Int. J. Oral Maxillofac. Surg.

2011; 40: 704–709

doi:10.1016/j.ijom.2011.02.026, available online at http://www.sciencedirect.com

Clinical Paper
TMJ Disorders

Temporomandibular joint A. Aliko1,, R. Ciancaglini2,3,

A. Alushi1, A. Tafaj4, D. Ruci4
1
Stomatology Department, Faculty of

involvement in rheumatoid Medicine, University of Tirana, Albania;

2
Department of Biomedical Sciences and
Technology, University of Milan, Italy; 3Dental
Clinic, San Paolo Hospital, Milan, Italy;

arthritis, systemic lupus 4

Rheumatology Clinic, University Hospital
‘‘Mother Theresa’’, Tirana, Albania

erythematosus and systemic

sclerosis
A. Aliko, R. Ciancaglini, A. Alushi, A. Tafaj, D. Ruci: Temporomandibular joint
involvement in rheumatoid arthritis, systemic lupus erythematosus and systemic
sclerosis. Int. J. Oral Maxillofac. Surg. 2011; 40: 704–709. # 2011 International
Association of Oral and Maxillofacial Surgeons. Published by Elsevier Ltd. All rights
reserved.

Abstract. The aim of the present study was to estimate the prevalence of
temporomandibular joint (TMJ) symptoms and clinical findings in Albanian
patients with rheumatoid arthritis, systemic lupus erythematosus and systemic
sclerosis. The authors examined 124 consecutive hospitalized patients (88 with
rheumatoid arthritis, 22 with systemic lupus erythematosus and 14 with systemic
sclerosis) and 124 age- and gender-matched healthy controls using a questionnaire
and an oro-facial clinical examination for assessing the presence of TMJ sounds,
pain in the TMJ area, tenderness of masticatory muscles and limited mouth opening.
Significantly more patients (67%) reported TMJ symptoms than controls (19%). A
significantly higher proportion of patients (65%) exhibited clinical signs of
temporomandibular dysfunction compared with controls (26%). The most frequent
findings in rheumatoid arthritis were temporomandibular sounds and pain. Pain was
found in a significantly higher proportion in patients with systemic lupus
Keywords: temporomandibular joint; rheuma-
erythematosus compared with controls. Difficulty and limitation in mouth opening
toid arthritis; systemic lupus erythematosus;
were observed in the majority of systemic sclerosis patients, and in only a minority systemic sclerosis.
of rheumatoid arthritis patients. This study supports the notion that TMJ
examination should be encouraged in the rheumatology setting and clinicians Accepted for publication 22 February 2011
should be able to provide pain management and patient support. Available online 3 April 2011

Rheumatoid arthritis (RA), systemic lupus
erythematosus (SLE) and systemic sclero-
sis (SSc) are amongst the main systemic
rheumatic diseases. Their aetiology and
pathogenesis is multifactorial and com-
plex. It may involve genetic predisposi-
tion, immune system disturbances and
environmental factors. Hormones may
also play a role, as the diseases affect
women more than men5,6,38.
RA is characterized by symmetric, ero-
sive synovitis, which may result in joint
deformity and disability15. Being a syno-
vial joint, the temporomandibular joint
(TMJ) is subject to the same disorders

0901-5027/070704 + 06 $36.00/0 # 2011 International Association of Oral and Maxillofacial Surgeons. Published by Elsevier Ltd. All rights reserved.

