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Int. J. Oral Maxillofac. Surg.

2001; 30: 104–112


doi:10.1054/ijom.2000.0017, available online at http://www.idealibrary.com on

Leading clinical paper:


Orthognathic surgery/trauma/TMJ disorders
Tore A. Larheim1,2
MR grading of Per-Lennart Westesson3,
Tsukasa Sano4
1

temporomandibular joint fluid: Department of Maxillofacial Radiology,


Faculty of Dentistry, University of Oslo,
Norway; 2Eastman Department of Dentistry,
University of Rochester School of Medicine

association with disk and Dentistry, NY, USA; 3Department of


Radiology, Division of Neuroradiology,
University of Rochester School of Medicine

displacement categories, and Dentistry, Rochester NY, USA;


4
Department of Oral Radiology, Showa
University School of Dentistry, Tokyo, Japan

condyle marrow abnormalities


and pain
T. A. Larheim, P.-L. Westesson, T. Sano: MR grading of temporomandibular joint
fluid: association with disk displacement categories, condyle marrow abnormalities
and pain. Int. J. Oral Maxillofac. Surg. 2001; 30: 104–112.  2001 International
Association of Oral and Maxillofacial Surgeons

Abstract. The purpose of this study was to investigate temporomandibular joint


(TMJ) effusion on magnetic resonance (MR) images, and its association with specific
categories of disk displacement, bone marrow abnormalities and pain. From a series
of 523 consecutive TMJ MR imaging studies of patients referred to imaging because
of pain and dysfunction, those with TMJ effusion, defined as an amount of fluid that
exceeded the maximum amount seen in a control group of asymptomatic volunteers,
were analysed. The selected patients were reassessed and the amount of TMJ fluid
was graded bilaterally according to a set of reference films. Other parameters
recorded included disk displacement categories and condyle marrow abnormalities.
Pain self-records were obtained from the patients immediately before MR imaging.
The association between the recorded parameters and TMJ pain was analysed with
t-tests and regression analysis. Of the 523 patients, 70 (13%) had TMJ effusion,
which was unilateral in 61%. Only 9% of the 70 patients had effusion bilaterally,
whereas bilateral disk displacement was found in 80%. In the 76 joints with effusion,
83% showed two specific categories of disk displacement at closed mouth. Condyle
marrow abnormalities were found in 31% of the 70 patients, mostly on one side, and
in 24% of the 76 joints. An in-patient regression analysis of the side difference in Key words: temporomandibular joint; internal
TMJ pain showed that effusion and condyle marrow abnormalities were significant derangement; joint effusion; bone marrow
pain-increasing factors. In conclusion, patients with TMJ effusion represent a edema; bone marrow necrosis; osteonecrosis.
subgroup with pain and dysfunction with more severe intra-articular pathology than
those with disk displacement but no other joint abnormalities. Accepted for publication 24 September 2000

Numerous studies have demonstrated a (TMJ) pain and dysfunction, but studies edge of why disk displacement is sometimes
high prevalence of disk displacement in have also shown that displacement may painful and is sometimes not, other intra-
patients with temporomandibular joint present without any pain6. To gain knowl- articular abnormalities should be studied.
0901-5027/01/020104+09 $35.00/0  2001 International Association of Oral and Maxillofacial Surgeons
TMJ effusion and marrow abnormalities 105

