and enthesitis sites in patients with spondyloarthritis who present with inflammatory back pain. Clin Exp Rheumatol. 2012;30:24–30.PubMed
27.
go back to reference Aloush V, Ablin JN, Reitblat T, Caspi D, Elkayam O. Fibromyalgia in women with ankylosing spondylitis. Rheumatol Int. 2007;27:865–8.CrossRefPubMed Aloush V, Ablin JN, Reitblat T, Caspi D, Elkayam O. Fibromyalgia in women with ankylosing spondylitis. Rheumatol Int. 2007;27:865–8.CrossRefPubMed
28.
go back to reference Althoff CE, Feist E, Burova E, Eshed I, Bollow M, Hamm B, et al. Magnetic resonance imaging of active sacroiliitis: do we really need gadolinium? Eur J Radiol. 2009;71:232–6.CrossRefPubMed Althoff CE, Feist E, Burova E, Eshed I, Bollow M, Hamm B, et al. Magnetic resonance imaging of active sacroiliitis: do we really need gadolinium? Eur J Radiol. 2009;71:232–6.CrossRefPubMed
29.
go back to reference Horneff G, Burgos-Vargas R, Constantin T, Foeldvari I, Vojinovic J, Chasnyk VG, et al. Efficacy and safety of open-label etanercept on extended oligoarticular juvenile idiopathic arthritis, enthesitis-related arthritis and psoriatic arthritis: part 1 (week 12) of the CLIPPER study. Ann Rheum Dis. 2014;73:1114–22.CrossRefPubMed Horneff G, Burgos-Vargas R, Constantin T, Foeldvari I, Vojinovic J, Chasnyk VG, et al. Efficacy and safety of open-label etanercept on extended oligoarticular juvenile idiopathic arthritis, enthesitis-related arthritis and psoriatic arthritis: part 1 (week 12) of the CLIPPER study. Ann Rheum Dis. 2014;73:1114–22.CrossRefPubMed
30.
go back to reference Horneff G, Foeldvari I, Minden K, Trauzeddel R, Kümmerle-Deschner JB, Tenbrock K, et al. Efficacy and safety of etanercept in patients with the enthesitis-related arthritis category of juvenile idiopathic arthritis: results from a phase III randomized, double-blind study. Arthritis Rheum. 2015;67:2240–9. Hoboken NJCrossRef Horneff G, Foeldvari I, Minden K, Trauzeddel R, Kümmerle-Deschner JB, Tenbrock K, et al. Efficacy and safety of etanercept in patients with the enthesitis-related arthritis category of juvenile idiopathic arthritis: results from a phase III randomized, double-blind study. Arthritis Rheum. 2015;67:2240–9. Hoboken NJCrossRef
31.
go back to reference Burgos-Vargas R, Tse SML, Horneff G, Pangan AL, Kalabic J, Goss S, et al. A randomized, double-blind, placebo-controlled multicenter study of adalimumab in pediatric patients with Enthesitis-related arthritis. Arthritis Care Res. 2015;67:1503–12.CrossRef Burgos-Vargas R, Tse SML, Horneff G, Pangan AL, Kalabic J, Goss S, et al. A randomized, double-blind, placebo-controlled multicenter study of adalimumab in pediatric patients with Enthesitis-related arthritis. Arthritis Care Res. 2015;67:1503–12.CrossRef
32.
go back to reference Horneff G, Fitter S, Foeldvari I, Minden K, Kuemmerle-Deschner J, Tzaribacev N, et al. Double-blind, placebo-controlled randomized trial with adalimumab for treatment of juvenile onset ankylosing spondylitis (JoAS): significant short term improvement. Arthritis Res Ther. 2012;14:R230.CrossRefPubMedPubMedCentral Horneff G, Fitter S, Foeldvari I, Minden K, Kuemmerle-Deschner J, Tzaribacev N, et al. Double-blind, placebo-controlled randomized trial with adalimumab for treatment of juvenile onset ankylosing spondylitis (JoAS): significant short term improvement. Arthritis Res Ther. 2012;14:R230.CrossRefPubMedPubMedCentral
33.
