ORAL AND MAXllLOFAClAL SURGERY Editor: Larry J.

Petersott

Histopathologic changesof the temporomandibular joint disk in

patients with chronic arthritic disease
A comparison with internal derangement

Tore Bj#rnland, DDS,” and Sigvald B. Refsum, MD,b Oslo, Norway

UNIVERSITY OF OSLO

Histopathologic examination was performed of the disk and the posterior attachment extirpated from 17
temporomandibular joints from 15 patients with chronic arthritic disease. Seven patients had rheumatoid arthritis (including two
with juvenile type), five had ankylosing spondylitis, and three had psoriatic arthropathy, which affected more joints than the
temporomandibular joint. Specimens removed from 16 temporomandibular joints from 15 patients with internal derangement
were used for histopathologic comparison. In both groups of patients, inflammatory changes were observed, but no specific
histopathologic signs could distinguish the groups. Patients with chronic arthritic disease seemed to have more pronounced
changes of vascular proliferation, perivascular cellular infiltrate, inflammatory cells, and fibrosis throughout the soft tissues.
Destruction of the disk was another finding evident in patients with chronic arthritic temporomandibular joint disease; there was
no visible disk structure in 8 of these 17 joints, compared with 1 of the 16 joints in the internal derangement group. (ORAL SURC
ORAL MD ORAL PATHOL 1994;77~572-8)

Surgical treatment of the temporomandibular joint
(TMJ) with synovectomies and diskectomies in a se-
ries of patients with chronic arthritic disease has re-
cently been published.’ The differential diagnosis be-
tween chronic arthritic disease and internal derange-
ment in the TMJ may be difficult even with
arthrotomography or magnetic resonance imaging.2$ 3
Furthermore, patients who have been given a general
diagnosis of chronic arthritic disease and who have
TMJ symptoms may have internal derangement as
the only abnormality observed at TMJ imaging3 and
TMJ surgery. 1
Histopathologic appearance of joint structures af-
fected by the rheumatoid process has been described
as infiltration with numerous inflammatory cells, hy-
perthrophic or hyperplastic synovial cells, vascular
changes with perivascular lymphocyte accumulation,
and cellular infiltrate and fibrosis.“6 There might be
a considerable variation within a single joint.4, 5 His-
aAssistant Professor, Department of Oral Surgery
icine, Faculty of Dentistry.
bAssistant Professor, Institute of Pathology,
Copyright @ 1994 by Mosby-Year Book. Inc.
0030-4220/94/$3.00+ 0 7/12/55019
572
topathologic examination may not separate the dif-
ferent arthropathies.5 To our knowledge, histopatho-
logic changes of the TMJ disk in patients with chronic
arthritic disease have only been described in an
autopsy study7 and a case report.8 However, the his-
topathologic changes of the TMJ disk in patients sur-
gically treated for internal derangement have been
described in detail.9-‘3
The aim of the present study was to evaluate the
histopathologic findings of the TMJ disk and posterior
attachment in joints affected by chronic arthritic dis-
ease and to compare these with the histopathic find-
ings in internal TMJ derangement. The histopatho-
logic changes present in internal derangement were
used as a baseline for changes that appeared only in
chronic arthritic TMJs.
MATERIAL. AND METHUDS
The material consisted of 17 specimens obtained at
synovectomies and diskectomies of the TMJ from 15
patients with chronic arthritic disease and arthritic
and Oral Med- TMJ disease (arthritis group) observed at surgery.’
Rikshospitalet.
Two specimens were obtained from one patient with
bilateral TMJ surgery and two specimens from one
patient with a reoperation in one TMJ.
ORAL SURGERY ORAL MEDICINE ORAL PATHOLOGY Bj@land and Refsum 573
Volume 77, Number 6