Previous magnetic resonance (MR) Table 1. Grading system for categorizing the amount of TMJ fluid on MR images
imaging studies have focused on signal Category Definition Illustration
alterations in the joint compartments No or minimal fluid No bright T2 signal from joint compartments or dots or
indicating fluid. In one of these studies lines of bright T2 signal along articular surfaces
an association with pain was found23, Moderate fluid Equal to this amount of bright T2 signal or more, but Fig. 1
whereas in another, this association was less than the amount defined as marked fluid
questioned14. Magnetic resonance signal Marked fluid Equal to this amount of bright T2 signals or more, but Fig. 2
alterations in the condyle marrow have less than the amount defined as extensive fluid fluid
also been reported, suggesting the occur- Extensive fluid Equal to this amount of bright T2 signal or more Fig. 3
rence of marrow edema and osteonecro-
sis18,20 while others have considered The aim of the present study was preted by one of the authors (P-L W).
such alterations to be caused by osteo- to study TMJ effusion in a larger The cases with a report of ‘joint fluid’
arthritis11. Recently, histological evi- consecutive series of patients with were reassessed by another author
dence for the existence of marrow edema pain and dysfunction referred for MR (TAL). In the reassessment, only
and osteonecrosis was documented9. imaging, and its association with specific patients with an amount of TMJ fluid
In a series of 62 asymptomatic
categories of disk displacement, condyle that was larger than the maximum
volunteers examined bilaterally by MR
marrow abnormalities and pain. amount found in the control subjects,
imaging, we could demonstrate that
small amounts of fluid were present in were selected for further analyses. This
more than half of the subjects, whereas series consisted of 70 patients with a
none had signal alterations in the con-
Material and methods mean age of 35.6 years (SD=14.2) and a
dyle marrow7. The observations were To recruit patients with TMJ pain and range from 11 to 81 years.
compared to those in a group of 58 dysfunction and with amounts of fluid All MR imaging studies were obtained
patients with TMJ pain and dysfunction, exceeding those seen in a control group with a 1.5 T Signa Imager (General
and about 10% proved to have an of asymptomatic volunteers7, we Electric, Milwaukee, WI) and consisted
amount of fluid that exceeded the reviewed the reports of bilateral TMJ of oblique sagittal and oblique coronal
maximum amount seen in the volun- MR imaging studies of 523 consecutive proton density and T2 weighted images
teers. A similar percentage showed patients examined from January 1995 to at closed mouth and, additionally,
signal intensity alterations in the man- May 1996. Those with previous TMJ oblique sagittal proton density and T2
dibular condyle7, supporting recent surgery, systemic inflammatory joint weighted images at open mouth15.
studies11,17. In another study comparing disease, facial growth disturbances, Both TMJs in each of the selected
different categories of disk position in direct trauma to or fractures of patients were graded for joint fluid
the same subjects, we could show that facial bones, condylar hypoplasias/ according to a set of reference films as
two specific categories of disk displace- hyperplasias/tumours and inferior image described in Table 1 and Figures 1–3.
ment were the only ones that were sig- quality had been excluded (83 from the Condyle marrow abnormalities were
nificantly more prevalent in the patients total consecutive series of 606 patients). recorded as present or absent and classi-
than in the volunteers10. All of these studies were initially inter- fied as proposed by L et al.9, and

Fig. 1. MRI of the TMJ in a 28 year-old man. (A) Sagittal oblique proton density image and (B) Corresponding T2-weighted image show
displaced disk (arrow) in lateral part of the joint (condyle not seen) and fluid in upper compartment of the anterior recess (arrow head). This was
used as reference film for the definition of moderate fluid, which was at least this amount.
106 Larheim et al.

Fig. 2. MRI of the TMJ in a 30 year-old woman. (A) Sagittal oblique proton density image of lateral part of the joint (c=condyle) and (B)
Corresponding T2-weighted image show anteriorly displaced and deformed disk (arrow) and fluid in upper compartment of the anterior recess
(arrow head). This was used as reference film for the definition of marked fluid,which was at least this amount.

Fig. 3. MRI of the TMJ in an 18 year-old woman. (A) Sagittal oblique proton density image of lateral part of the joint (c=condyle) and (B)
Corresponding T2-weighted image show anteriorly displaced and deformed disk (arrow) and fluid in upper compartment of the anterior recess
(arrow head). This was used as reference film for the definition of extensive fluid, which was at least this amount.