go back to reference Windschall D, Müller T, Becker I, Horneff G. Safety and efficacy of etanercept in children with the JIA categories extended oligoarthritis, enthesitis-related arthritis and psoriasis arthritis. Clin Rheumatol. 2015;34:61–9.CrossRefPubMed Windschall D, Müller T, Becker I, Horneff G. Safety and efficacy of etanercept in children with the JIA categories extended oligoarthritis, enthesitis-related arthritis and psoriasis arthritis. Clin Rheumatol. 2015;34:61–9.CrossRefPubMed
34.
go back to reference Stoll ML, Bhore R, Dempsey-Robertson M, Punaro M. Spondyloarthritis in a pediatric population: risk factors for sacroiliitis. J Rheumatol. 2010;37:2402–8.CrossRefPubMedPubMedCentral Stoll ML, Bhore R, Dempsey-Robertson M, Punaro M. Spondyloarthritis in a pediatric population: risk factors for sacroiliitis. J Rheumatol. 2010;37:2402–8.CrossRefPubMedPubMedCentral
35.
go back to reference Fisher C, Ioannou J, Sen D. Enthesitis related arthritis- 2 distinct clinical phenotypes? Pediatr Rheumatol. 2011;9:P151.CrossRef Fisher C, Ioannou J, Sen D. Enthesitis related arthritis- 2 distinct clinical phenotypes? Pediatr Rheumatol. 2011;9:P151.CrossRef
36.
go back to reference Ravelli A, Consolaro A, Schiappapietra B, Martini A. The conundrum of juvenile psoriatic arthritis. Clin Exp Rheumatol. 2015;33:40–3. Ravelli A, Consolaro A, Schiappapietra B, Martini A. The conundrum of juvenile psoriatic arthritis. Clin Exp Rheumatol. 2015;33:40–3.
37.
go back to reference Martini A. It is time to rethink juvenile idiopathic arthritis classification and nomenclature. Ann Rheum Dis. 2012;71:1437–9.CrossRefPubMed Martini A. It is time to rethink juvenile idiopathic arthritis classification and nomenclature. Ann Rheum Dis. 2012;71:1437–9.CrossRefPubMed
38.
go back to reference Katsicas MM, Russo RA. Classification of juvenile spondyloarthropaties according to ASAS criteria. Pediatr Rheumatol. 2014;12:O10.CrossRef Katsicas MM, Russo RA. Classification of juvenile spondyloarthropaties according to ASAS criteria. Pediatr Rheumatol. 2014;12:O10.CrossRef
39.
go back to reference Sieper J, van der Heijde D, Landewé R, Brandt J, Burgos-Vagas R, Collantes-Estevez E, et al. New criteria for inflammatory back pain in patients with chronic back pain: a real patient exercise by experts from the assessment of SpondyloArthritis international society (ASAS). Ann Rheum Dis. 2009;68:784–8.CrossRefPubMed Sieper J, van der Heijde D, Landewé R, Brandt J, Burgos-Vagas R, Collantes-Estevez E, et al. New criteria for inflammatory back pain in patients with chronic back pain: a real patient exercise by experts from the assessment of SpondyloArthritis international society (ASAS). Ann Rheum Dis. 2009;68:784–8.CrossRefPubMed
Metadata
Title
Clinical features of children with enthesitis-related juvenile idiopathic arthritis / juvenile spondyloarthritis followed in a French tertiary care pediatric rheumatology centre
Authors
Maxime Goirand
Sylvain Breton
Frédéric Chevallier
Ngoc-Phoi Duong
Florence Uettwiller
Isabelle Melki
Richard Mouy
Carine Wouters
Brigitte Bader-Meunier
Chantal Job-Deslandre
Pierre Quartier
Publication date
01-12-2018
Publisher
BioMed Central
Published in
Pediatric Rheumatology / Issue 1/2018
Electronic ISSN: 1546-0096
DOI
https://doi.org/10.1186/s12969-018-0238-9

Other articles of this Issue 1/2018

Pediatric Rheumatology 1/2018 Go to the issue