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Utility of corticosteroid injection for temporomandibular arthritis in children with juvenile idiopathic arthritis.

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ARTHRITIS & RHEUMATISM
Vol. 52, No. 11, November 2005, pp 3563–3569
DOI 10.1002/art.21384
© 2005, American College of Rheumatology
Utility of Corticosteroid Injection for
Temporomandibular Arthritis in
Children With Juvenile Idiopathic Arthritis
Bita Arabshahi,1 Esi Morgan Dewitt,2 Ann Marie Cahill,2 Robin D. Kaye,2 Kevin M. Baskin,2
Richard B. Towbin,2 and Randy Q. Cron2
Objective. To assess the effects of computed tomography (CT)–guided injection of corticosteroid into
the temporomandibular joint (TMJ) in children with
juvenile idiopathic arthritis (JIA) and clinical and
magnetic resonance imaging (MRI) evidence of TMJ
inflammation.
Methods. Twenty-three children ages 4–16 years
with JIA and MRI evidence of TMJ inflammation
received CT-guided TMJ injections of corticosteroid
(triamcinolone acetonide [n ⴝ 16] or triamcinolone
hexacetonide [n ⴝ 7]). Jaw pain or dysfunction and
maximal incisal opening (MIO) distance were assessed
before and after injection. Fourteen patients had followup MRI studies of the TMJ 6–12 months after
injection.
Results. Of the 13 patients with symptoms of jaw
pain prior to corticosteroid treatment, 10 (77%) had
complete resolution of pain (P < 0.05). Prior to corticosteroid injection, MIO in all 23 patients was below
age-matched normal values. After injection, the MIO
was improved by at least 0.5 cm in 10 patients (43%)
(P ⴝ 0.0017). Patients under 6 years of age at the time
of injection showed the best response, with a postinjection MIO similar to that in age-matched controls (P ⴝ
0.2267). There was involvement of 23 TMJs in the 14
patients who had followup MRI studies; resolution of
effusions was observed in 11 (48%) of the TMJs. Other
than short-term facial swelling in 2 patients, there were
no side effects.
Conclusion. The majority of children with symptomatic TMJ arthritis improved after intraarticular
corticosteroid injection. Approximately half the patients
experienced significant improvement in MIO and TMJ
effusion. These data suggest that corticosteroid injection
may be a useful procedure for the prevention and treatment of morbidities associated with TMJ arthritis in JIA.
Juvenile idiopathic arthritis (JIA) occurs in ⬃1 in
1,000 children worldwide (1). Involvement of the temporomandibular joint (TMJ) in JIA was recognized as
early as 1897 (2). The reported prevalence of TMJ
arthritis has varied widely (i.e., 17–87%), based on
subtype of JIA, methods used for diagnosis, and population studied (3). The worst outcomes are reported in
patients with systemic or polyarticular disease, positive
antinuclear antibodies (ANAs), and decreased mouth
opening (4,5).
Unlike other diarthrodial joints, the mandibular
growth plate is located just beneath the fibrocartilage of
the condylar head, making it particularly vulnerable to
inflammatory damage. Arthritis-induced destruction of
this fibrocartilage can lead to significant limitations in
mandibular growth and development (6). Resultant abnormalities include micrognathia in up to 30% of children with JIA, and malocclusion in up to 69% (7,8).
Other complications include decreased mouth opening,
chewing difficulties, and pain with jaw movement (9).
Clinical signs associated with TMJ inflammation include
Dr. Cron’s work was supported by grants from the Ethel
Brown Foerderer Fund for Excellence and the Nickolett Family
Awards Program for JRA Research.
1
Bita Arabshahi, MD: Children’s Hospital of Philadelphia,
Philadelphia, Pennsylvania; 2Esi Morgan Dewitt, MD (current address: Duke University Medical Center, Durham, NC), Ann Marie
Cahill, MD, Robin D. Kaye, MD, Kevin M. Baskin, MD, Richard B.
Towbin, MD, Randy Q. Cron, MD, PhD: Children’s Hospital of
Philapelphia and University of Pennsylvania School of Medicine,
Philadelphia, Pennsylvania.