shown in Table 2. Cortical bone abnor- patients were asked to specify the side placements were included) and anterior
malities (erosions, osteophytes, sclerosis) and side difference if they had bilateral disk displacement at open mouth. The
indicating osteoarthritis or inflamma- pain. The degree of pain was reported as variables of the pain-free joints in
tory arthritis, were recorded as present none, mild, moderate, severe or extreme. the patient group and the joints in the
or absent. A detailed classification of Of the 70 patients, five did not have pain control group of asymptomatic volun-
disk position at closed mouth was made, records available. teers were compared using Fisher’s
modified after T et al.22, as recently In the statistical analyses all variables exact test. A regression analysis of the
described10. Additionally, disk position recorded were first dichomotized: TMJ in-patient side difference of TMJ pain
at open mouth was determined. fluid (all joints with moderate fluid or was then made with the following vari-
Pain record was obtained from the more were included), condyle marrow ables: age, sex and differences between
questionnaire, which the patient filled in abnormalities, abnormal disk position the right and left joint concerning fluid,
before MR imaging and was based on at closed mouth (all joints with com- disk displacement at closed mouth,
TMJ pain on chewing. In particular, the plete anterior or anterolateral disk dis- disk displacement at open mouth, bone
TMJ effusion and marrow abnormalities 107

Table 2. Alterations in the mandibular condyle marrow on MR images categorized according Discussion
to L et al.9
Category Definition The present investigation focused on
Normal marrow Homogeneous bright signal on proton density and homogeneous TMJ effusion and condyle marrow
intermediate signal on T2 weighted images abnormalitites in addition to disk dis-
Marrow edema Decreased signal on proton density and increased signal on T2 weighted placement, and showed that pain-free
images; edema pattern joints in the patient group had signifi-
Osteonecrosis A. Decreased signal on proton density and on T2 weighted image;s; cantly more disk displacement, fluid and
sclerosis pattern
B. Combination of edema pattern and sclerosis pattern; ‘combined’
cortical bone abnormalities, but not
pattern bone marrow abnormalities, than joints
in the asymptomatic volunteer group.
Thus, the patients seemed to have cer-
Table 3. Number of joints (n=76) with marked or extensive joint fluid (see Table 1) related to tain joint abnormalities when compared
disk position at closed mouth10 (modified after T et al.22), disk displacement at open to healthy controls. As a result of
mouth, bone marrow abnormalities (see Table 2) and cortical bone abnormalities bilateral disk displacement being so
Disk position categories at closed mouth* common in the patient group, we made a
regression analysis of the in-patient side
NL PA (lat) A PAL AL AM L Total
difference of the recorded variables that
All joints 3 4 35 4 28 1 1 76 showed a significant and positive associ-
Disk displacement at open mouth 27 22 1 1 51
ation between TMJ pain, effusion and
Bone marrow abnormalities 1 10 6 1 18
Cortical bone abnormalities 2 16 1 10 1 1 31 bone marrow abnormalities.
Since MR evidence of TMJ fluid was
*NL=disk is normally positioned in all oblique sagittal and coronal images. first recognized in 19852, several studies
PA(lat)=disk is anteriorly displaced in lateral portion of joint and otherwise normally have demonstrated the typical bright sig-
positioned. nal on T2-weighted images from the
A=disk is anteriorly displaced in entire joint without a lateral or medial displacement.
PAL=disk is anteriorly displaced in lateral portion of joint with a lateral displacement in
joint space in patients with TMJ pain
addition and otherwise normally positioned. and dysfunction14,16,19,23. However,
AL=disk is anteriorly displaced in entire joint with a lateral displacement in addition. observations in healthy volunteers have
AM=disk is anteriorly displaced in entire joint with a medial displacement in addition. been limited to only a few cases until we
L=disk is laterally displaced and otherwise normally positioned. could demonstrate in a larger series of
volunteers that dots or lines of bright
T2-signal are commonly seen and evenly
marrow abnormalities and cortical condyle, of which 20 (90.9%) had uni- distributed between upper, lower and
bone abnormalities. lateral findings. Of the 24 joints, eight both TMJ compartments7. More than
showed edema pattern (Fig. 6), eight this amount was categorized as moder-
showed sclerosis pattern (Fig. 7) and ate fluid and found in about one fifth of
Results
eight showed ‘combined’ pattern (Fig. the volunteers. When compared to find-
Seventy of the 523 patients (13.4%) had 8). Of the total of 76 joints, 18 (23.7%) ings in a patient group with pain and
TMJ effusion, i.e., either marked (Fig. 2) had condyle marrow abnormalities dysfunction, about 10% proved to have
or extensive TMJ fluid (Fig. 3), which (Table 3). an amount of TMJ fluid that was larger
was unilateral in 43 (61.4%). Of those Concerning pain-free joints, t-tests than that found in any of the volun-
with bilateral fluid, the majority had between patients and volunteers showed teers7. In the study group of 58 patients,
moderate fluid (Fig. 1) in the contra- that the patient group had significantly this constituted six patients.
lateral joint. Only six (8.6%) of the 70 more joint fluid, disk displacement at In the present study we wanted to
patients had effusion bilaterally. Of the closed mouth, disk displacement at record more patients with unquestion-
total of 76 joints (Table 3), 68.4% open mouth and cortical bone abnor- able TMJ effusion. Of the 85 patients
showed effusion exclusively or predomi- malities. No significant differences with a routine report of ‘joint fluid’, 15
nantly in the upper compartment of the could be found concerning the were excluded when the MR films were
anterolateral recess (Figs 2, 3). The condyle marrow abnormalities in these reassessed and compared to the set of
most impressive effusions also occurred comparisons. reference films. The majority of those
in other parts of the joint (Fig. 4). Regression analysis showed that the excluded had an amount of fluid that
Sixty-seven (95.7%) of the 70 patients self-reported in-patient TMJ pain side was similar to the maximum amount of
had disk displacement, which was difference was positively dependent on fluid seen in the healthy volunteers7.
bilateral in 56 patients (80%). Of the TMJ fluid (P=0.000) and condyle mar- Thus, the frequency of 13.4% virtually
total of 76 joints, 63 patients (82.9%) row abnormalities (P=0.001), and nega- represents those with TMJ effusion, i.e.
had either anterior disk displacement in tively dependent on cortical bone an increased amount of TMJ fluid when
all oblique sagittal images without any abnormalities (P=0.005) when they compared to the healthy controls.
sideways component, i.e. complete occurred simultaneously with fluid and Our figure can not be compared with
anterior disk displacement (Fig. 4) or abnormal bone marrow. The following previously reported frequencies of TMJ
complete anterior disk displacement variables did not show significance in the effusion, which have been as high as
with a lateral component, i.e. antero- regression analysis: age (P=0.311), sex 88%19, because most studies have not
lateral displacement (Fig. 5). (P=0.204), disk displacement at closed graded the amount of fluid in patients or
Twenty-two (31.4%) of the 70 patients mouth (P=0.177) and disk displacement in volunteers. A differentiation between
had bone marrow abnormalities in the at open mouth (P=0.610). normal and abnormal joint fluid has
108 Larheim et al.

