Outcome of TMJ arthritis 1 Long-term Outcomes of Temporomandibular Joints in Juvenile Idiopathic Arthritis: 17 years of follow-up of Nordic Juvenile Idiopathic Arthritis (JIA) cohort. Mia Glerup MD 1 , Peter Stoustrup Associate Professor, DDS, PhD 2 , Louise Hauge Associate Professor, DDS, PhD 3 , Veronika Rypdal MD 4,5 , Ellen Nordal MD, PhD 4,5 , Paula Frid DDS 5,6 , Ellen Dalen Arnstad MD 7,8 , Marite Rygg Professor, MD, PhD 7,9 , Olafur Thorarensen DDS 10 , Maria Ekelund MD 11,12 , Lillemor Berntson MD, PhD 12 , Anders Fasth Professor, MD, PhD 13 , Håkan Nilsson DDS, PhD, Dr. Odont 14 , Suvi Peltoniemi MD 15 , Kristiina Aalto MD, PhD 15 , Sirpa Arte, DDS, PhD 16 , Peter Toftedal MD, PhD 17 , Susan Nielsen MD 17 , Sven Kreiborg Professor, DDS, PhD, Dr. Odont 18 , Troels Herlin Professor, MD, DMSc 1 and Thomas Klit Pedersen Professor, DDS, PhD 2,19 . 1 Department of Pediatrics, Aarhus University Hospital, Denmark, 2 Section of Orthodontics, Aarhus University, Denmark, 3 Section of Oral Radiology, Department of Dentistry and Oral Health, Aarhus University, Denmark, 4 Department of Pediatrics, University Hospital of North Norway, 5 Department of Clinical Medicine, Faculty of Health Sciences, UIT, The Arctic University of Norway, Tromsø, Norway 6 Department of Otorhinolaryngology and Department and Division of Oral and Maxillofacial Surgery, University Hospital North Norway and Public Dental Service Competence Center of North Norway, Tromsø, Norway, 7 Department of Clinical and Molecular Medicine, Faculty of Medicine and Health Sciences, NTNU - Norwegian University of Science and Technology, Trondheim, Norway, 8 Department of Pediatrics, Levanger Hospital, Nord-Trøndelag Hospital Trust, Levanger, Norway, 9 Department of Pediatrics, St. Olavs Hospital, Trondheim, Norway, 10 Department of Oral and Craniomaxillofacial Surgery, St. Olavs Hospital, Norway, NTNU, 11 Department of Pediatrics, Ryhov County Hospital, Jönköping, Sweden, 12 Department of Women´s and Children´s Health, Uppsala University, Uppsala, Sweden, 13 Department of Pediatrics, Sahlgrenska Academy, University of Gothenburg, Sweden, 14 Department of Oral and Maxillofacial Surgery/Stomatognathic Physiology, The Institute for Postgraduate Dental Education, Jönköping, Sweden, 15 Hospital for Children and Adolescents, University of Helsinki, Finland, 16 Orthodontics, Oral and Maxillofacial Diseases, University of Helsinki and Helsinki University Hospital, Finland, 17 Department of Pediatrics, Copenhagen University Hospital, Denmark, 18 Department of Pediatric Dentistry and Clinical Genetics, University of Copenhagen, Denmark, 19 Department of Oral and Maxillofacial Surgery, Aarhus University Hospital, Denmark. The study has not received any financial support or other benefits from commercial sources and the authors have no financial interests that could create a potential conflict of interest or the appearance of a conflict of interest. Correspondence to: Mia Glerup, Department of Pediatrics, Aarhus University Hospital, Skejby, Palle Juul-Jensens Blvd. 99, 8200 Aarhus N, Denmark. Phone: +45 61333138. E-mail: [email protected]Page 1 of 22 Accepted Article This article has been accepted for publication in The Journal of Rheumatology following full peer review. This version has not gone through proper copyediting, proofreading and typesetting, and therefore will not be identical to the final published version. Reprints and permissions are not available for this version. Please cite this article as doi 10.3899/jrheum.190231. This accepted article is protected by copyright. All rights reserved. www.jrheum.org Downloaded on November 27, 2021 from
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Outcome of TMJ arthritis
1
Long-term Outcomes of Temporomandibular Joints in Juvenile Idiopathic Arthritis:
17 years of follow-up of Nordic Juvenile Idiopathic Arthritis (JIA) cohort.
