Temporomandibular joint involvement in children with juvenile idiopathic arthritis: a preliminary report

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Temporomandibular joint involvement in children with juvenile idiopathic arthritis: a preliminary report

D1X XShelly Abramowicz,D2X XDMD, MPH, FACS, Associate Professor,aD3X XJoshua M. Levy,D4X XDMD, MD, Resident,b D5X XSampath Prahalad,D6X XMD, MSc, Professor,cD7X XCurtis D. Travers,D8X XMPH,dand

D9X XSheila T. Angeles-Han,D10X XMD, MSc, Associate Professore

Objective. Children with juvenile idiopathic arthritis (JIA) are at risk for temporomandibular joint (TMJ) arthritis. This can lead to pain, limited mouth opening, facial asymmetry, and malocclusion. Our objective was to characterize patients with JIA and TMJ involvement in a single center.

Study Design. This was a retrospective study of children with JIA evaluated at Children’s Healthcare of Atlanta. Inclusion criteria were confirmed JIA and jaw complaints. Medical records were reviewed to document demographics, JIA information, age at first TMJ complaint, and involvement of other joints. Descriptive statistics were computed.

Results. Majority of patients were white (mean age 13 years; range 5-18 years) with polyarticular rheumatoid factor (RF) negative or oligoarticular persistent JIA. Some were antinuclear antibody (ANA) positive, RF positive, or human leukocyte antigen (HLA)- B27 positive. Patients had involvement of other joints (e.g., fingers, knees, wrists). Of those with TMJ symptoms, 6 (10%) had TMJ arthritis.

Conclusions. In our cohort, 60 (10%) of patients were diagnosed with TMJ arthritis. In this population, patients who are female, white, RF negative, HLA-B27 negative, ANA negative, and polyarticular RF-negative subtype and have involvement of other joints have a higher likelihood of having TMJ symptoms. If a patient meets these criteria, careful evaluation of TMJs should take place.

(Oral Surg Oral Med Oral Pathol Oral Radiol 2019;127:1923)

Juvenile idiopathic arthritis (JIA) is the most common rheumatic disease of childhood. The disease affects approximately 300,000 children in the United States.1 JIA is defined by the International League of Associations for Rheumatology (ILAR) as arthritis of unknown etiology that begins in children at age 16 years or less.

The diagnosis is based on a combination of medical his- tory, clinical presentation, and radiologic and laboratory abnormalities. Accordingly, JIA is categorized into 7 sub- types (systemic, oligoarthritis, RF-positive, RF-negative,

psoriatic, enthesitis-related, undifferentiated). The diag- nosis is based on the presence of 2 of the following fea- tures for at least 6 weeks: pain or limitation of motion, warmth overlying joint, and joint swelling.2 Children with JIA often develop inflammation of the temporoman- dibular joint (TMJ), with a reported prevalence between 17% and 87%.3-6Untreated TMJ involvement in children with JIA can lead to restricted mandibular growth, caus- ing jaw asymmetry, malocclusion, and limited maximal incisal opening.4,7-10

Diagnosis of TMJ involvement in children with JIA remains a challenge. It would be beneficial to be able to identify children who are at high risk for TMJ involvement. Providers would be able to refer and intervene sooner and likely help prevent progression.

TMJ involvement can be present in all subtypes of JIA.11Sometimes it is the only involved joint7,12The purpose of this study was to characterize a population of patients with TMJ involvement in a single-center cohort study of patients with JIA.

Statement of Clinical Relevance

Temporomandibular joint involvement in children with juvenile idiopathic arthritis can lead to restricted mandibular growth, jaw asymmetry, mal- occlusion, and limited mouth opening. It would be beneficial to identify children who are at high risk for temporomandibular joint involvement to prevent progression.

Presented at the Annual Meeting of the American Association of Oral and Maxillofacial Surgeons; Las Vegas, NV, USA, September 2226, 2016, and at the Pediatric Rheumatology Symposium, Hous- ton, TX, USA, May 1720, 2017.

Dr. Angeles-Han received funding support from the National Eye Institute (K23 EY021760), Bethesda, MD, USA.

aDivision of Oral and Maxillofacial Surgery, Departments of Surgery and Pediatrics, Emory University School of Medicine and Associate Chief, Section of Dentistry/Oral and Maxillofacial Surgery, Child- ren’s Healthcare of Atlanta, Atlanta, GA, USA.

bDivision of Oral and Maxillofacial Surgery, Department of Surgery, Emory University School of Medicine, Atlanta, GA, USA.

cEmory University School of Medicine and Chief, Division of pediat- ric rheumatology, Children’s Healthcare of Atlanta, Atlanta, GA, USA.

dDepartment of Pediatrics, Emory University School of Medicine, Atlanta, GA, USA.

eDepartment of Pediatrics, University of Cincinnati, Cincinnati Children’s Hospital Medical Center, Cincinnati, OH, USA.

