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7/17/2019 Clinical Significance of Changes in the Bone.pdf http://slidepdf.com/reader/full/clinical-significance-of-changes-in-the-bonepdf 1/14 Clinical Significance of Changes in the Bone Marrow and Intra-Articular Soft Tissues of the Temporomandibular Joint Tore Arne Larheim, Tsukasa Sano, and Yoritaka Yotsui Patients with facial pain and jaw function problems constitute a large and heterogeneous group. Disk displacement and osteoarthritis are the most com- mon intra-articular abnormalities observed at imaging. As disk displacement is seen rather frequently in asymptomatic volunteers, it is a challenge to explain why disk displacement sometimes is symptomatic and sometimes is not. The present review focuses on abnormalities in the condylar bone marrow and the intra-articular soft tissues accompanying the disk displacement. The findings of temporomandibular joint in asymptomatic volunteers and in temporomandib- ular disorder (TMD) patients are reviewed. Both bone marrow edema and marrow necrosis are documented at histology and at magnetic resonance imaging (MRI) in TMD patients. Intra-articular soft tissue changes, such as synovitis, are additionally documented at arthroscopy. However, there is a controversy concerning which diagnostic imaging information is essential. Although there is no doubt that disk displacement and osteoarthritis may be accompanied by inflammatory alterations in the bone marrow and the intra- articular soft tissues, it has been difficult to consistently relate a specific imag- ing manifestation (bone edema, joint effusion, and synovitis) to joint pain. Longitudinal studies are needed to evaluate the importance of MRI abnormal- ities in the management of TMD patients. (Semin Orthod 2012;18:30-43.) Crown Copyright  ©  2012 Published by Elsevier Inc. All rights reserved. atients with facial pain and jaw function problems constitute a large and heteroge- neous group with the umbrella diagnosis tem- poromandibular disorder (TMD). 1,2 There is consensus that myofascial pain disorder of the masticatory muscle system is the most common of all TMDs. Disk derangement disorders and osteoarthritis are the most common intra-articu- lar disorders. Rheumatoid arthritis is less com- mon, but is the most frequent of the arthritides that may involve the temporomandibular joint (TMJ). In this article, we will focus on disk de- rangement disorders and osteoarthritis. In patients with pain and impaired jaw func- tion referred for diagnostic magnetic resonance imaging (MRI), disk displacement with or with- out osteoarthritis is the most common intra-ar- ticular abnormality observed. However, disk dis- placement is seen rather frequently also in asymptomatic volunteers. Therefore, it has been and still is a challenge to explain why disk dis- placement sometimes is symptomatic and some- times is not. A number of joint abnormalities accompanying disk displacement have been in-  vestigated. Knowledge of TMJ findings in asymptomatic  volunteers is mandatory to rule out joint mani- festations that may be responsible for patient  Department of Maxillofacial Radiology, Faculty of Dentistry, Institute of Clinical Dentistry, University of Oslo, Oslo, Norway;  Department of Oral and Maxillofacial Radiology, Tokyo Dental College, Mihama-ku, Chiba, Japan; Department of Oral Radiology, Osaka Dental University, Chuo-ku, Osaka, Japan. Address correspondence to Tore Arne Larheim, DDS, PhD, De-  partment of Maxillofacial Radiology, Institute of Clinical Dentistry,  Faculty of Dentistry, University of Oslo, PO Box 1109, Blindern 0317, Oslo, Norway. E-mail: [email protected] Crown Copyright © 2012 Published by Elsevier Inc. All rights reserved. 1073-8746/12/1801-0$30.00/0 doi:10.1053/j.sodo.2011.10.006 30  Seminars in Orthodontics, Vol 18, No 1 (March), 2012: pp 30-43 

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Clinical Significance of Changes in the BoneMarrow and Intra-Articular Soft Tissues of theTemporomandibular Joint