Fig. 4. MRI of the TMJ in a 54 year-old man. (A) Sagittal oblique proton density image and (B) Corresponding T2-weighted image show
anteriorly displaced and deformed disk (arrow), severe osteoarthritis (c=condyle) and extensive fluid in upper compartment of the anterior recess
and in posterior recess as well (arrow heads). (C) Coronal oblique proton density image and (D) Corresponding T2-weighted image show the disk
(arrows) in anterior position to the condyle (not seen) without any lateral or medial component and extensive fluid in upper compartment of the
lateral and medial recesses (arrow heads).

only been suggested in two studies, in both spaces. Although most effusions complete anterior disk displacement or
defining no T2-signal or a line of signal were seen in the lateral part of the joint, complete anterior disk displacement
along the articular surfaces as nor- some effusions were also seen in the with a lateral component, i.e. antero-
mal14,23. With this definition, about 30% medial part. The oblique coronal images lateral displacement. This association
of patients7 and about 30% of joints in were helpful to visualize the distribution with specific subgroups of disk displace-
patients23 referred for TMJ MR imaging of fluid in the mediolateral direction. In ment at closed mouth has not previously
have shown joint effusion. the present study, all the joint effusions been stated. Our finding is in line, how-
Our detailed imaging analysis were seen in both the sagittal and coro- ever, with recent observations indicating
showed that the joint effusion was nal images. In joints with a smaller that these two categories of disk dis-
most commonly seen in the upper space amount of fluid, it could occasionally be placement are frequently seen in patients
of the anterolateral recess. This specific seen either in sagittal or in coronal but seldom in asymptomatic volun-
localization is in agreement with pre- images, substantiating a previous study teers10,22. In the present study of joints
vious reports19,23. From the present using both imaging planes23. with effusion, anterolateral disk dis-
study, however, it was clear that TMJ About 83% of the joints with effusion placements constituted almost the same
effusions may also occur in the lower or in the present series showed either number as those with pure anterior disk
TMJ effusion and marrow abnormalities 109