affecting other synovial joints, including
RA. TMJ involvement in RA was first
scientifically described in 1874 by GAR-
9
ROD . The frequency of its recognition in
later studies ranges widely, from 5 to
86%, depending, in part, on diagnostic
criteria, the population studied, and the
means of TMJ assessment8,34. The most
common clinical findings are pain in the
TMJ area and tenderness of the mastica-
tory muscles, joint sounds and limited
joint function4,11,29.
SLE may display a broad spectrum of
clinical manifestations with multiple end-
organ involvement. It is well known that a
great proportion of patients present with
arthritis5, but TMJ findings in SLE are
given far less attention than in RA. JONS-
SON et al. found that TMJ involvement was
common in SLE21. Although most studies
of SLE arthritis in joints other than the
TMJ have shown minimal radiographic
evidence of bone erosion35, erosion of
the TMJ condyles similar to changes seen
in RA patients was noted in 8 (11%) of the
patients investigated by JONSSON et al.
There are few case reports related to
TMJ findings in SSc, indicating resorption
of the condylar process13. It is suggested
that bone resorption is due to pressure
ischaemia (from tight skin and muscle
atrophy) and vascular ischaemia. It is
likely that atrophic and fibrotic alterations
of the synovia may also contribute to TMJ
involvement in SSc.
The aim of the present study was to
estimate the prevalence of symptoms and
clinical findings related to TMJ in Alba-
nian patients with RA, SLE and SSc and to
compare the findings with those in age-
and gender-matched healthy subjects.
Materials and methods
The patient group consisted of 124 con-
secutive hospitalized patients. 88 patients
had RA, 22 had SLE, and 14 patients had
SSc. All patients with RA met the Amer-
ican Rheumatism Association (ARA)
revised criteria for the classification of
RA3, patients with SLE met the revised
ARA criteria for the classification of
SLE39, and SSc patients fulfilled the
ACR37 and LEROY et al.28 criteria.
The controls were respondents to a
cross-sectional general health survey,
which was carried out on individuals ran-
domly selected from the Tirana population
register by the Albanian Institute of Sta-
tistics. Respondents consented to a home
visit and the authors obtained data from
124 subjects, each being matched for age
and gender with one of the patients, and
with no history of previous immune sys-
TMJ symptoms in RA, SLE and systemic sclerosis
tem/autoimmune disorder, or history of
immunosuppressive treatment.
Ethical approval was given by the
Faculty of Medicine Committee, Univer-
sity of Tirana, and patients and controls
were included during the period from May
2008 to June 2009.
A detailed medical history was taken
from all patients and controls, which
included RA, SLE and SSc history, dura-
tion of disease (defined as years since
diagnosis), and complications, a list of
other medical diagnoses, as well as med-
ical treatment. Demographic details, years
of education and urban versus rural resi-
dence were also recorded.
Examination of TMJ
The TMJ of the subjects was examined
according to WHO criteria (1997). TMJ
symptoms were recorded for all patients
and controls by means of a questionnaire.
The questions concerned TMJ sounds
(including clicking and crepitation), pain
during occlusion or mouth opening,
unprovoked pain from the TMJ area,
and difficulty in mouth opening. A single
positive statement to any of the questions
classified a subject as symptomatic.
Patients were also asked if TMJ symptoms
occurred in relation to their self-perceived
disease severity, and if they had occurred
once or periodically since the disease was
diagnosed.
The patient and control subjects under-
went a routine oro-facial examination to
detect signs of TMJ involvement. The
examination included palpation of the
masticatory muscles and TMJ. Tenderness
was recorded whenever palpation pro-
duced a palpation reflex or when the
patient reported subjective discomfort.
The following masticatory muscles were
palpated bilaterally: the posterior, middle
and anterior part of the temporalis muscle,
insertion and origin of the masseter mus-
cle, body of the masseter muscle, lateral
and medial pterygoid muscle. TMJ sounds
on mandible movement, such as clicking
(reciprocal or other) and crepitation, were
assessed by palpation on each side sepa-
rately. Maximum mouth opening (defined
as the distance between the incisal edge of
the central maxillary incisor that is most
vertically oriented and the labioincisal
edge of the opposing mandibular incisor
during maximal opening, added the
amount of vertical incisor overlap) was
measured to the nearest millimetre with a
ruler. Maximal mouth opening was con-
sidered reduced if it measured < 40 mm7.
A single positive finding classified a
subject as having objective signs of
705
TMJ dysfunction. Clinical examination
included assessment of lateral or anterior
open bite. The collection of TMJ data was
conducted by a single examiner (A.A.)
trained in the use of the assessment instru-
ments used in the study.
Statistical analysis
Statistical analysis of the differences
between the patient and the control group
were carried out using the Mc Nemar test
for paired samples. The level of signifi-
cance was set at P < 0.05. The associa-
tions between variables were analysed
using the x2 test. The data were analysed
using the SPSS/PC software version 17.0
(SPSS Inc., Chicago, IL, USA).
Results
124 RA, SLE, and SSc patients and 124
control subjects were examined. 85% of
patients and 85% of controls were female.
In the patient group the mean age was
49.3  10.0 (range 21–73) years for
females and 52.7  10.9 (range 25–70)
years for males. The mean age of the
control subjects was 50.1  12.2 (range
21–77) years for females and 50.1  12.6
(range 26–72) years for men. The mean
duration of disease for the patient group
was 9.1  8.1 (range 0.3–37) years. The
characteristics of each patient group and
controls are shown in Table 1.
Medical treatment in both groups
104 (84%) of the patients overall were
treated with oral steroids, 90 (73%) with
non-steroidal anti-inflammatory drugs
(NSAIDs), 78 (63%) with disease-modi-
fying anti-rheumatic drugs (DMARDs),
either as monotherapy, or as combination
therapy (Table 1). The most frequent oral
steroids and DMARDs given were
methylprednisolone and methotrexate,
respectively. 56 (45%) of the patients were
treated with other drugs, including heart
and vascular drugs, gastrointestinal drugs,
or hypoglycaemic drugs.
30 (24%) of the control subjects were
medically treated with drugs, mainly anti-
hypertensives and beta-blockers, and 10
were using over-the-counter analgesics.
Significantly more patients (77%) were
using analgesic drugs than were the con-
trol subjects (8%), P = 0.000.
TMJ involvement
The proportion of symptomatic subjects
was higher in the patient group (67%) than
in the control group (19%), P = 0.000. The
706 Aliko et al.