Address correspondence and reprint requests to Bita Arabshahi, MD, Children’s Hospital of Philadelphia, Center for Childhood
Arthritis and Rheumatic Disease, 3405 Civic Center Boulevard, Philadelphia, PA 19104-4399. E-mail: arabshahi@email.chop.edu.
Submitted for publication February 14, 2005; accepted in
revised form July 27, 2005.
3563
3564
pain with jaw excursion, asymmetric jaw opening, crepitation, and absence of jaw translation (9). Not all
children with TMJ arthritis have clinical signs, making
clinical examination alone inadequate for detecting condylar degeneration in JIA (10).
Magnetic resonance imaging (MRI) with gadolinium enhancement is currently the gold standard for
diagnosing TMJ inflammation (11). Unlike plain film
tomography, enhanced MRI can be used to detect early
inflammatory changes such as synovial proliferation and
joint effusions preceding the development of cartilage
destruction and bony erosions (12). Studies using animal
models have confirmed the correlation between histologic findings in TMJ arthritis and early inflammatory
changes detected by MRI (13). Earlier detection of
disease may in turn allow for earlier therapeutic intervention.
Modalities for the treatment of TMJ arthritis in
JIA have included systemic drugs such as methotrexate
(MTX), as well as local treatments using arthrocentesis,
occlusal devices, and intraarticular injections of steroids
or sodium hyaluronate (14–18). Among these, intraarticular corticosteroid injections show the most promise
for controlling the inflammation with little or no systemic effect. Intraarticular corticosteroids have proven
beneficial in prevention of leg-length discrepancy in
children with oligoarthritis of the knee (19). By inference, the use of these agents in TMJ arthritis could
potentially prevent mandibular growth alterations,
which lead to micrognathia and jaw deviation. Studies of
TMJ corticosteroid injection in JIA are few (17,18).
Horton first reported on this procedure in 1953 (20), but
many pediatric rheumatologists have been reluctant to
recommend it based on reports of steroid-induced chondrolysis in adults with TMJ pain (21). Preliminary
short-term results from Cahill and colleagues suggest a
good symptomatic response to intraarticular steroid
injection without evidence of complication in children
with JIA (22). Long-term studies by 2 groups in Sweden
(23,24) also show a favorable prognosis, with condylar
remineralization and remodeling, and symptomatic improvement in pain and jaw mobility, 8–12 years following corticosteroid injection.
Our aim in the present study was to investigate
the safety and effectiveness of TMJ corticosteroid injections in a cohort of patients with JIA. We used clinical
examination, pre- and postinjection MRI, and a postinjection patient questionnaire to assess side effects and
response to treatment.
ARABSHAHI ET AL
PATIENTS AND METHODS
Patients. Twenty-three patients ages 4–16 years who
attended the pediatric rheumatology clinic at Children’s Hospital of Philadelphia during the years 2000–2004 underwent
corticosteroid injection of 1 or more TMJs, based on clinical
evidence of TMJ disease that was confirmed by evidence of
TMJ inflammation seen on MRI. All children had JIA based
on the Durban criteria (25). None had isolated TMJ involvement or cervical spine arthritis. Six to 12 months after intraarticular steroid injection, followup MRIs were obtained in 14
of the 23 patients. All patients had followup measurements of
their maximal incisal opening (MIO), and all completed a
verbal questionnaire evaluating symptoms of pain, jaw locking,
jaw appearance, and side effects following injection.
Data collection. Data were collected retrospectively
from medical records and prospectively from patient questionnaires. The medical record data collected included the following: demographic characteristics (including sex, race, age at
disease onset, duration of disease, and age at the time of
corticosteroid injection), type of JIA, concomitant drug use at
the time of corticosteroid injection, MIO, jaw deviation/
micrognathia, laboratory data, number of joints injected, and
MRI findings before and after injection (including presence of
joint effusions, bony erosions, flattening of condyles, and disk
changes). Severity of TMJ inflammation seen on pre- and
postinjection MRI was assessed as follows, based on the
grading system developed by Cahill et al (22): grade 1 ⫽
normal joint; grade 2 (acute) ⫽ presence of joint effusion,
synovial thickening, or marrow edema; grade 3 (chronic) ⫽
presence of juxtaarticular erosions; and grade 4 (chronic) ⫽
condylar sclerosis or loss of articular cartilage. Grades 3a and
4a signify acute findings in the setting of chronic findings, and
grade 5 denotes ankylosis of the TMJ. The patient satisfaction
questionnaire was administered after the injection to assess the
presence of pain, jaw locking, and chewing dysfunction before
and after injection, perceived improvement in jaw appearance,
and occurrence of side effects from the injection (including
erythema, skin atrophy, infection, and facial swelling).