Fig. 5. MRI of the TMJ, same patient as in Fig. 3. (A) Coronal oblique proton density image and (B) corresponding T2-weighted image anterior
to the condyle (not seen) show laterally displaced disk (arrow) and fluid in lateral recess of the upper compartment (arrow head).

Fig. 6. MRI of the TMJ in a 33 year-old woman. (A) Sagittal oblique proton density image and (B) Corresponding T2-weighted image of the
lateral part of the joint (c=condyle) show anteriorly displaced and deformed disk (arrow) and marrow edema in the condyle.

displacement. The high occurrence of a two-thirds showed disk displacement tive series of patients referred for MR
lateral component to the anterior dis- without reduction. imaging7,11,17. Our finding of an
placement is in accordance with recent We categorized the MR signal abnor- increased prevalence of bone marrow
studies indicating that the medial malities in the bone marrow of the man- abnormalities in patients with joint effu-
component is more uncommon10,22, dibular condyle either as marrow edema, sion versus those consecutively exam-
although more equal frequencies of marrow sclerosis or a combination of the ined, is in agreement with the core
lateral and medial components to the two patterns. This is in accordance with biopsy study of the mandibular condyle
displacements have been reported5. a recent study correlating MR imaging marrow in patients surgically treated for
More importantly, we found that joints and histological findings in the condyle internal derangement9. Histological evi-
with effusion had severe, i.e. complete, marrow9. These patterns of bone mar- dence of bone marrow edema or
disk displacement, which is very seldom row abnormalities have also been used in osteonecrosis was displayed in 36% of
seen in asymptomatic volunteers. other TMJ MR imaging studies11,17. In the joints and MR imaging evidence of
Almost every disk displacement in vol- the present study almost one-third of the effusion was found in half of the joints
unteers is partial and shows a reduction patients had bone marrow abnormalities with osteonecrosis9. In the present MR
on mouth opening10,22. In the present and this figure is three to four times as imaging study of joints with effusion,
series of joints with effusion, more than frequent (8–10%) as found in consecu- almost a quarter of the joints had bone
110 Larheim et al.

Fig. 7. MRI of the TMJ in a 41 year-old woman. (A) Sagittal oblique proton density image and (B) Corresponding T2-weighted image show
anteriorly displaced and deformed disk (arrow), severe osteoarthritis (c=condyle), extensive fluid in upper compartment of the anterior recess
and around the condyle (arrow heads) and marrow sclerosis in the condyle.

Fig. 8. MRI of the TMJ in a 53 year-old woman. (A) Sagittal oblique proton density image and (B) Corresponding T2-weighted image show
anteriorly displaced disk (arrow), osteoarthritis (c=condyle), and both marrow edema (open arrow head) and marrow sclerosis (open arrow) in
the condyle.

marrow abnormalities. The association arthritis. In the total series of joints these arthritis17, substantiating the view that
between osteonecrosis and joint effusion figures were 67% and 41%, respectively. marrow edema or osteonecrosis of the
is well known from studies of the hip13. The association between bone marrow mandibular condyle may be separate
Joints with bone marrow abnormali- abnormalities and osteoarthritis sup- entities from osteoarthritis. In other
ties in our series proved to be a subgroup ports observations in the core biopsy joints such as the hip, the osteonecrotic
of severe joint conditions. More than study9, although joints with marrow process starts in the marrow and second-
91% (22 of 24 joints) showed a displaced edema or osteonecrosis occasionally arily, after weakening of the subarticular
disk that did not reduce on mouth open- showed normal cortical bone. A recent bone with collapse and fracture, osteo-
ing and more than 95% (23 of 24 joints) MR imaging study has also demon- arthritis develops21.
showed cortical bone abnormalities indi- strated that bone marrow abnormalities Our observation of large amounts of
cating osteoarthritis or inflammatory may occur in the absence of osteo- TMJ fluid and evident bone marrow
TMJ effusion and marrow abnormalities 111