The specimens consisted of articular disk, the pos- Table I. Histopathologic observations with grading
terior attachment, or both. In this present study the of the findings 0 to 3,* expressed in arithmetic
material was collected from 13 women and 2 men with means of the 8 disks found in the arthritis group
an age range of 17 to 65 years (mean, 38.8 years). The and the 15 disks found in the derangement group.
initial diagnosis of chronic arthritic disease had been Mann-Whitney nonparametric test used for group
made by rheumatologists on the basis of clinical, ra- comparison ( f SD).
diologic, and serologic examinations in these 15 Arthritis Derangement
patients: two had juvenile rheumatoid arthritis,14 five Findings group group p-value
had classical or definite rheumatoid arthritis,15 five
had ankylosing spondylitis,16 and three had psoriatic Fissureformation 2.25 (2 0.70) 1.73 (k 0.96) NS

arthropathy. l7 All patients had arthritic involvement Edema 1.5 (+ 0.75) 1.06 (20.59) NS
Vessels 1.37 (57 0.51) 0.73 (* 0.59) 0.022
of more than one joint in addition to the TMJ; the Synovialcovering 0.87 (+ 0.64) 0.66 (k 0.48) NS
duration of the general disease ranged from 1 to 30 Fibrosis 0.12 (i: 0.35) 0.2 (+ 0.41) NS
years (mean, 11.6 years). The duration of TMJ Inflammatory cells 0 0 NS
symptoms varied from 1 to 12 years (mean, 4.1 years). NS, not significant.
The criteria for surgery, surgical technique, and the *0 = no histopathologic changes
I = minimal changes
surgical observations were previously reported.’ 2 = moderate changes
Sixteen specimens removed from 15 patients surgi- 3 = pronounced changes
cally treated for internal TMJ derangement (de-
rangement group) were used as a control material for
comparison. These patients had no history of gener- performed by one of us (S.B.R.) in random order with
alized joint disease, and the clinical examination and no knowledge of the preoperative diagnosis or the
routine blood tests indicated no chronic arthritic dis- surgical observations. Observations were made of
ease. They were randomly selected from among recognizable tissue in the specimens: disk, posterior
patients treated by the same surgeon (T.B.) within the attachment, or both and the histopathologic changes.
same time interval (1986 to 1991). Two specimens A scoring system of 0 to 3 were used, with 0 indicat-
were obtained from one patient with bilateral surgery. ing no histopathologic changes, 1 = minimal changes,
This group of patients comprised 14 women and 1 2 = moderate changes, 3 = pronounced changes, for
man with an age range from 21 to 61 years (mean, each of the parameters and applied to all parts of the
36.6 years). The indications for diskectomies were disk and retrodiskal tissue.
pain and reduced mandibular motion not alleviated by
previous therapy. Symptoms from the TMJs had a STATISTICAL METHODS
duration of 2 to 20 years (mean, 7.8 years) in this The results are expressed in arithmetic means and
group. standard deviations (SD) and between group com-
Five additional specimens were also obtained from parison was made with Mann-Whitney nonparamet-
five patients (women aged 32 to 48 years, mean, 40 ric test.
years) with a general diagnosis of rheumatoid arthri-
tis (two patients), ankylosing spondylitis (two pa- RESULTS
tients), and psoriatic arthropathy (one patient). How- At surgery, displacement of the disk was seen in 4
ever, surgical observations had previously character- of the chronic arthritic TMJs. At the microscopic ex-
ized these TMJs as nonarthritic, that is, internal amination, disk tissue was found in 8 of 17 specimens
derangement with disk displacement and fibrous ad- in the arthritis group (no disk was found in the re-
hesions.’ The findings in these patients are not in- operated joint) and in 15 of 16 specimens in the de-
cluded in the tables. rangement group. The amount of disk tissue was also
Care was taken to remove all the articular soft tis- reduced in the arthritis group compared with the de-
sue, and the diskectomies were done by incision rangement group. The posterior attachment was
through the retrodiskal tissue and the lateral, medial, found in all the chronic arthritic TMJs and in all but
and anterior part of the disk close to the attachments. one in the derangement group.
The specimens were fixed in 10% buffered formalde- The histopathologic findings of the disks are sum-
hyde-solution, embedded in paraplast, and sectioned marized in Table I. There was a significant increase
at 4 pm for microscopic analysis. The specimens were of the vessel proliferation in the disks in the arthritis
stained with hematoxylin, saffron, and eosin (Masson group. Furthermore, fibrillation and fissure formation
trichrome), (Fig. 1) were sometimes embracing nearly all the disk,
The histologic examination of all the specimens was leaving only a small rim of remaining disk tissue. The
---
574 Bjdrnland and Refsum ORAL SURGERY ORAL MEDICINE ORAL PATHOLOGY
June 1994