Table 1. Characteristics of the study groups. (46%) of the patients overall, or in 71% of
Rheumatoid Systemic lupus Systemic the subgroup classified as having objective
arthritis erythematosus sclerosis Controls signs of TMJ dysfunction. The majority of
(n = 88) (n = 22) (n = 14) (n = 124) patients had only one sign, but 5 of them
Gender (M/F) 17/71 0/22 2/12 19/105 had all three.
Mean age (SD), years 52.5 (8.5) 40.2 (11.6) 47.6 (8.3) 50.0 (12.2) The proportion of patients with at least
Mean duration of disease 9.5 (8.2) 6.6 (7.0) 9.4 (8.1) – one TMJ finding, either as a symptom, or
(SD), years as a clinical finding, was higher in the
Medication (no. of subjects, %) patients group (75%) than in controls
Oral steroids 72 (81.8) 20 (90.9) 12 (85.7) – (32%) (P = 0.000).
NSAIDs 66 (75.0) 15 (68.2) 9 (64.3) 4 (3.2) The breakdown of patients TMJ signs
DMARDs 61 (69.3) 13 (59.1) 4 (28.6) –
by type of disease is given in Table 2.
Monotherapy
MTX 45 (51.1) 1 (4.5) 4 (28.6) Sounds occurred frequently in all three
HCQ 6 (6.8) 9 (40.9) – patients groups, but the difference
Rituximab 1 (1.1) – – between patients and controls was statis-
Combination therapy tically significant only for the RA group.
MTX + HCQ – 3 (13.6) – Crepitation was present in 12 (14%) of the
MTX + LFL 3 (3.4) – – RA patients, but was uncommon in the
MTX + Rituximab 4 (4.5) – – other study groups. The proportion of
LFL + Rituximab 1 (1.1) – – patients with pain in palpation was sig-
MTX + LFL + Rituximab 1 (1.1) – – nificantly higher in the RA and SLE
NSAIDs, non-steroidal anti-inflammatory drugs; DMARDs, disease-modifying anti-rheumatic groups compared with controls, but no
drugs; MTX, methotrexate; HCQ, hydroxychloroquine; LFL, leflunomide. difference was found between SSc
patients and controls. Reduction in max-
imum mouth opening was found in a
frequency distributions were significantly also more prevalent in the SLE group than higher proportion in SSc patients than in
different for TMJ sounds (P = 0.000), pain in matched controls, especially pain, but controls, but no difference was found
from the TMJ area and/or during mandib- difference in the difficulty in mouth open- between RA or SLE patients and controls.
ular movement (P = 0.000), and difficulty ing was not statistically significant. The One RA patient had developed anterior
in opening mouth (P = 0.000). The most majority of SSc patients reported pain and open bite, and panoramic radiography
commonly reported symptom in patients difficulty in mouth opening. Although half revealed erosion in both condyles.
was ‘TMJ sounds’, present in 60 (48%) of the SSc patients reported TMJ sounds as
patients overall, or in 72% of the subgroup well, no statistically significant difference
Discussion
classified as ‘symptomatic’, and ‘pain’ was found with their matched controls.
reported by 59 (48%) of the patients over- Crepitation was reported by only 5 RA In the present study the prevalence of TMJ
all, or by 71% of the subgroup classified as patients and one patient with SLE. symptoms and signs of dysfunction in
‘symptomatic’. 55% of the symptomatic A higher proportion of patients (65%) Albanian hospitalized patients with RA,
patients reported more than one TMJ had objective signs of TMJ dysfunction SLE and SSc was investigated. The main
symptom, and one-quarter reported all compared with controls (26%), P = 0.000. outcome of the study is that patients with
three. All three TMJ signs were significantly RA, SLE and SSc have more TMJ symp-
The breakdown of patients’ TMJ symp- found more in the patient group compared toms, and more signs of TMJ dysfunction
toms by type of disease is given in Table 2. with controls; TMJ sounds (P = 0.000), than matched healthy controls.
All three symptoms were reported by RA pain on palpation (P = 0.000), and reduc- Despite the wide range of reported pre-
patients more often than by matched con- tion in maximum mouth opening valence of TMJ involvement in RA,
trols, especially TMJ sound, reported by (P = 0.007). The most common sign in results of most studies indicate that more
half of RA patients. TMJ symptoms were patients was ‘TMJ sounds’, found in 57 than half of patients with RA exhibit