Sixteen of the 23 patients were injected with 1 cc (40
mg) triamcinolone acetonide (Kenalog-40; Bristol-Myers
Squibb, New York, NY) in each of the involved TMJs. The
remaining 7 patients were injected with 1 cc (20 mg) triamcinolone hexacetonide (Aristospan-20; SAB-Pharma, Lake Forest, IL). The volume of medication injected was chosen
empirically based on the general ease of administration of this
volume into the potential joint space without resistance. Corticosteroid injections were performed by 3 experienced pediatric interventional radiologists, using a 30-gauge needle under
computed tomography (CT) guidance. Patients undergoing
injections were sedated intravenously using a combination of
fentanyl citrate 1–3 mg/kg, pentobarbital sodium 2–5 mg/kg,
and midazolam hydrochloride 0.1–0.3 mg/kg as described (22).
Pre- and postinjection MRIs were performed with gadolinium
enhancement. Children under 8 years of age were sedated for
the MRI using the above agents, and images were obtained in
open- and closed-mouth views.
Statistical analysis. The following parametric and nonparametric tests were performed to evaluate distribution and
variability in measurements: Student’s t-test, analysis of variance, Pearson’s chi-square test, and Fisher’s exact test for
CORTICOSTEROID INJECTION FOR TMJ ARTHRITIS IN JIA
3565
Table 1. Characteristics of the study population (n ⫽ 23)*
Characteristic
Sex
Female
Male
JIA onset type
Oligoarticular
Polyarticular
Psoriatic
Concomitant drugs
None
NSAIDs
NSAIDs ⫹ MTX
NSAIDs ⫹ MTX ⫹ TNF inhibitor
Positive serologic results
ANA
RF
HLA–B27
No. (%)
Age at injection,
median years
Age at JIA onset,
median years
Duration of disease,
median years
20 (87)
3 (13)
9
6
5
6
2.7
0.7
5 (22)
17 (74)
1 (4)
6
9
16
4
6
12
2
2
4.5
4 (17)
4 (17)
10 (43)
5 (22)
7
9
9
7
6
6
7
6
1
2
1.5
0.4
18 (78)
3 (13)
0 (0)
* JIA ⫽ juvenile idiopathic arthritis; NSAIDs ⫽ nonsteroidal antiinflammatory drugs; MTX ⫽ methotrexate; TNF ⫽ tumor
necrosis factor; ANA ⫽ antinuclear antibody; RF ⫽ rheumatoid factor.
1-tailed data. P values less than 0.05 were considered significant. All analyses were performed with the JMP IN version 5
package (SAS Institute, Cary, NC).
RESULTS
Demographic characteristics. The study population consisted of 20 girls and 3 boys, with a median age
of 9 years, median age at disease onset of 5.5 years, and
median disease duration of 2 years. Clinical characteristics in relation to age and disease duration are summarized in Table 1. Seventy-four percent of the patients
had polyarticular JIA, and 26% had oligoarticular JIA.
One patient had oligoarticular JIA that progressed to
psoriatic arthritis. The median age was slightly lower in
the oligoarticular JIA group, but duration of disease was
similar between the 2 groups. Seventy-eight percent of
the patients were ANA positive, and 13% were positive
for rheumatoid factor. None were positive for HLA–
B27. Seventeen percent of the patients were not receiving any medications. Another 17% were taking nonsteroidal antiinflammatory drugs (NSAIDs) (either
naproxen or ibuprofen) as monotherapy, 43% were
taking NSAIDs plus MTX, and 22% were taking
NSAIDs, MTX, and etanercept. The median age at the
time of injection, age at disease onset, and duration of
disease were similar among the 4 treatment groups.