Received for publication Mar 26, 2018; returned for revision Jun 29, 2018; accepted for publication Jul 9, 2018.

Ó 2018 Elsevier Inc. All rights reserved.

2212-4403/$-see front matter

http://doi.org/10.1016/j.oooo.2018.07.008

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MATERIALS AND METHODS

This study was approved by the Emory University Institutional Review Board (IRB00017214) and con- formed to the US Health Insurance Portability and Pri- vacy Act requirements. Informed consent was obtained from parents and children, as appropriate.

This was a retrospective study of children with JIA evaluated by the Pediatric Rheumatology division at the Children’s Healthcare of Atlanta (CHOA, Atlanta, GA) from November 2011 to December 2015. Patients were diagnosed with JIA by a pediatric rheumatologist according to the International League of Associations for Rheumatology (ILAR) criteria.11 A description of JIA and its subtypes is beyond the scope of this article and can be found elsewhere.2Children were enrolled at varied time points after their JIA diagnosis and followed up prospectively from time of enrollment. They returned for their usual follow-up clinic visit every 3 to 6 months.

Inclusion criteria consisted of the following: (1) a confirmed diagnosis of JIA by a pediatric rheumatolo- gist, (2) evaluation by rheumatology service, and (3) TMJ involvement (pain or limited function as identi- fied by the patient or an abnormal result on clinical examination). All patients were enrolled in a study assessing uveitis in JIA. Exclusion criteria consisted of the following: (1) incomplete medical records of the initial cohort; (2) presence of congenital or acquired facial anomalies (e.g., hemifacial macrosomia, cleft lip and palate, Treacher Collins syndrome, TMJ ankylosis, etc.); or (3) a history of facial fractures. As part of par- ticipation in the uveitis study, patients responded to a questionnaire regarding symptoms (including jaw symptoms) during each rheumatology visit. When indi- cated, patients were referred for a detailed evaluation by the Oral and Maxillofacial Surgery department.

TMJ magnetic resonance imaging (MRI) was ordered, depending on patient history and clinical examination findings by an oral and maxillofacial surgeon (OMS).

Medical records were reviewed to document demo- graphics (sex, race, age, parents’ self-described race and ethnicity), JIA information (onset, age at first TMJ com- plaint, date of diagnosis, JIA subtype, joints [in addition to TMJ] with tenderness, swelling or limitation), labora- tory results (rheumatoid factor [RF], antinuclear anti- body [ANA], human leukocyte antigen [HLA]-B27, anticyclic citrullinated peptide, erythrocyte sedimenta- tion rate), and imaging reports (MRI). Follow-up data were collected at 3- to 6-month intervals from the time of the last study visit to the current study visit.

Patient information was recorded on a spreadsheet.

Statistical analyses were conducted by using SAS ver- sion 9.4 for Windows (SAS Institute, Cary, NC). Data were summarized by using means and standard devia- tions, medians and interquartile ranges (25th-75th per- centiles), or counts and percentages, when appropriate.

RESULTS

This cohort consisted of 330 patients with JIA. Of these, 60 patients (52 females, 8 males) had TMJ symptoms and met the inclusion criteria (Table I).

Table I. Summary of patients (N = 60)

Characteristic N (%)(mean [range])

Sex

- Female 52 (86.7%)

- Male 8 (13.3%)

Race

- White 43 (71.7%)

- Black 4 (6.7%)

- Hispanic 7 (11.7%)

- Other 6 (10%)

Age at first Jaw complaint, median (IQR) (N = 20)*

13 (10-16)

RF Lab (N = 52)

- Positive 5 (9.6%)

- Negative 47 (90.4%)

HLA B27 Status (N = 49)

- Positive 9 (18.4%)

- Negative 40 (81.6%)

ANA Status

- Positive 26 (43.3%)

- Negative 34 (56.7%)

Other Jointsy

- None 22 (36.7%)

- Fingers 18 (30%)

- Knees 18 (30%)

- Wrists 14 (23.3%)

- Hips 9 (15%)

- Back 7 (11.7%)

- Ankles 6 (10%)

- Entheses 5 (8.3%)