Table 2. Temporomandibular joint (TMJ) symptoms and clinical findings in rheumatoid arthritis (RA), systemic lupus erythematosus (SLE) and
systemic sclerosis (SSc) patients and in matched controls.
No. of RA patients No. of SLE patients No. of SSc patients No. of controls
(%) n = 88 (%) n = 22 (%) n = 14 (%) n = 124
Reported symptoms
TMJ sounds 45 (51.1)** 8 (36.4)* 7 (50) 18 (14.5%)
Pain 36 (40.9)** 11 (50)* 12 (85.7)* 10 (8.1%)
Difficulty in opening mouth 14 (15.9)* 6 (27.3) 12 (85.7)* 3 (2.4%)
At least one symptom 57 (64.8)** 13 (59.1)* 13 (92.9)* 24 (19.4)
Clinical findings
TMJ sounds 44 (50)** 8 (36.4) 5 (35.7) 27 (21.8%)
Pain 24 (27.3)** 6 (27.3)* 5 (35.7) 2 (1.6%)
Reduced mouth opening 7 (8) 1 (4.5) 11 (78.6)* 6 (4.8%)
At least one clinical finding 56 (63.6)** 11 (50) 13 (92.9)* 32 (25.8)
At least one symptom or clinical finding 65 (73.9)** 14 (63.6) 14 (100)* 39 (31.5)
*
Statistically significant difference between patient and matched controls, P < 0.05.
**
Statistically significant difference between patient and matched controls, P < 0.001.