In general, TMJ corticosteroid injections were
performed if initial MRI revealed joint effusion or
pannus formation. Based on these criteria, 6 patients
(26%) underwent unilateral TMJ corticosteroid injection and 15 (65%) underwent bilateral TMJ corticosteroid injections. Two other patients (9%) underwent
bilateral injections based on abnormalities found on
MRI of 1 TMJ and the presence of pain in the contralateral TMJ.
Subjective symptoms. Prior to corticosteroid injection, 13 patients (57%) reported having symptoms of
pain with either chewing, maximal jaw exertion, or
palpation. Of these patients, 77% had complete resolution of their pain after corticosteroid injection (P ⬍
0.05). In 2 of 3 patients with jaw locking, this improved
postinjection (Table 2). Eighteen patients (78%) had
lateral jaw deviation; 2 (9%) had micrognathia, and 3
(13%) had normal jaw size and positioning. There was
no significant improvement in jaw deviation or micrognathia following injection.
Objective signs. Prior to corticosteroid injection,
100% of the measured MIOs were below mean values in
age-matched normal subjects (26,27). Mean MIO was
slightly lower in patients with jaw pain (3.4 cm) than in
those without pain (3.8 cm). Postinjection, the mean ⫾
Table 2. Improvement in symptoms among 23 patients with JIA,
after TMJ corticosteroid injection*
No. (%) with symptom
Preinjection
Postinjection
% with symptom relief
P
Pain
Jaw locking
13 (57)
3 (13)
77
⬍0.001
3 (13)
1 (4)
67
0.17
* P values were obtained using Pearson’s chi-square test, with a 70%
hypothesized probability of improvement based on an estimated
1-sided confidence interval of 50.5–100.0. JIA ⫽ juvenile idiopathic
arthritis; TMJ ⫽ temporomandibular joint.
3566
SD MIO increased from 3.59 ⫾ 0.725 cm to 4.07 ⫾ 0.606
cm (P ⫽ 0.0017 by paired t-test). Forty-three percent of
the patients had a clinically significant improvement in
MIO of ⬎0.5 cm (equal to 1 SD of age-matched normal
means). Figure 1 demonstrates the improvement in MIO
among the subjects divided into 3 age groups at time of
injection; normative MIO data are shown for comparison. Patients of all age groups improved, but patients
injected at 0–6 years of age showed the best response,
with a postinjection MIO similar to that of age-matched
healthy children (P ⫽ 0.2267).
Results of statistical tests to evaluate whether
clinical response to treatment was associated with various clinical variables (age at disease onset, age at
injection, disease duration, JIA type, concomitant medications, serologic findings, corticosteroid preparation
injected) were largely unrevealing. The only clinical
variable associated with improvement in MIO was young
age. Children with disease onset prior to age 5 years had
a significantly greater response to injection compared
with children older than 5 years at disease onset (P ⫽
0.04). There were no statistically significant associations
between MIO improvement and other clinical variables.
Radiographic findings. Figure 2 shows the distribution of TMJ grades (22) before and after corticosteroid injection. Twenty-three TMJs in 14 patients were
evaluated by MRI before and after intraarticular steroid
injection. Ten TMJs had evidence of condylar sclerosis
as well as joint effusions prior to injection (grade IVa).
Of these, 8 improved, with resolution of effusions but no
change in bony abnormalities (grade IV). Two TMJs (1
grade IV and 1 grade I) progressed to develop an
effusion after corticosteroid injection. Bony resorption
was seen in 19 of 23 TMJs studied at baseline. Postinjection, bony resorption worsened in 3 TMJs, improved
in 1 TMJ, and remained stable in the rest.
Among the 14 patients who underwent followup
MRI, 13 (57%) of the 23 TMJs exhibited findings of
acute joint effusion at the time of the first injection.