Table Ill. Grading of vascular changes of the 17

posterior attachments from the arthritis group and
15 posterior attachments observed in the
derangement group. (For further information of
histopathologic grading, see Table I.)
__-.. .-.. ~~~.~..T~~~--..-...~----
/ Arthritis Derangement
Finding.5 group group p-value

Perivascular fibrosis 1.82 (kO.63) 1.5 (kO.96) NS

Vascular proliferation 1.76 ( k 0.66) 1.25 ( c 0.77) 0.046
Vascular wall fibrosis 0.94 (t0.55) 0.93 (20.85) NS
Perivascular cellular 0.88 (+ 1.05) 0.12 (t0.34) 0.011
infiltrate
Obliteration 0.76 (r0.66) 0.81 (k0.75) NS
Vascular wall 0.17 (~~0.39) 0.06 (~~0.25) NS
infiltrate
-____--. ---__- __-_
NS, not significant.
Fig. 1. Disk tissue with cartilagenous changes, degener-
ated nuclei with atypia, and fissure formation and fibrillar
destruction of the matrix in a patient with ankylosing
Table IV. Grading of histopathologicobservations of
spondylitis. (Masson tricrome stain; original magnification
x350.1
the synovial membrane in 17 specimens in the
arthritis group and 14 specimens in the
derangement group where synovial cells were
found. (For further information of histopathologic
Table II. Grading of the histopathologic observations
grading, see Table I.)
of the 17 posterior attachments in the arthritis ______--
group and the 15 posterior attachments observed in Arthritis Derangement
Findings group / group p-value
the derangement group. (For further information
of histopathologic grading, see Table I.) Bone fragments 1.35 (t 1.41) 0.5 (kO.65) NS
Fibrinoid deposits 0.76 (k1.09) 0.21 (kO.42) NS
Arthritis Derangement
Synovial inflammation 0.29 (kO.68) 0.06 (k0.25) NS
Finding group grow p-value
NS, not significant.
Fissure formation I .76 ( f 0.83) 1.8(kO.77) NS
Synovial covering 1.41 (kO.87) 1.31 (-r-0.79) NS
Edema 1.05 (rt0.55) 1.33 (kO.48) NS
Fat cells 0.88 (k0.85) 0.37 (kO.71) NS in the arthritis group and one of the attachments in
Inflammatory cells 0.82 (k 0.95) 0.06 (kO.25) 0.005 the derangement group.
Fibrosis 0.41 (* 0.79) 0 0.049
The vascular changes of the posterior attachment
Glandular tissue 0.41 (+0.93) 0.12 (kO.71) NS
-______ are summarized in Table III. Vascular proliferation
NS, not significant. was seen in all the specimens in the arthritis group and
in 14 of the specimens in the derangement group,
whereas the perivascular cellular infiltrate was seen in
disk could sometimes be submitted to a fibrillar de- nine and two specimens in the arthritis and derange-
generation with a more or less complete disappear- ment group, respectively. The ingrowth of capillaries
ance of the double refractile collagen fibers. There and fibroblasts could be seen on the surface as a pan-
was a concommitant cartilagenous change in the cells, nus sometimes covered by synovial cells or as an in-
sometimes with nuclear atypia or lack of nuclei at the growth to the disk. Pannus formation was seen in both
surface as well. These changes seemed to start at the groups of patients but usually without inflammatory
surface of the disk. cells in the derangement group. In the arthritis group
The examination of the posterior attachment (Ta- the perivascular cell infiltrate consisted mostly of
ble II) showed the same fissure formation with edema lymphocytes and histiocytes; a few also had a cellular
and fibrillation as in the disk but without any chon- infiltrate in the vessel wall itself (Fig. 2, A). There
droid tissue transformation. Fibrosis was only seen in could also be a variable perivascular fibrosis thus pro-
the arthritis group, and together with inflammatory voking an obliteration of the lumina in some areas,
cells was significantly pronounced. Glandular tissue both in the arthritis group (Fig. 2, B) and in the de-
from the parotid gland was seen in three attachments rangement group (Fig. 2, C’).
ORAL SURGERY ORAL MEDICINE ORAL PATHOLOGY BjBrnland and Refsum 575
Volume 77, Number 6