clinically evident TMJ involve-
ment4,22,27,29,31,33. 65% of the RA patients
in the present study reported having TMJ
symptoms. 64% of patients showed objec-
tive signs of involvement, confirming pre-
vious findings.
In agreement with other studies4,8,33,
the most frequent TMJ findings in RA
were sounds, which were observed in
about half of the RA patients. Sounds were
mainly observed as clicking, whilst the
frequency of crepitation on clinical exam-
ination was 14%, which contrasts with
other studies. 21% of patients studied by
KOH et al.24, and 36% of the patients of
YAMAKAWA et al. had crepitation42. The
prevalence found by HELENIUS et al. was
clearly higher (75%), but both studies
involved minor samples16,17. In a series
of 61 RA patients, 30% of the sample
presented with crepitations4. Compared
with previous studies, the frequency of
crepitation was clearly lower in the pre-
sent study. This may be partly ascribed to
the difference in medication. In the present
study, all patients were hospitalized and
were receiving either single or combina-
tion therapy with corticosteroids and
DMARDs.
Crepitation often indicates structural
damage to the TMJ8,16,18,41 and these
drugs have the potential to reduce or pre-
vent joint damage, as well as to preserve
joint integrity and function23.
It can be speculated that RA outpatients
in the other studies received less medica-
tion than the present patients, but compar-
isons cannot be made, since most of those
studies did not report on drug therapy;
however, structural TMJ change may
occur without crepitation. AKERMAN et
al. studied the relationship between clin-
ical and radiological TMJ findings in 101
patients with RA and found that although
80% of the TMJs that presented with
crepitation also exhibited radiographic
evidence of erosion, crepitation revealed
a low sensibility in detecting joints with
erosion, since half of the joints with ero-
sion presented with either a click or no
sound at all1. Lack of sounds in spite of
joint damage may be a result of remodel-
ling and adaptation of the articular sur-
faces19.
TMJ pain and masticatory muscle ten-
derness are common in RA and associated
with findings suggestive of more active
disease31. Previous studies have reported
the prevalence of reported pain in RA in
the range of 24–52% and the prevalence of
pain in palpation in the range of 40–
88%8,10,16,22,24,29. The present findings
suggest a high prevalence of pain in RA
patients and are within reported ranges.
TMJ symptoms in RA, SLE and systemic sclerosis
Although the majority of RA patients
investigated were using analgesics, a dif-
ference in the prevalence of TMJ pain and
tenderness of masticatory muscles with
control subjects was detected. This excess
in pain in relation to controls may be due
to joint inflammation12, and/or condylar
changes17 caused by RA, which may not
be controlled easily by analgesics.
Previous studies report that complaints
of difficulty in mouth opening are com-
mon in RA patients16,17,22,29,42. The
patients in the study reported here also
experienced difficulty in mouth opening
more often than controls and that may be
caused by pain, the presence of fibrous
adhesions, or a more severe degeneration
of the TMJ associated with RA12. Objec-
tive measurement of the inter-incisor dis-
tance revealed that maximal mouth
opening was reduced in a small proportion
of the RA patients and there was no sta-
tistically significant difference with the
control group. These findings are in agree-
ment with the studies of FRANKS8 and
LARHEIM & FLÖYSTRAND26, and may sug-
gest that although TMJ involvement is
common in RA, it is associated with less
functional impairment and disability than
other body joints, probably due to the
unique characteristics of the TMJ, such
as the presence of a more resistant fibro-
cartilage instead of hyaline cartilage on
the articular surfaces. LARHEIM & FLÖY-
STRAND also noted that, although mouth
opening was minimally impaired in RA
patients, condylar translation was signifi-
cantly restricted in many26.
In severe cases, when condylar support
has been lost, retrognathia and an anterior
open bite may result. Pronounced destruc-
tive changes were observed artroscopi-
cally in the two patients that developed
an anterior open bite in the study by
GYNTHER et al.12. In the present study there
was one case of anterior open bite (1%),
and panoramic radiography revealed ero-
sion in both condyles. Open bite was
registered in two (4%) of the 50 RA
patients investigated by MOEN et al.31,
and in three (5%) of the 56 RA patients
examined by LIN et al.29. Retrognathia
secondary to TMJ destruction may affect
upper/airway size and function, especially
when lying supine. Episodes of upper air-
way obstruction and sleep-breathing dis-
orders have been described in RA patients
with TMJ involvement; therefore physi-
cians should be aware of this rare, but