Mia Glerup MD1, Peter Stoustrup Associate Professor, DDS, PhD2, Louise Hauge Associate Professor, DDS, PhD 3,
Veronika Rypdal MD4,5, Ellen Nordal MD, PhD4,5, Paula Frid DDS5,6, Ellen Dalen Arnstad MD7,8, Marite Rygg
Professor, MD, PhD7,9, Olafur Thorarensen DDS10, Maria Ekelund MD11,12, Lillemor Berntson MD, PhD12, Anders
Fasth Professor, MD, PhD13, Håkan Nilsson DDS, PhD, Dr. Odont14, Suvi Peltoniemi MD15, Kristiina Aalto MD,
PhD15, Sirpa Arte, DDS, PhD 16, Peter Toftedal MD, PhD17, Susan Nielsen MD17, Sven Kreiborg Professor, DDS, PhD,
Dr. Odont18, Troels Herlin Professor, MD, DMSc1 and Thomas Klit Pedersen Professor, DDS, PhD2,19.
1Department of Pediatrics, Aarhus University Hospital, Denmark, 2Section of Orthodontics, Aarhus University,
Denmark, 3Section of Oral Radiology, Department of Dentistry and Oral Health, Aarhus University,
Denmark, 4Department of Pediatrics, University Hospital of North Norway, 5Department of Clinical Medicine, Faculty
of Health Sciences, UIT, The Arctic University of Norway, Tromsø, Norway 6 Department of Otorhinolaryngology and
Department and Division of Oral and Maxillofacial Surgery, University Hospital North Norway and Public Dental
Service Competence Center of North Norway, Tromsø, Norway, 7Department of Clinical and Molecular Medicine,
Faculty of Medicine and Health Sciences, NTNU - Norwegian University of Science and Technology, Trondheim,
Norway, 8Department of Pediatrics, Levanger Hospital, Nord-Trøndelag Hospital Trust, Levanger,
Norway, 9Department of Pediatrics, St. Olavs Hospital, Trondheim, Norway, 10Department of Oral and
Craniomaxillofacial Surgery, St. Olavs Hospital, Norway, NTNU, 11Department of Pediatrics, Ryhov County Hospital,
Jönköping, Sweden, 12 Department of Women´s and Children´s Health, Uppsala University, Uppsala,
Sweden, 13Department of Pediatrics, Sahlgrenska Academy, University of Gothenburg, Sweden, 14Department of Oral
and Maxillofacial Surgery/Stomatognathic Physiology, The Institute for Postgraduate Dental Education, Jönköping,
Sweden, 15Hospital for Children and Adolescents, University of Helsinki, Finland, 16 Orthodontics, Oral and
Maxillofacial Diseases, University of Helsinki and Helsinki University Hospital, Finland, 17Department of Pediatrics,
Copenhagen University Hospital, Denmark, 18Department of Pediatric Dentistry and Clinical Genetics, University of
Copenhagen, Denmark, 19Department of Oral and Maxillofacial Surgery, Aarhus University Hospital, Denmark.
The study has not received any financial support or other benefits from commercial sources and the authors have no
financial interests that could create a potential conflict of interest or the appearance of a conflict of interest.
Correspondence to: Mia Glerup, Department of Pediatrics, Aarhus University Hospital, Skejby, Palle Juul-Jensens
Objective: To determine the prevalence of orofacial symptoms, dysfunctions, and deformities of the
temporomandibular joint (TMJ) in juvenile idiopathic arthritis (JIA) 17 years after disease onset.
Methods: Drawn from a prospective, population-based Nordic JIA cohort with disease onset from
1997-2000, 420 consecutive cases were eligible for orofacial evaluation of TMJ involvement. The
follow-up visit included demographic data, a standardized clinical orofacial examination, and full-
face cone-beam computed tomography (CBCT). For comparison, 200 age-matched healthy controls
were used.