Fig. 2. A, Specimen collected from patient with juvenile rheumatoid arthritis. Small vesselwith heavy lym-
phocyte infiltration in the vesselwall (posterior attachment). (Masson tricrome stain; original magnification
x350.) B, Remains of fibrous and obliterated small vesselsin posterior attachment in patient with rheuma-
toid arthritis. (Masson tricrome stain; original magnification x350.) C, Specimen collected from patient with
internal derangement. Fibrous and obliterated vesselwith surrounding vasculitis in the posterior attachment.
(Masson tricrome stain; original magnification x350.)

Synovial cells were seen in all extirpated specimens,
except in two from the internal derangement group
(Table IV). Synovial hyperplasia was found on one
extirpated disk in each group, whereas synovial
hyperplasia on the posterior attachment was found in
six specimens in both the arthritis group (Fig. 3, A)
and the derangement group. Bone fragments in the
synovial membrane and stroma were seen in nine of
the attachments in the arthritis group (Fig. 3, B) and
in three of the attachments in the derangement group.
Histopathologic examination of the five specimens
from patients with a general diagnosis of chronic ar-
thritic disease but with surgical observation of only
internal derangement in the TMJs had all recogniz-
able disks and posterior bands and thus resembled the
control group. There was, however, vessel prolifera-
tion into the disk and increased perivascular infiltrate
as seen in the arthritis group. In two specimens syn-
ovial inflammation grade 1 was seen. All the other
observations were as characterized for the derange-
ment group.
DISCUSSION
Our group of 15 patients with chronic arthritic dis-
ease and the control group of 15 patients with inter-
nal derangement of the TMJs were comparable with
respect to age and sex distribution. TMJ symptoms in
the arthritis group were of shorter duration than in the
derangement group. This might have indicated less
severe changes in the arthritis group, but the histo-
--_
576 Bjghzland and Refsum
Fig. 3. Synovial changes in patient with rheumatoid ar-
thritis. (Masson tricrome stain; original magnification
X350.). A, Hyperplastic synovial cell layer with a prominent
infiltration of macrophages in the underlying stroma. B,
Necrotic bone fragments in the synovial stroma.
pathologic changes in general were more enhanced in
this group.
Histopathologic classification of the disk and the
posterior attachment may contain underregistration
of tissue present in the TMJs, because the extirpated
material did not always represent the true picture of
a joint. The pathologic process may destroy or trans-
form the soft tissue in the joint, and we may get a
general vascularization of the disk tissue with disap-
pearance of the normal fibrocartilagenous tissue. Un-
less we could recognize any fibrocartilagenous tissue,
we could not distinguish such a vascularized connec-
tive tissue apart from the posterior attachment. The
different tissue identifications were based on these as-
sumptions, and with these reservations in mind we can
discuss the different changes found.
The absence of the disk in eight chronic arthritic
TMJs was in accordance with the surgical observa-
ORAL SURGERY ORAL MEDICINE ORAL PATHOLOGY
,Iune 1994
tions previously described.’ Macroscopic evaluation
underestimated the loss of disk structure. This can be
due to adaptive changes of the posterior disk attach-
ment,” thus making a macroscopic identification be-
tween the disk and the posterior attachment difficult.
In an imaging study,3 replacement of the disk by- an-
other fibrous tissue was indicated by magnetic reso-
nance, but differentiation between disk and attach-
ment may still be difficult. The loss of disk structure
and the fact that more of the specimens in the arthri-
tis group had only small disk remnants remaining has
to our knowledge not been verified histopathologically
in this group of patients, except for patients with fi-
brous or bony ankylosis.‘. I8 Using arthroscopic in-
terventions of the TMJ Sanders and Buoncristianii9