potentially fatal condition2.
TMJ involvement in SLE and SSc is
less documented. In a previous study on
TMJ involvement in SLE, JONSSON et al.
reported that up to two-thirds of the
707
patients have had TMJ symptoms in the
past, which were usually transient, and
almost half of the patients showed objec-
tive signs of involvement, including radio-
graphic signs21. As might be expected
from the high prevalence of arthritis in
SLE in general5, and in agreement with the
findings of JONSSON et al., TMJ symptoms
were common in SLE patients in the pre-
sent study. Pain was the most frequent
complaint reported by half of the SLE
patients. Pain during palpation was eli-
cited in 27% of the patients. Comparison
with the healthy controls indicates that
pain may be related to SLE arthritis.
SLE patients also reported TMJ sounds
more often than controls, but no statisti-
cally significant difference was detected in
TMJ sounds on palpation. A possible
explanation for this excess of complaints
of TMJ sounds, but not TMJ sounds on
palpation in SLE compared with controls,
may be that healthy subjects may tend to
overlook mild symptoms, contrary to hos-
pitalized patients, who are instructed to
report symptoms and repeatedly asked
about their joint complaints. Therefore
sounds, like reduced mouth opening, are
not related to SLE arthritis, but the rela-
tively small number of SLE patients and
matched controls examined limits the
power of this study’s conclusions.
As expected, most of the SSc patients
exhibited difficulty in mandibular move-
ment and diminished inter-incisor dis-
tance, in line with previous findings40.
Although joint involvement in general is
common in SSc30, it was not possible in
this study to determine whether the find-
ings could be attributable to TMJ involve-
ment, because fibrosis of lips, skin and
subcutaneous tissues also lead to reduced
mouth opening. As a consequence of
reduced opening, oral hygiene, eating
and performance of dental procedures
may be jeopardized. Mouth-opening lim-
itation seemed to be the main factor impli-
cated in disability due to mouth and face
involvement for SSc patients32. Dentists
should consider teaching SSc patients
exercises to increase mouth opening.
The authors observed an excess in the
rate of self-reported symptoms compared
with the respective objective findings in
patients (Table 2). This may be related to
the extent to which the condition mani-
fests itself as a single acute episode, as
repeated episodes, or as a persistent or
chronic problem. In the present study,
questions inquiring into the presence of
symptoms intended to gather information
on past and present history, whilst clinical
examination assessed only actual presence
or absence of TMJ signs, which may
708 Aliko et al.
explain the difference between self-
reported symptoms and the respective
objective findings. On the contrary, in
controls, TMJ sounds, but not pain, were
observed more often during palpation than
as a self-reported symptom, which may be
a reflection of the fact that healthy indi-
viduals are not significantly bothered by
their TMJ sounds and therefore tend to
under-report it.
TMJ changes in these patients may not be
solely due to the RA or SLE inflammatory
process. It is often difficult to discriminate
between TMJ disorders affected by sys-
temic inflammatory disease and any other
local pathology (arthritis secondary to disc
displacement, osteoarthritis, traumatic
arthritis). Radiological and magnetic reso-
nance imaging (MRI) could be included in
further studies to complete examination
and aid differential diagnosis. Contrast-
enhanced MRI would be of special value
in assessing rheumatoid pannus25, which
has been shown to be associated with RA
activity, due to its invasive and destructive
behaviour. MRI has the disadvantage of
lack of clinical availability and cost, so
high resolution ultrasound could be used
as an alternative imaging technique for
monitoring TMJ disorders20.
A limitation of this study could be the
lack of data on the psychological and
social status of patients and controls. An
examination of the psychosocial factors
appears sensible, in that anxiety, life
stress, depression and muscle hyperactiv-
ity are common in RA, SLE and SSc14,
and have often been proposed as possible
risk factors for temporomandibular disor-
ders36. The results are limited to hospita-
lized patients, who might have higher
disease activity or severity compared with
outpatients.
Within the limitations of this study, the
authors conclude that TMJ involvement is
common in patients with RA, SLE and
SSc. The results of the present study sup-
port the notion that examination of the
TMJ should be encouraged in the rheu-
matology clinic and clinicians should be
able to provide pain management and
patient support.
Funding
None.
Competing interests
None declared.
Ethical approval
Not required.
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