Results: Of 420 eligible participants with JIA, 265 (63%) were included (mean age 23.5 ± 4.2 years) and completed a standardized clinical orofacial examination. Of these, 245 had a full-face
CBCT performed. At least one orofacial symptom was reported by 33%. Compared to controls, the
JIA group significantly more often reported TMJ pain, TMJ morning stiffness, and limitation on
chewing. Furthermore, among participants reporting complaints, the number of symptoms was also
higher in the JIA. The mean maximal incisal opening was lower in the JIA group (p<0.001), and
TMJ pain on palpation was more frequent. Condylar deformities and/or erosions were observed in
61% as assessed by CBCT, showing bilateral changes in about 70%. Risk factors of condylar
deformities were orofacial dysfunction or biologic treatment; enthesitis-related arthritis was
protective.
Conclusion: This first study on long-term consequences of TMJ involvement in a population-based
JIA cohort reports persistence of comprehensive symptoms, dysfunctions, and damage of the TMJ
into adulthood. We suggest interdisciplinary follow-up of JIA patients also in adulthood.
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juvenile idiopathic arthritis, but normal facial profile was also found at the 27-year follow-up. Scand J Rheumatol. 2010;39:373-9.15. Berntson L, Andersson Gare B, Fasth A, Herlin T, Kristinsson J, Lahdenne P, et al.Incidence of juvenile idiopathic arthritis in the Nordic countries. A population based studywith special reference to the validity of the ILAR and EULAR criteria. J Rheumatol.2003;30:2275-82.16. Nordal E, Zak M, Aalto K, Berntson L, Fasth A, Herlin T, et al. Ongoing diseaseactivity and changing categories in a long-term nordic cohort study of juvenile idiopathicarthritis. Arthritis Rheum. 2011;63:2809-18.17. Stoustrup P, Twilt M, Spiegel L, Kristensen KD, Koos B, Pedersen TK, et al. ClinicalOrofacial Examination in Juvenile Idiopathic Arthritis: International Consensus-basedRecommendations for Monitoring Patients in Clinical Practice and Research Studies. JRheumatol. 2017;44:326-33.18. Petty RE, Southwood TR, Manners P, Baum J, Glass DN, Goldenberg J, et al.International League of Associations for Rheumatology classification of juvenile idiopathicarthritis: second revision, Edmonton, 2001. J Rheumatol. 2004;31:390-2.19. Consolaro A, Ruperto N, Bazso A, Pistorio A, Magni-Manzoni S, Filocamo G, et al.Development and validation of a composite disease activity score for juvenile idiopathicarthritis. Arthritis Rheum. 2009;61:658-66.20. Consolaro A, Bracciolini G, Ruperto N, Pistorio A, Magni-Manzoni S, Malattia C, etal. Remission, minimal disease activity, and acceptable symptom state in juvenile idiopathicarthritis: defining criteria based on the juvenile arthritis disease activity score. ArthritisRheum. 2012;64:2366-74.21. Wallace CA, Ruperto N, Giannini E. Preliminary criteria for clinical remission forselect categories of juvenile idiopathic arthritis. J Rheumatol. 2004;31:2290-4.22. Stoustrup P, Resnick CM, Pedersen TK, Abramowicz S, Michelotti A, Küseler A, etal on behalf of the TMJ Juvenile Arthritis Working group (TMJaw). Standardizing Terminologyand Assessment for Orofacial Conditions in Juvenile Idiopathic Arthritis: International,Multidisciplinary Consensus-based Recommendations. J Rheumatol 2019;46:518-22.23. Beaton DE, Bombardier C, Guillemin F, Ferraz MB. Guidelines for the process ofcross-cultural adaptation of self-report measures. Spine 2000;25:3186-91.24. Stoustrup P, Kristensen KD, Kuseler A, Herlin T, Pedersen TK. Normative valuesfor mandibular mobility in Scandinavian individuals 4-17 years of age. J Oral Rehabil.2016;43:591-7.25. McHugh ML. Interrater reliability: the kappa statistic. Biochem Med (Zagreb).2012;22:276-82.26. Slade GD, Bair E, Greenspan JD, Dubner R, Fillingim RB, Diatchenko L, et al. Signsand symptoms of first-onset TMD and sociodemographic predictors of its development: theOPPERA prospective cohort study. J Pain. 2013;14(12 Suppl):T20-32 e1-3.27. Slade GD, Ohrbach R, Greenspan JD, Fillingim RB, Bair E, Sanders AE, et al. PainfulTemporomandibular Disorder: Decade of Discovery from OPPERA Studies. J Dent Res.2016;95:1084-92.28. Isong U, Gansky SA, Plesh O. Temporomandibular joint and muscle disorder-typepain in U.S. adults: the National Health Interview Survey. J Orofac Pain. 2008;22:317-22.29. Kellenberger CJ, Junhasavasdikul T, Tolend M, Doria AS. Temporomandibularjoint atlas for detection and grading of juvenile idiopathic arthritis involvement by magneticresonance imaging. Pediatr Radiol. 2018;48:411-26.