Resolution of TMJ effusion was seen in 48% of these
TMJs, reflecting improvement in more than two-thirds
of the acutely affected joints after corticosteroid injection. An example of a TMJ in which the effusion
resolved is shown in Figure 3. Factors that significantly
correlated with resolution of MRI effusion included
polyarticular subtype of JIA (P ⫽ 0.05) and age 7–10
years at the time of injection (P ⫽ 0.03). The remaining
clinical variables (age at disease onset, disease duration,
concomitant medications, serologic findings, corticosteroid preparation injected) were not associated with
radiologic improvement as judged by the presence of
effusion postinjection. However, this analysis was lim-
ARABSHAHI ET AL
Figure 1. Improvement in maximal incisal opening (MIO) post–
corticosteroid injection. All groups improved, but patients injected at
0–6 years of age showed the best response, with a postinjection MIO
similar to that in age-matched healthy children. Values for patients
pre- and postinjection are box plots, where the boxes represent the
25th to 75th percentiles, the lines within the boxes represent the
median, and the lines outside the boxes represent the highest and
lowest values. Values for normal subjects are the mean ⫾ SD.
CORTICOSTEROID INJECTION FOR TMJ ARTHRITIS IN JIA
3567
DISCUSSION
Figure 2. Response to temporomandibular joint (TMJ) corticosteroid
injection based on magnetic resonance imaging (MRI) grade (grade
I ⫽ normal joint; grade II ⫽ joint effusion, synovial thickening, or
marrow edema; grade III ⫽ juxtaarticular erosions; grade IV ⫽
condylar sclerosis or loss of articular cartilage; grades IIIa and IVa
signify acute findings in the setting of chronic findings). Grade I joints
were injected only if there was pain and an effusion was detected in the
contralateral TMJ.
ited by the long time elapsed from corticosteroid injection to performance of followup MRI. Comparison of
clinical improvement (MIO ⬎0.5 cm) with resolution of
MRI effusion did not reveal a significant association
(P ⫽ 0.5).
Side effects. After corticosteroid injection, 2 patients developed facial swelling consistent with Cushing’s
syndrome, lasting 2 days in 1 patient and 2 weeks in the
other. There was no incidence of erythema, infection, or
subcutaneous atrophy following injection.
TMJ arthritis is common in JIA and affects all
subtypes of the disease. The majority of patients in this
study were ANA-positive girls with polyarticular JIA and
decreased MIO; none were positive for HLA–B27. This
pattern is consistent with previous descriptions of risk
factors in patients with TMJ inflammation (4,5). Bilateral TMJ involvement was seen more commonly than
unilateral involvement in our patients; other reports on
this have varied (3). Early-onset disease (prior to age 9
years) was also seen more commonly, and could explain
the high prevalence of lateral jaw deviation (78%) or
micrognathia (9%) observed in our patients. Considering that the majority of mandibular growth occurs in the
first decade of life, alterations in the condylar growth
plate during this time have a large impact on final
mandibular structure. In our observations, the jaw deviated toward the TMJ with the higher degree of inflammation or bony resorption, consistent with decreased
growth of the mandible on the involved side.
Although more than half of our patients reported
having jaw pain prior to corticosteroid injection, the
presence of jaw pain did not significantly correlate with
the presence of effusions on MRI (P ⫽ 0.96). In fact,
effusions were seen more frequently in patients who did
not have pain (80%) than in those who were symptomatic (53%). Prior to corticosteroid injection, mean MIO
was slightly lower in patients with jaw pain than in those
without, perhaps reflecting pain-limited movement of
the jaw at the time of MIO measurement. However, this
Figure 3. Resolution of effusion post–corticosteroid injection. A, T2-weighted proton-density parasagittal
magnetic resonance image (MRI) through the right temporomandibular joint, showing an effusion (arrowhead)
just anterior to the condyle (C) in the superior and inferior synovial spaces. B, Followup T2-weighted MRI of the
same joint post–corticosteroid injection, showing resolution of the effusion (arrowhead).
3568
difference was not statistically significant (P ⫽ 0.24).
Despite the observation that corticosteroid injections
alleviated pain in more than two-thirds of symptomatic
patients, one-third of these patients had persistence of
effusions on followup MRI. Although the number of
symptomatic patients in our study was small, these data
suggest that the presence or resolution of pain may not
accurately predict the presence of TMJ inflammation.
Since the pain assessment questionnaire was administered after the injections, recall bias may play a role in
these findings.