Tore Arne Larheim, Tsukasa Sano, and Yoritaka Yotsui 

Patients with facial pain and jaw function problems constitute a large andheterogeneous group. Disk displacement and osteoarthritis are the most com-mon intra-articular abnormalities observed at imaging. As disk displacement isseen rather frequently in asymptomatic volunteers, it is a challenge to explainwhy disk displacement sometimes is symptomatic and sometimes is not. Thepresent review focuses on abnormalities in the condylar bone marrow and theintra-articular soft tissues accompanying the disk displacement. The findings oftemporomandibular joint in asymptomatic volunteers and in temporomandib-

ular disorder (TMD) patients are reviewed. Both bone marrow edema andmarrow necrosis are documented at histology and at magnetic resonance

imaging (MRI) in TMD patients. Intra-articular soft tissue changes, such assynovitis, are additionally documented at arthroscopy. However, there is acontroversy concerning which diagnostic imaging information is essential.Although there is no doubt that disk displacement and osteoarthritis may beaccompanied by inflammatory alterations in the bone marrow and the intra-articular soft tissues, it has been difficult to consistently relate a specific imag-ing manifestation (bone edema, joint effusion, and synovitis) to joint pain.

Longitudinal studies are needed to evaluate the importance of MRI abnormal-ities in the management of TMD patients. (Semin Orthod 2012;18:30-43.) Crown 

Copyright  ©  2012 Published by Elsevier Inc. All rights reserved.

P atients with facial pain and jaw functionproblems constitute a large and heteroge-

neous group with the umbrella diagnosis tem-poromandibular disorder (TMD).1,2 There isconsensus that myofascial pain disorder of themasticatory muscle system is the most commonof all TMDs. Disk derangement disorders andosteoarthritis are the most common intra-articu-

lar disorders. Rheumatoid arthritis is less com-mon, but is the most frequent of the arthritidesthat may involve the temporomandibular joint (TMJ). In this article, we will focus on disk de-rangement disorders and osteoarthritis.

In patients with pain and impaired jaw func-tion referred for diagnostic magnetic resonanceimaging (MRI), disk displacement with or with-out osteoarthritis is the most common intra-ar-ticular abnormality observed. However, disk dis-placement is seen rather frequently also inasymptomatic volunteers. Therefore, it has beenand still is a challenge to explain why disk dis-placement sometimes is symptomatic and some-times is not. A number of joint abnormalitiesaccompanying disk displacement have been in- vestigated.

Knowledge of TMJ findings in asymptomatic volunteers is mandatory to rule out joint mani-festations that may be responsible for patient 

 Department of Maxillofacial Radiology, Faculty of Dentistry,

Institute of Clinical Dentistry, University of Oslo, Oslo, Norway;  Department of Oral and Maxillofacial Radiology, Tokyo Dental College, Mihama-ku, Chiba, Japan; Department of Oral Radiology,Osaka Dental University, Chuo-ku, Osaka, Japan.

Address correspondence to Tore Arne Larheim, DDS, PhD, De-  partment of Maxillofacial Radiology, Institute of Clinical Dentistry, Faculty of Dentistry, University of Oslo, PO Box 1109, Blindern 0317, Oslo, Norway. E-mail:  [email protected] 

Crown Copyright © 2012 Published by Elsevier Inc. All rights reserved.

1073-8746/12/1801-0$30.00/0 doi:10.1053/j.sodo.2011.10.006 

30   Seminars in Orthodontics, Vol 18, No 1 (March), 2012: pp 30-43 

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symptomatology. Therefore, TMJ findings inhealthy individuals will be reviewed first. Then, joint abnormalities reported as possible causesof facial pain in TMD patients will be discussed.

TMJ Findings in Asymptomatic HealthyVolunteers

 Disk position and function  in asymptomatic volun-teers has been thoroughly investigated. Larheimet al3 found disk displacement in about one-third of the volunteers, significantly less fre-quently than in the patients referred for MRI,and this is in accordance with a number of ear-lier studies.4-6 This study also showed that diskdisplacement in the volunteers was predomi-nantly unilateral, in contrast with the bilateral

displacement that was frequently seen in the

patients.3 Further, the disk displacement wasfound to be less severe in the volunteers; the disk was commonly (90%) displaced in one portionof the joint and normally located in another(Fig. 1). In joints with such partial disk displace-

ment, the displacement was mostly found in thelateral part of the joint, supporting an investiga-tion on the variability of disk position f rom thelateral to the medial portion of the joint.7 Partialdisk displacement   has previously been con-firmed by surgery,8 and has also been observedin autopsy studies.6,9,10 Most interestingly, par-tial disk displacement occurred with similar fre-quency percentages (about 22%) in the volun-teers and the patients. In both groups, the vast majority showed reducing disk displacement.3  A higher frequency of part ial disk displacement 

has also been observed.