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30. Stoustrup PB, Ahlefeldt-Laurvig-Lehn N, Kristensen KD, Arvidsson LZ, Twilt M,Cattaneo PM, et al. No association between types of unilateral mandibular condylarabnormalities and facial asymmetry in orthopedic-treated patients with juvenile idiopathicarthritis. Am J Orthod Dentofacial Orthop. 2018;153:214-23.31. Kellenberger CJ, Bucheli J, Schroeder-Kohler S, Saurenmann RK, Colombo V, EttlinDA. Temporomandibular joint magnetic resonance imaging findings in adolescents with anteriordisk displacement compared to those with juvenile idiopathic arthritis. J Oral Rehabil. 2019; 46:14-2232. Kristensen KD, Stoustrup P, Kuseler A, Pedersen TK, Twilt M, Herlin T. Clinical predictors of temporomandibular joint arthritis in juvenile idiopathic arthritis: A systematic literature review. Semin Arthritis Rheum. 2016;45:717-32.33. Pedersen TK, Jensen JJ, Melsen B, Herlin T. Resorption of the temporomandibular condylar bone according to subtypes of juvenile chronic arthritis. J Rheumatol. 2001;28:2109-15.34. Twilt M, Mobers SM, Arends LR, ten Cate R, van Suijlekom-Smit L. Temporomandibular involvement in juvenile idiopathic arthritis. J Rheumatol. 2004;31:1418-22.35. Consolaro A, Ravelli A. Unraveling the Phenotypic Variability of Juvenile Idiopathic Arthritis across Races or Geographic Areas--Key to Understanding Etiology and Genetic Factors? J Rheumatol. 2016;43:683-5.36. Hatcher D. Progressive Condylar Resorption: Pathologic Processes and Imaging Considerations. Seminars in Orthodontics. 2013;19:97-105.
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Table 1 Demographic and clinical characteristics by JIA categories in the TMJ study of the Nordic JIA cohort at the 17-year follow-up visit.
No of pati-ents
Total cohort (n=265)
sJIA
(n=11)
Oligo persist(n=56)
Oligo ext(n= 58)
Poly RF-(n=52)
Poly RF+(n=4)
Psoriatic
(n=14)
ERA
(n=27)
Undiff
(n=43)
Females (%) 265 186(70.6)
8/11(72.7)
40/56(71.4)
44/58(75.9)
38/52(73.1)
3/4(75.0)
10/14(71.4)
9/27(33.3)
35/43(81.4)
Age at onset mean±(SD)
265 6.2(4.0)
5.0(2.9)
5.5(3.5)
4.9(3.9)
5.9(4.1)
11.1(2.6)
6.4(3.7)
9.0(3.4)
7.3(4.0)
Age at last follow up mean±(SD)
265 23.5(4.2)
23.0(3.1)
22.7(3.5)
22.0(4.0)
22.9(4.3)
28.7(2.6)
23.4(4.2)
26.4(3.5)
24.8(4.5)
Disease duration mean±(SD)
265 17.3(1.0)
17.9(0.8)
17.3(1.1)
17.2(1.1)
17.2(1.0)
17.6(1.0)
17.0(0.9)
17.4(1.1)
17.3(0.9)
ANA positive,n (%)
234 80(34.2)
2(25.0)
12(21.4)
20(34.5)
15(28.8)
2(50.0)
5(35.7)
8(29.6)
16(36.4)
HLA-B27 positive, n (%)
264 57(21.6)
0(0.0)
6(10.7)
7(12.1)
8(15.4)
1(25.0)
3(21.4)
21(77.8)
11(25.0)
CRP >10 mg/L,n (%)
257 14(5.4)
0 1/53(1.9)
2/55(3.6)
3/52(5.8)
0 2/14(14.3)
4/27(14.8)
2/42(4.8)
ESR >20 mm/h,n (%)
218 15(6.7)
0 2/48(4.2)
2/48(4.2)
3/47(6.4)
0 3/14(21.4)
2/22(9.1)
3/33(9.1)
PatPain VAS Median(IQR)*
260 1.0(0-3.5)
0(0-2.0)
0(0-2.0)
1.0(0-4.0)
1.0(0-4.0)
5.0(2.0-6.5)
1.5(0-3.0)
1.0(0.5-3.5)
2.0(0.5-4.8)
PatGA VASmedian (IQR)*
260 1.0(0-3.0)
0(0-1.0)
0(0-1.0)
1.0(0-2.5)
0.8(0-2.8)
4.0(1.3-7.8)
1.0(0-2.0)
2.0(1.0-4.5)
2.0(0-4.5)
PhysGA VAS median (IQR)
265 0(0-1.0)