found disk destruction in 2 of 1 1 patients with rheu-
matoid arthritis.
Almost all changes concerning the disks were more
pronounced in the arthritis group. Degeneration of
the intercellular matrix from the surface of the disk
may be a result of liberation of lysosomal and prote-
olytic enzymes as part of an inflammatory process
caused by altered biomechanical properties or a
reduced nutrition of essential metabolites.20 As the
pathologic process seemed to signify ischemic or met-
abolic changes, the fissure formation illustrated in
Fig. 1 and the disk perforation may be due to de-
creased blood flow. In early stages of an inflammatory
joint disease, blood flow usually increases, but in later
stages the most affected joints often have the least
blood flo~.~ A diffusion failure may be due to a vas-
cular insufficiency, partly because of the enhanced
perivascular inflammatory changes and vessel wall
reaction found in our arthritis group. A mechanical
tear may result in fissure formation in internal TMJ
derangements,” but this is less probable in the
arthritis group because the disk when present was
normally positioned in the majority of chronic ar-
thritic TMJs.‘. ’ The vascular proliferation found
both in the disk and the posterior attachment might
be an initial reparative phenomenon caused by is-
chemic changes in these structures. Four of the disks
in the chronic arthritic TMJs were displaced, and this
may have influenced the pathologic process because
degenerative changes may occur both in TMJs with
or without disk displacementZO In one of the patients
in the derangement group, no disk tissue was seen in
the specimen but there were findings of synovial
inflammation, cellular infiltrate into the vessel walls,
and inflammatory cells in the posterior band. This
might be a patient with a monoarticular arthritis. Fi-
brosis and inflammation in the posterior attachment
as a diffuse cellular reaction were statistically pro-
nounced in the arthritis group. The other changes
were not significant and were as expected. This agrees
ORAL SURGERY ORAL MEDICINE ORAL PATHOLOGY
Volume 77, Number 6
with the report of Yates and Scott22 in their exami-
nation of rheumatoid arthritis in the knee; fibrotic
histology was seen when the disease had been active
for more than 18 months. Normally no glandular tis-
sue is present in the TMJ, but fibrosis and shrinkage
of the posterior attachment may pull the glandular
tissue forward to be removed at surgery.
Vascular proliferation and perivascular cellular in-
filtrate in the posterior attachment were significant
findings in the arthritis group. These findings are
usually present in immune-mediated chronic inflam-
matory joint disease. The T lymphocyte is one of the
most common cells in chronic arthritic diseases, and
the activation of T lymphocytes sets up a cascade of
nonspecific inflammatory reactions.6 Our findings of
unspecific vascular changes such as thickening of the
wall and obliteration in the derangement group are in
agreement with other reports.“, 13,23,24 Stegenga et
a1.25 explained diminished blood flow in the TMJ as
a result of negative pressure in the upper joint space
thus creating increased joint debris and subsequent
osteoarthosis caused by muscular hyperactivity. In
our study, however, this theory cannot explain both
the hard and soft tissue alteration seen in the arthritis
group. 1, 3 Destruction of the hard and soft tissue may
take place by diminished blood flow caused by the in-
flammatory reaction in and around the vessels or by
the T lymphocyte activation and cytokine liberation.6
This may also explain the high number of totally de-
stroyed disks and small amounts of disk tissue seen in
the specimens from the arthritis group. Proliferation
of capillaries and fibroblasts as a pannus formation
both in the arthritis joints and derangement joints
may indicate that pannus formation is an attempt to
repair the degenerated disk and posterior attachment.
The mechanism behind the inflammatory reaction
seen both in the arthritis group and derangement