7

 Almost all displaced

Figure 1.   Partial disk displacement. MRI (A, B, C) of TMJ in asymptomatic volunteer and autopsy specimen of TMJ (D, E). (A) Lateral image. (B) Centromedial image. Anterior disk displacement in lateral part and normaldisk position in centromedial part of the joint with closed mouth. (C) Open mouth image. Normal disk positionand normal bone. ([A-C] Reprinted with permission from Larheim et al, 3 © Radiological Society of North

 America.) (D) Lateral section. (E) Medial section. Anterior disk displacement in lateral part  and normal diskposition in medial part of the joint. ([D-E] Reprinted with permission from Larheim et al,21 © S. Karger AG,Basel, Switzerland.) (Color version of figure is available online.)

31Changes in the Bone Marrow and Soft Tissues of TMJ 

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disks in asymptomatic volunteers reported in theliterature have been found to normalize onmouth opening.3-6

Complete disk displacement, that is, disk dis-placement in all sections throughout the joint,

occurred very seldom in the volunteers, but ratheroften in the patients.3 Almost all joints with nonre-ducing disk displacement belonged to this sub-group.

Retrodiskal tissues   (posterior disk attachment,bilaminar zone) in asymptomatic volunteershave a brighter signal than the disk that is uni-formly dark, with no increased signal intensity on T1- or   T2-weighted magnetic resonance(MR) images.11

Contrast enhancement  of intra-articular soft tis-sues on T1-weighted MR images after i.v. injec-

tion of contrast medium in asymptomatic volun-teers is very slight or is not seen. This was first demonstrated by Smith et al12 and later con-firmed by others.13,14

 Joint fluid , dots or lines of bright T2 signalalong articular surfaces,15  was demonstrated  inmore than half of 62 asymptomatic volunteers.16

In about one-fifth, even more fluid was ob-served, consistently related to disk displacement in that portion of the joint (Fig. 2).

Cortical bone  alterations have been reportedto occur in 0 to 3% of TMJs in asymptomatic volunteers.6,17,18 The osseous changes have

consisted of condylar flattening and small os-teophyte formation found unilaterally,  but oth-erwise with smooth cortical outline.18 Minimalflattening of the condyle and/or the articulareminence has been found in  about one-third of 

asymptomatic volunteers.17

Such an osseouschange should generally not be interpreted asosteoarthritis because the bony changes most likely represent remodeling, that is, a functionaladaptation of the joint with an intact surfacelayer.

Bone marrow   of the mandibular condyle hasbeen reported as normal in all joints of allasymptomatic volunteers examined with MRI,although very few series focusing on TMJ bonemarrow in healthy individuals are available.16,17

Normal bone marrow findings at histology and

MRI are described in   Tables 1   and   2,

19

andillustrated in Fig. 3.

TMJ Findings in Patients

Disk displacement is by far the most frequent intra-articular abnormality in patients with TMJdisorders. It is commonly referred to as  internal derangement , defined as a mechanical fault that interferes with the smooth action of the joint.20

 Joint abnormalities that may accompany internalderangement will be discussed in the following

Figure 2.   Normal joint fluid. MRI of TMJ in asymptomatic volunteer. (A) Proton-density image. (B) Corre-sponding T2-weighted image. Increased T2 signal consistent with fluid in superior joint compartment of theanterolateral recess. (The disk is displaced in this part of the joint.) Maximum amount of fluid seen inasymptomatic volunteers. (Reprinted with permission from Larheim et al.16)

32   Larheim, Sano, and Yotsui 

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sections, with focus on changes in the bone mar-row and intra-articular soft tissues.21,22