0(0-0.5)
0(0-0)
0(0-1.5)
0(0-0.8)
1.0(0-2.5)
0(0-1.0)
1.0(0-2.5)
0(0-2.0)
JADAS 71 ≤1 n (%)
244 97(39.8)
8(80.0)
31(63.3)
19(36.5)
21(42.0)
1(25.0)
5(38.5)
3(11.5)
9(22.5)
Values: Age at onset, age at last follow-up and disease duration: years, CRP =mg/L,ESR =mm/h, No = number. IQR =1st-3rd inter quartile range, Pat Pain VAS =patient´s intensity of pain on a 21-numbered circle visual analog scale (0-100). Pat GA VAS =the patient´s global assessment of the overall wellbeing on a 21-numbered circle visual analog scale. PhysGA VAS =the physician´s global assessment of disease activity on a 21-numbered circle visual analog scale. PhysGA is reported if a follow-up visit was performed. sJIA = systemic JIA, Oligo persist =oligo persistent JIA, oligo ext =oligo extended JIA, Poly RF- =polyarticular rheumatoid factor negative JIA, Poly RF+ =polyarticular rheumatoid factor positive JIA, ERA =enthesitis-related arthritis, Undiff =undifferentiated JIA. * =Statistical significance (p ≤ 0.05) among the JIA categories.
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Number of dysfunctions Per subject; median (1st-3rd quartile) 1(0;2) 0 (0;2) z=2.34 0.02 *
Values indicate the number and percentage of patients. 1Pain frequency =1 indicates not every week; 2 =several times a week; 3 =several times a day; 4 =all the time. 2Pain index =pain frequency x pain intensity 3MIO =maximal incisal opening <-2SD below mean of normative values (<40.9mm, ref (27)), 4OR =odds ratio, 5z =z score, *= Statistical significance (p ≤ 0.05).
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Table 3 CBCT appearance of the condylar head of the left and right temporomandibular joints in the Nordic JIA cohort at the 17-year follow-up visit (n=245).
Values indicate the number and percentage of joints. Each TMJ was scored as normal/abnormal and the abnormal joints were subsequently scored with deformity/erosion or with a combination of the two possibilities. The scoring system does not refer to a scale with gradual progression. Normal =normal condylar shape with smooth and intact outline/surface. Deformation =deformity of the condyle, with marked flattening or other changes in shape with smooth and intact outline/surface. Erosion =erosion of the condyle, with disruption of outline or uneven surface due to cysts or erosion. Deformity and erosion =deformities plus erosive changes.
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Table 5 Associations between clinical characteristics at baseline, 8-year follow-up or at any time during the disease course and condylar deformities/erosions at the 17-year follow-up.
Multivariate odds ratio (95% CI)
P-value
PREDICTORS EARLY IN DISEASE COURSEn=211
Age at onset < 6 yearsFemale genderActive joint count at baseline visit > 4 joints ESR > 20 at baseline
Cumulative active joint count >4 JADI-A >0MTX BiologicsERA
ASSOCIATIONS DURING THE DISEASE COURSE**n=244
Age at onset < 6 yearsFemale genderDMARDs during disease course Biologics during disease course Cumulative active joints >4 at 17-year FUOrofacial dysfunction at 17-year FUERA