group is unclear, and it remains questionable whether
the inflammation is a cause or a sign of the disease in
these compromised joints subject to continuous phys-
iologic loads.
Our findings of synovial hyperplasia but no villous
changes are in agreement with an arthroscopic study
by Holmlund et a1.24 in which synovial hyperplasia
was found in 4 of 21 patients with rheumatoid arthri-
tis. This is in contrast to another arthroscopic study26
in which 11 of 67 TMJs were reported to have synovial
villi and chronic arthritic disease in other joints.5,22
This may be explained by the fact that our specimens
only contained synovial covering on the disk and pos-
terior attachment and not the synovial membrane in
other parts of the joint. Another explanation may be
that most of our cases were advanced with chronic
arthritic involvement of the TMJ over a long period
of time, and therefore no exudative synovitis is
Bjqknland and Refsum 577
expected.22 The finding of no significant difference of
fibrosis or inflammation in the synovial membrane
between the two groups of patients agrees with a
study27 of synovial membrane histology in the knee in
which intensity of inflammation and fibrosis could be
similar in rheumatic arthritis and osteoarthritis de-
pending on the medication received by the patients.
Fibrinoid deposits were more pronounced in the
arthritis group as were bone fragments found in the
synovial membrane. Bone fragments as a frequent
finding in the synovial membrane in chronic arthritic
TMJs has to our knowledge not been described ear-
lier. Also the fact that this finding was present in pa-
tients with juvenile rheumatoid arthritis, rheumatoid
arthritis, psoriatic arthropathy, in addition to anky-
losing spondylitis where bone fragments were most
pronounced may explain the possibility of develop-
ment of bony TMJ ankylosis in the different arthrit-
ides. The findings of bone fragments indicated that
the hard tissues were also involved in the disease pro-
cess. Our finding of bone fragments in the synovial
membrane is not in agreement with the statement of
Bywaters and Edmonds4 that claimed bone fragments
were present in the synovial membrane until some
months after onset of the rheumatic disease.
In the five specimens from five patients with a gen-
eral diagnosis of chronic arthritic disease without
surgical findings of arthritic TMJs, the preoperative
imaging in two of them disagreed3 with observations
of irregularly outlined contrast medium that indi-
cated synovial proliferation. One question that arises
is whether an internal derangement with synovial in-
flammation is an incidental finding in patients with
chronic arthritic disease or if internal derangement
may develop in patients with chronic arthritic TMJ
disease as described by Larheim et a1.28Because some
of the cases of chronic arthritic TMJs also had inter-
nal derangement, inflammation in the disk and poste-
rior attachment may be related to the different stages
of internal derangement. 29 There might also be a
considerable variation of synovitis within a single
joint, 4, ‘3 3o and this may also be an explanation for
disagreement between preoperative imaging and the
surgical versus the histopathologic findings.
In conclusion, the present study demonstrated pro-
nounced differences between the two groups with re-
spect to the vascular proliferation, perivascular cellu-
lar infiltrate, fibrosis, and inflammatory cells in the
posterior band. Vessel proliferation in the disk and
destruction of the disk is another evident finding in
chronic arthritic TMJ disease. Even if the inflamma-
tory reaction was more pronounced in cases of chronic
arthritic TMJs, no specific histopathologic changes
separated patients with chronic arthritic TMJ disease
from patients with internal derangement. Surpris-
578 Bj&xland and Refsum ORAL SURGERY ORAL MEDICINE ORAL PATHOLOGY
June I994

ingly, the differences between the two groups were less mally positioned disks and patients with internal derangement.
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