- Toes 4 (6.7%)

- Neck 2 (3.3%)

- Shoulders 2 (3.3%)

- Elbows 2 (3.3%)

Subtype

- Polyarticular RF negative 19 (31.7%) - Oligoarticular, persistent 15 (25%)

- Enthesitis related 9 (15%)

- Oligoarticular, extended 7 (11.7%)

- Polyarticular RF positive 4 (6.7%)

- Systemic 3 (5%)

- Psoriatic 2 (3.3%)

- Undifferentiated 1 (1.7%)

Current Medicationsy

- NSAIDs 41 (68.3%)

- Methotrexate 37 (61.7%)

- None 7 (11.7%)

- Prednisone 7 (11.7%)

- Adalimumab 7 (11.7%)

- Etanercept 5 (8.3%)

- Infliximab 3 (5.0%)

- Mycophenolate 1 (1.7%)

*First jaw complaint on study.

yNot mutually exclusive. Percentages may add to more than 100%.

ANA, antinuclear antibody; HLA, human leukocyte antigen; IQR, interquartile range; NSAIDs, nonsteroidal anti-inflammatory drugs;

RF, rheumatoid factor; SD, standard deviation.

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Of the 60 patients who met the inclusion criteria, mean age was 13 years (range 5-18 years). Most were white (n = 43 [71.7%]) and the rest were His- panic (n = 7 [11.7%]), black (n = 4 [6.7%]), or other (n = 6 [10%]). JIA categories were polyarticular RF negative (n = 19), oligoarticular persistent (n = 15), enthesitis related (n = 9), oligoarticular extended (n = 7), polyarticular RF positive (n = 4), systemic (n = 3), psoriatic (n = 2), and undifferentiated (n = 1) (Figure 1). Overall, 38 patients (63%) had involve- ment of joints other than TMJ, for example, fingers (n = 18, 30%), knees (n = 18, 30%), and wrists (n = 14, 23.3%) (Figure 2). Most of the patients were ANA negative (34 [90.4%]), RF negative (47 [18.4%]), or HLA-B27 negative (40 [81.6%]).

Patients were taking the following systemic medica- tions at the time of initial TMJ symptoms: nonsteroi- dal anti-inflammatory drugs (NSAIDs; n = 41 [68.3%]), methotrexate (n = 37 [61.7%]), prednisone (n = 7 [11.7%]), adalimumab (n =7 [11.7%]), etaner- cept (n = 5 [8.3%]), infliximab (n = 3 [5%]), or

mycophenolate (n = 1 [1.7%]). Seven patients (11.7%) were not taking any medications (Table II).

All patients were referred for a detailed evaluation by an OMS. Of them, 9 (15%) underwent MRI. Six (10%) had evidence of TMJ synovitis or degenerative condylar changes on MRI and were ultimately diagnosed with TMJ arthritis. They underwent TMJ surgery (i.e., lysis, lavage, or arthroscopy). Eventually, the dosage of systemic medi- cations was escalated (seeTable II).

DISCUSSION

In previous studies, estimates of TMJ involvement in JIA ranged from 17% to 87% as a result of differing methods of evaluation and examination. In our popula- tion, age at first jaw complaint was 13 years. This age, which is older than the typical age of JIA diagnosis, is important to note because long-term TMJ degeneration is associated with younger age at JIA onset.13 In our population, the majority of patients (n = 38 [63%]) had involvement of other joints. This finding is similar to that in other studies where patients had involvement of

Fig. 2. Other joint involvement in children with temporomandibular joint (TMJ) involvement.

Fig. 1. Juvenile idiopathic arthritis (JIA) subtypes of patients.

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other joints14 but different from that of a recent study where the initial manifestation of JIA was TMJ arthritis.12

Previous studies have found a higher prevalence of TMJ symptoms in patients with the systemic subtype of JIA and polyarticular involvement.14 However, unlike those in other studies, our population had the highest prevalence of TMJ symptoms in the polyarticu- lar RF-negative subtype, whereas the systemic subtype had only 3% involvement. In a previous study, investi- gators found that HLA-B27 positivity was associated with a lower incidence of TMJ involvement.11 The results of our study are similar to the findings of that study; the majority of our patients were HLA-B27 neg- ative.