Bone Marrow Abnormalities 

In a series of 50 TMJs in 44 patients in whomMRI and surgery were performed for painfulinternal derangements, a core biopsy specimen was obtained from the marrow of the mandibu-lar condyles at the time of surgery.19 The biopsy 

 was obtained whether or not abnormal MRI sig-nals were seen from the condyle marrow. Thishighly selected material from surgically treatedpatients showed histologically abnormal bonemarrow in more than one-third (36%) of the joints. Half of these joints showed marrow edema without osteonecrosis (Fig. 4) and theother half showed osteonecrosis (Fig. 5) with or without marrow edema. Table 2 shows the MRIclassification of the bone marrow, and Table 3

shows the correlation of MRI and histologic eval-uation of the core biopsy specimens. More thanhalf of the joints with marrow edema were nor-mal on MRI, probably because the edemas werefocal, occupying only small areas of the condyle

marrow (Fig. 4). Thus, MRI seemed to be fairly insensitive for the detection of focal marrow edemas, as also experienced in an experimentalstudy of the femoral head.23

The detection of osteonecrosis in the mandib-ular condyle with MRI showed a sensitivity of 78% (Table 3).19 The most reliable MRI featureof osteonecrosis in the bone marrow was foundto be a combination of edema pattern and scle-rosis pattern (Fig. 6). Marrow sclerosis patternon MRI could either be osteonecrosis (Fig. 7) oradvanced osteoarthritis without osteonecrosis,

histologically (Fig. 8), giving a positive predictive value of only 54%. Thus, an overestimation of osteonecrosis was found when the imaging diag-nosis was based on the MR signal pattern of marrow sclerosis (Table 3). The combination of decreased and increased MR signal recognizedin osteonecrotic TMJs is rather similar to the“double line sign” seen on T2-weighted imagesof hip or knee osteonecrosis.24,25 The focal sub-chondral signal intensity in those joints isthought to represent sclerosis and hyper vasculargranulation tissue w ith devitalized bone.25,26

Larheim et al19 found that 39% (7 of 18

cases) with histologically documented marrow edema and/or osteonecrosis showed MRI signsof joint effusion (Fig. 7), in both early and late

Table 2.  MRI Classification of Bone Marrow of Mandibular Condyles

MRI Classification Signal Intensity Patterns 

I. Normal Homogeneous bright signal onT1-weighted (protondensity) images andhomogenous intermediatesignal on T2-weightedimages.

II. Edema Decreased signal on T1- weighted (proton density)images and increased signalon T2-weighted images;edema pattern.

III. Osteonecrosis a. Decreased signal on T1- weighted (proton density)images and on T2-weightedimages; sclerosis pattern.

b. Combination of edema (II)and sclerosis (IIIa) pattern.

Reprinted with permission from Larheim et al.19

Table 1.   Histologic Classification of Core Biopsiesof Mandibular Condyles

Histologic Classification Description of Microscopic Features 

I. Normal a. Without reactive bone formation:

Normal marrow architecture,preservation of thehematopoietic marrow, normaltrabecular and cortical bonearchitecture.

b. With reactive bone formation:Normal marrow architecture,preservation of thehematopoietic marrow, evidenceof increased bone cell activity,increased bone remodeling andreactive bone formation.

II. Edema a. Early: Edema fluid with serumprotein exudate within marrow interstitium, preservation of hematopoietic marrow elements,

no evidence of reticulin fibrosis.b. Late: Edema fluid with serumprotein exudate within marrow interstitium, preservation of hematopoietic marrow elements,focal evidence of disruption of marrow interstitium and reticulinfibrosis.

III. Osteonecrosis a. Early: Loss of hematopoieticmarrow elements, loss of normalmarrow stroma and marrow fat,no evidence of reticulin fibrosis.

b. Late: Loss of hematopoieticmarrow elements, loss of normalmarrow stroma and marrow fat,evidence of reticulin fibrosis.