Limitations in mouth opening are often not obvious to patients unless they are accompanied by symptoms (27). Nevertheless, based on Sheppard and Sheppard’s analysis of MIO in normal subjects versus those
with periodontal or TMJ disease, failure to open ⱖ3.5–
4.0 cm is indicative of some restraining effect on mandibular function warranting further investigation (26). In
our study, 70% of the patients had a preinjection MIO of
⬍4.0 cm. This decreased to 39% postinjection. The most
significant improvements were seen in patients diagnosed before 5 years of age and those injected at 0–6
years of age. This suggests that early intervention,
particularly in patients in whom mandibular growth is
not completed, results in greater response to treatment.
One of the most objective means of assessing
TMJ inflammation in JIA is MRI evaluation. The use of
gadolinium enhances synovial proliferation and joint
effusions, which precede bony erosions (28). In our
patient population, the majority of TMJs studied by
followup MRI showed bony erosions at baseline, and
therefore had an arthropathy grade of III or higher
before administration of corticosteroids. This reflects
longstanding TMJ arthritis in most of the children
studied. Corticosteroid injections resulted in resolution
of effusions in more than two-thirds of TMJs with acute
effusions at baseline. One limitation to this finding is
that followup MRIs were performed 6–12 months after
corticosteroid injection, and it is possible that the TMJs
not showing improvement had initially responded to
corticosteroid injection but had recurrent disease by the
time the MRI was repeated.
In contrast to our expectations, patients with
polyarticular JIA had a greater response to corticosteroid injection in terms of effusion resolution (P ⫽
0.05), even though clinical response based on MIO was
better in the oligoarticular disease group. As a result,
we were not able to demonstrate a significant relationship between clinical and radiologic improvement after
corticosteroid injection (P ⫽ 0.5). One possible explanation for this discrepancy is that the head coil used
ARABSHAHI ET AL
during MRI acquisition may be more sensitive in detecting joint effusions in older children, who comprised
the majority of the polyarticular disease group. The use
of a surface coil during imaging would allow detection
of joint effusions in younger patients with greater sensitivity. Additionally, pre- and postinjection MRIs were
often not read by the same radiologist, introducing a
possible source of assessor bias in the interpretation of
MRI results.
In the majority of patients in our study, there
were no side effects from TMJ corticosteroid injection.
In the 2 patients who experienced facial swelling, the
effects were relatively short in duration, and not accompanied by any subcutaneous atrophy or pain. The use of
CT guidance to ensure proper needle placement prior to
injection was effective in minimizing potential side effects, although ultrasound guidance may be just as effective
while allowing both real-time assessment during needle
positioning and confirmation of intraarticular injection.
Interestingly, 15 of the 23 children with JIA and
TMJ arthritis in this study were being treated with MTX
(in general, 1 mg/kg/week subcutaneously). In addition,
5 of these 15 patients were receiving a tumor necrosis
factor inhibitor at the time of TMJ corticosteroid injection (Table 1). This provides indirect evidence that the
combination of MTX and tumor necrosis factor inhibition, in at least a subset of children with JIA, is inadequate to control the destructive changes seen with TMJ
arthritis. This may reflect a slightly different cartilage
composition of the TMJ and/or the close proximity of
the mandibular growth plate to the thin overlying cartilage. Regardless of the reason, it is instructive and
suggests that children with JIA and TMJ arthritis should
be treated by intraarticular corticosteroid injection, possibly along with other therapies.
Our study was limited by small sample size, lack
of treatment controls, assessor bias, recall bias, and a
relatively short followup period. However, the findings
illustrate that JIA patients with jaw deviation or limited
incisal opening often have advanced TMJ arthritis,
which responds best to corticosteroid injection if instituted early. Initiation of an early radiographic and
clinical screening program to detect TMJ arthritis in
children with JIA would allow earlier intervention to
preserve normal jaw structure and function. Future
studies on the incidence of TMJ arthritis in JIA and
clinical predictors of active disease would aid in this
effort and are currently under way at our institution.
This report is dedicated to the memory of Dr. Frida
Gudmundsdottir.
CORTICOSTEROID INJECTION FOR TMJ ARTHRITIS IN JIA
3569
ACKNOWLEDGMENTS
The authors thank Dr. David D. Sherry for critical
review of the manuscript and Dr. Andrew J. Cucchiara for
assistance with statistical analysis.
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idiopathic, temporomandibular, injections, arthritis, corticosterone, juvenile, children, utility
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