abnormalities in the mandibular condyle that TMJ effusion occurred less fre- dence of temporomandibular joint fluid
are in agreement with the growing evi- quently in joints with osteoarthritis than and condyle marrow alterations: occur-
dence that inflammatory reactions may in joints with disk displacement but rence in asymptomatic volunteers and
take place in patients with TMJ pain and without osteoarthritis. In our regression symptomatic patients. Int J Oral Maxillo-
dysfunction, but with no generalized analysis, osteoarthritis proved to be a fac Surg 2001: 30: 113–117.
inflammatory joint diseases, as demon- pain-decreasing factor when occurring 8. L TA, S H-J, A F.
Rheumatic disease of temporomandibu-
strated at arthroscopy and in surgical simultaneously with fluid and bone
lar joint with development of anterior
specimens1,3,4,12,24. Histological obser- marrrow abnormalities, which proved to
disk displacement as revealed by mag-
vations have even suggested that inflam- be pain-increasing factors. This is well in netic resonance imaging: a case report.
matory changes in patients with known accordance with our clinical experience Oral Surg Oral Med Oral Pathol 1991:
inflammatory arthritidis and internal and the general view that patients even 71: 246–249.
derangement without such arthritidis with severe osteoarthritis, may be pain- 9. L TA, W P-L, H
can be quite similar1. One patient in the free. DG, E L, B D. Osteo-
present series had a follow-up MR imag- In conclusion, the patients with TMJ necrosis of the temporomandibular joint:
ing study, suggesting an evident altera- effusion, i.e. an amount of fluid that Correlation of magnetic resonance imag-
tion in the amount of fluid within a exceeded the maximum amount seen in a ing and histology. J Oral Maxillofac Surg
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in some TMJs with internal derange- teers, seem to represent a subgroup with 10. L TA, W P-L, S T.
ment may possibly resemble the fluctu- pain and dysfunction with more severe Temporomandibular joint disk displace-
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been demonstrated by a longitudinal with disk displacement but no other volunteers and patients. Radiology 2001
MR imaging study of a patient with abnormalities. (in press).
psoriatic TMJ arthritis8. In fact, both 11. L JM, G CL, M
AO, S RD. Prevalence of bone
that patient and the patient in the
Acknowledgments. This study has been marrow signal abnormalities observed in
present study had pain records that the temporomandibular joint using mag-
followed the variation in joint effusion. supported by The Research Council of
Norway. We thank Dr Marek Rösler netic resonance imaging. J Oral Maxillo-
Almost every patient in the present fac Surg 1996: 54: 434–439.
for the statistical analyses and Hakon
series showed disk displacement and the 12. M RG, Y WY, L M. A
Störmer for the photographic work with
displacement was frequently bilateral. histologic evaluation of the accuracy
the illustrations.
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O MR, L LB. MR of 109: 249–262. Department of Maxillofacial Radiology
osteochondritis dissecans and avascular 23. W P-L, B SL. Tem- Faculty of Dentistry
necrosis of the mandibular condyle. poromandibular joint: relationship University of Oslo
AJNR 1989: 10: 3–12. between MR evidence of effusion and PO Box 1109, Blindern
21. S DE, M JE. Pathogenesis the presence of pain and disk displace- 0317 Oslo
of osteonecrosis. In: Resnick D, ment. Am J Roentgenol 1992: 159: 559– Norway
Niwayama G, eds: Diagnosis of bone and 563. Tel: +4722852016/+4722852234
joint disorders. Philadelphia, PA: 24. W CH. Internal derangements of the Fax: +4722852347
Saunders 1988: 3188. temporomandibular joint: pathological E-mail: larheim@odont.uio.no

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