Reprinted with permission from Larheim et al.19

33Changes in the Bone Marrow and Soft Tissues of TMJ 

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osteonecrosis. This is in accordance with MRIobservations in the various stages of osteonecro-sis of the hip.27 In a consecutive series of patients with internal TMJ derangements and evident  joint effusion,   abnormal bone marrow   wasfound in 31%.28 In both these studies,19,28  joint effusion was defined as a larger amount of TMJfluid t han was seen in any asymptomatic volun-

teer.16

The association between abnormal bone

marrow and effusion in the TMJ has been alsoobserved previously in clinical MRI studies.29-31

 Almost half (4 of 9) of the patients with his-tologically documented marrow edema (without evidence of necrosis) and 2 patients with histo-logic evidence of osteonecrosis showed normalcortical bone on MRI.19 The observation of ab-normal bone marrow in joints with intact corti-

cal outline   has been substantiated in clinicalMRI studies28,32,33 (Fig. 9), suggesting that mar-

Figure 3.  Normal bone marrow. MRI (A, B) of TMJ and bone marrow biopsy of mandibular condyle (C) in TMDpatient. (A) Proton-density image. (B) Corresponding T2-weighted image. Normal homogeneous signal fromthe bone marrow (and slightly displaced disk and small condylar osteophyte). (C) Histologic section showsnormal hematopoietic elements interspersed with marrow fat and intact trabecular bone (Hematoxylin eosin;original magnification     50). (Reprinted with permission from Larheim et al.19) (Color version of figure isavailable online.)

Figure 4.   Bone marrow edema. Bone marrow biopsy of mandibular condyle in TMD patient. Histologicsection shows early marrow edema, a patchy focus

 with serum proteins within marrow interstitium sur-rounded by areas of normal hematopoietic marrow (Hematoxylin eosin; original magnification     50).(Reprinted with permission from Larheim et al.19)(Color version of figure is available online.)

Figure 5.   Bone marrow necrosis. Bone marrow bi-opsy of mandibular condyle in TMD patient. Histo-logic section shows osteonecrosis, complete loss of hematopoietic marrow and evidence of inflammatory cell infiltrate (Hematoxylin eosin; original magnifica-tion 50). (Reprinted with permission from Larheimet al.19) (Color version of figure is available online.)

34   Larheim, Sano, and Yotsui 

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row edema and osteonecrosis may occur as sep-arate entities from osteoarthritis of the TMJ.This is well known from the hip where osteoar-thritis develops secondary to osteonecrosis after

 weakening of the subarticular bone with collapseand subarticular fracture.34

The pathogenesis of osteonecrosis is, in gen-eral, poorly understood, but it is well known that marrow edema in the hip may be a precursor toosteonecrosis, and that a marrow edema condi-tion may be transient.23,35 In the hip, the predis-posing factors for osteonecrosis include sicklecell disease, long-term steroid therapy, and alco-

holism. Nontraumatic cases are frequently bilat-eral; how ev er, trauma can cause unilateral osteo-necrosis.36 No such systemic factors were present in the patient group studied with histology of the TMJ, and all cases were unilateral, including

the 2  patients with bilateral histologic observa-tions.19 Therefore, the pathogenesis may be dif-ferent in the TMJ than in other joints. As most patients with histologic evidence of osteonecro-sis showed MRI signs of osteoarthritis and allpatients had internal derangement, the etiology in the TMJ may be possibly related to local mi-crotrauma from internal derangement ratherthan vascular compromise. However, bone mar-row abnormalities seem to occur in both joints with and without int ernal TMJ derangement.Recently, Orhan et al37 demonstrated marrow 

alterations of the TMJs in patients with chronicanemia, showing no cases with internal TMJ de-rangement and using healthy individuals as con-trols. This is the first study reporting bone mar-row alterations in the TMJs of patients withsystemic diseases.

The relationship between bone marrow alter-ations and osteoarthritis is not fully understood,not in the TMJ,19 or in other joints. It was re-

Table 3.   Correlation of MRI Interpretation andHistologic Evaluation of Core Biopsy Specimensfrom 50 Mandibular Condyles