In our cohort, 60 patients (18%) experienced jaw symp- toms either prior to or during enrollment in the study. In children diagnosed with JIA, untreated TMJ symptoms can lead to malocclusion, asymmetry, and decreased man- dibular opening.9Thus, early diagnosis and prevention are essential. The differentiation between TMJ arthritis and myofascial pain dysfunction (MPD)15in patients with con- firmed JIA and jaw pain may be difficult, and the distinc- tion may not be completely clear.16However, it is critical to determine if a patient has MPD, TMJ arthritis, or both because the management strategies are different.17Patients diagnosed with MPD should be treated with nonsurgical interventions (e.g., diet adjustments, behavior modifica- tions, physical therapy, or an occlusal splint). Patients with TMJ synovitis may receive lysis and lavage of TMJ, arthroscopy with or without steroid injections or a change in systemic medications. Those diagnosed with TMJ syno- vitis and MPD should be treated for both concurrently.16,17 Patients with TMJ synovitis, as seen on MRI, should be considered for TMJ lysis and lavage. However, use of routine corticosteroid injections after lysis and lavage is controversial because of the risk for further TMJ erosion.18Nevertheless, in a symptomatic (pain, limited maximal incisal opening) patient with other- wise well-controlled disease where MPD has been eliminated, TMJ lysis and lavage, perhaps with steroid injections as a temporary measure to decrease symp- toms, should be considered. Another option is TMJ arthroscopy, which allows for direct examination of the synovium.19 This is part of an ongoing investiga- tion, which will serve as a follow-up to the present study. The present study serves as a preliminary inves- tigation on JIA.

There were limitations in this study because of its retrospective design. Some patients did not follow up with the OMS, and therefore TMJ involvement could not be confirmed. This may have been a result of diffi- cult access or referral patterns. In addition, patients were referred to the OMS at variable intervals after the initial JIA diagnosis. At our institution, we now have a TableII.CharacteristicsofsubjectswithTMJinvolvement(orarthritisifjustified) SubjectSexRaceJIAsubtypeAgeatfirstjawcomplaintRFstatus)ANAstatus)HLA-B27status)OMSintervention 1FemaleWhiteOligo-persistentUnknown* (<6years)NegativePositiveNotdoneRarthroscopy 2FemaleMulti-racialOligo-extendedUnknown* (<14years)NegativeNegativeNegativeRarthroscopy,Llysisandlavage 3FemaleWhitePoly-RF-negative13yearsNegativePositiveNotdoneBarthrocentesis,eventuallyBTMJreplacement 4FemaleMulti-racial,Oligo-persistent11yearsNegativeNegativeNotdoneNonsurgicalintervention 5FemaleMulti-racialPoly-RF-negativeUnknown* (<12years)NegativeNegativeNotdoneNonsurgicalintervention 6FemaleWhiteEnthesitisrelatedUnknown* (<13years)NegativePositiveNegativeBarthroscopy 7FemaleWhiteSystemicarthritisNeveryNotdoneNegativeNotdoneBarthroscopy 8FemaleWhiteOligo-extendedUnknown* (<9years)NegativePositiveNegativeNonsurgicalintervention 9MaleWhitePoly-RF-negativeNeveryNegativeNegativeNotdoneNonsurgicalintervention ANA,antinuclearantibody;B,bilateral;L,left;HLA,humanleukocyteantigen;JIA,juvenileidiopathicarthritis;NSAIDs,nonsteroidalanti-inflammatorydrugs;OMS,oralandmaxillofacialsurgeon;R,right; RF,rheumatoidfactor;SD,standarddeviation. *Firstepisodeofjawpainwasinthepast(priortorecruitmenttostudy).Theageistheageatfirstvisit. yPatientnevercomplainedofjawpainbuthadclinicalorradiographicsignsofTMJinvolvement.

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dedicated OMS, who examines patients with JIA at regular intervals. In addition, enrolling patients at dis- ease onset in prospective studies would better enable clinicians to determine the natural history of TMJ involvement in patients with JIA. In this study, TMJ symptoms were patient reported, and this may have biased the sample toward a higher incidence because of lack of specificity. Similarly, there is a risk of miss- ing patients with asymptomatic TMJ involvement.

CONCLUSIONS

The results of this study indicate that in this study pop- ulation, TMJ arthritis occurs more often in females who are white, polyarticular RF-negative JIA subtype, HLA-B27 negative, and ANA negative, and who have involvement of other joints. It is important to evaluate patients with JIA for TMJ involvement for early recog- nition of symptoms and prevention of potential compli- cations.

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Reprint requests:

Shelly Abramowicz

Division of Oral and Maxillofacial Surgery Department of Surgery

Emory University 1365 Clifton Road NE Building B, Suite 2300 Atlanta

GA 30306 USA.

sabram5@emory.edu

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