MRI 

Histology Normal 

Marrow 

 Edema Osteonecrosis Total 

Normal 27 2 3 32Marrow edema 5 1 3 9Osteonecrosis 2 0 7 9Total 34 3 13 50

MRI, magnetic resonance imaging.Reprinted with permission from Larheim et al.19

Figure 6.  Disk displacement, osteoarthritis, and bone marrow necrosis. MRI (A, B) of TMJ and bone marrow biopsy (C, D) of mandibular condyle in TMD patient. (A) Proton-density image with open mouth. (B)Corresponding T2-weighted image. Anterior disk displacement without reduction, osteoarthritis, and marrow edema pattern combined with marrow sclerosis pattern within the condylar head. Marrow edema pattern;decreased signal on proton-density image (A) and increased signal on T2-weighted image (B). Marrow sclerosispattern; decreased signal on proton-density image (A) and on T2-weighted image (B). (C) Histologic sectionshows osteonecrosis, complete loss of hematopoietic marrow and evidence of inflammatory cell infiltrate.(Hematoxylin eosin; original magnification    50.) (D) Histologic section shows marked increase of reticulinfiber deposition. (Reticulin fiberstain; original magnification 50.) (Reprinted with permission from Larheimet al.19) (Color version of figure is available online.)

35Changes in the Bone Marrow and Soft Tissues of TMJ 

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cently stated that bone marrow edema may play a central role in the evolution of knee osteoar-thritis and needs to be further explored.38 More-over, the distinction between primary osteone-

crosis and necrosis secondary to osteoarthritismay be impossible based on core biopsy speci-mens. In advanced cases of osteoarthritis, micro-scopic foci of necrosis are frequently foundimmediately adjacent to the joint surface. Occa-sionally, small infarcts can occur, but again they are found at the joint surface and only in joints with advanced osteoarthritis.39 The end-stages of both of these pathologic processes are likely tobe indistinguishable.

Bone marrow edema is generally demonstratedas a nonspecific finding on MRI in relation to a

number of conditions, including osteoarthritis.40

 When it occurs in isolation not triggered by any obvious bone pathology in a clinical setting of joint pain, it constitutes the “bone marrow edema syn-drome.” Radiology–histology correlation studieshave, however, shown variably interstitial marrow edema, necrosis, fibrosis, and trabecular bone ab-normalities. In studies that have attempted to elu-cidate the underlying histopathology, conflictingevidence has thus been generated with regards to

the contribution of the various morphologic ele-ments yielding the bone marrow edema patternon MRI.40 Further research in this field is needed.

Intra-Articular Soft Tissue Changes 

Changes in the retrodiskal tissues  that are not seenin asymptomatic volunteers have been demon-strated in patients with TMJ disorders. Sano and Westesson41 demonstrated a correlation be-tween increased T2 signal in this area and TMJpain. More recently, this observation was con-firmed by Chiba et al,42  who found that 22% of 283 TMJs showed an increased T2 signal andthat 77% of those reported pain compared with44% of those with low signal intensity. They also

showed that the high signal intensity was closely related to the severity of internal derangement,occurring in 8.5% of joints with reducing diskdisplacement, in 21.8% of joints with nonreduc-ing disk displacement, and in 32.4% of joints with nonreducing disk displacement and osteo-arthritis.

Chiba et al42 applied T2-weighted fat-sup-pressed MR images of TMJs to confirm the pres-ence of increased water content, consistent with

Figure 7.  Disk displacement, osteoarthritis, and bone marrow necrosis with joint effusion. MRI of TMJ in TMDpatient. (A) Proton-density image. (B) Corresponding T2-weighted image. Disk  displacement, osteoarthritis,

 joint effusion in superior joint component, and marrow sclerosis pattern (see   Fig. 6) in major part of themandibular condyle. Histology (not shown) demonstrated osteonecrosis. (Reprinted with permission fromLarheim et al.19)

36   Larheim, Sano, and Yotsui 

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inflammatory changes in the posterior disk at-tachment. However, it should be noted that themajority of the joints showed reduced signalintensity in the posterior disk attachment. Inprevious studies on internal TMJ derangement,such reduced signal has been associated withfibrosis,43,44 probably a result of altered function

and loading in this area.Contrast enhancement of intra-articular soft tissues 

after i.v. contrast-medium injection has beenshown in several studies.13,14,45,46 One of thesestudies focused on contrast enhancement of theposterior disk attachment,13  whereas the othersdemonstrated contrast enhancement in the in-ferior or the superior joint compartment (Fig.10). In all studies, contrast-enhanced TMJs wereassociated with internal derangement and joint pain. In one of these studies, the thickness of thesoft tissue surrounding the condyle was mea-

sured to a mean of 4.58 mm in the painful TMJgroup, compared with 1.03 mm in the painlessTMJ group and 0.71 mm in the control group,demonstrating a significant difference betweenthe painful TMJ group and the other 2 groups.14

It is unclear what kind of tissue is enhancingin these TMJ studies because no histologic doc-umentation is available. However, in one study of knee joints with osteoarthritis or rheumatoidarthritis, MR assessment of contrast enhance-

ment and joint effusion was compared with his-tologically diagnosed biopsies.47 The amount of contrast enhancement correlated with the over-all histologic assessment of inflammation andreflected the mass of cell-infiltrated vascularizedsubsynovial tissue, and to lesser extent the cu-mulative synovial proliferative activity.

Arthroscopic TMJ studies  have frequently shownsynovitis and osteoarthritis.48-51 Synovitis hasbeen defined as hypervascularity (hyperemia) orsynovial hyperplasia, and osteoarthritis has beendefined as fissured articular eminence or disk,subchondral bone exposure, or disk perfora-tion.51 In one of these studies, 90% of 114 highly symptomatic TMJs showed synovitis when basedon the degree of vascularity alone.50 Osteoarthri-tis was found in 62% of the joints, of which the vast majority (92%) had an associated synovitis.Osteoarthritis was based on the appearance of 

fissure or erosion of the cartilage lining at thearticular eminence as well as fissure or perfora-tion of the disk. The majority of the jointsshowed synovitis and osteoarthritis or only syno- vitis; only osteoarthritis rarely occurred.50 Theseobservations substantiate those of previous ar-throscopic studies,48,49 although placing evenmore emphasis on the prevalence of synovitis.

 Joint effusion was found to reflect TMJ synovitis inone arthroscopic study of internal derangements.52

Figure 8.   Disk displacement, osteoarthritis but no bone marrow necrosis. MRI (A, B) of TMJ and bone marrow 

biopsy (C) of mandibular condyle in TMD patient. (A) Proton-density image. (B)  Corresponding T2-weightedimage. Anterior disk displacement and osteoarthritis, marrow sclerosis pattern (see Fig. 6) in major part of thecondyle. (C) Histologic section shows replacement of marrow space by dense sclerotic bone and fibrous tissue,suggesting a reparative process and not osteonecrosis (Hematoxylin eosin; original magnification     50).(Reprinted with permission from Larheim et al.19) (Color version of figure is available online.)

37Changes in the Bone Marrow and Soft Tissues of TMJ 

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This seems to be the first study that has comparedthe amount of joint fluid and the degree of synovitis.It should be noted that joint effusion was defined asmore fluid than just lines of increased T2 signalintensity in the joint compartments.

Histologic evidence of inflammatory changes   in

symptomatic TMJs based on biopsies obtainedduring open TMJ surgery procedures has beendemonstrated in several studies. In particular, analtered vascularity has been consistently ob-served, being increased53-56 or decreased.57-59

Furthermore, synovial proliferation has beendemonstrated.55,60,61

What Diagnostic Imaging Information Is Essential? 

There seems to be no doubt that internal derange-ment and osteoarthritis are frequent TMJ abnor-

malities in patients with TMJ disorders. It is alsoclear that these manifestations may be accompa-nied by inflammatory alterations in the bone mar-row and the soft tissues. However, it has beendifficult to consistently relate a specific imagingmanifestation to the joint pain. Also, longitudinalstudies on the outcome of treatment have givenconflicting results. This is not specific for theTMJ. Chronic or recurrent pain in the knee is acentral feature of osteoarthritis, but consistent cor-

relations have not been found between pain andimaging findings of osteoarthritis.38

 Another aspect of the TMJ literature becameobvious in a systematic literature review on theefficacy of MRI in the diagnosis of degenerativeand inflammatory TMDs.62 The authors con-

cluded that in 

5% of the articles reviewed, theconclusions were based on moderate or low levelsof evidence.

Bone Marrow Abnormalities

In one TMJ study, patients with abnormal bonemarrow on MRI had a greater degree of painthan those with normal bone marrow.33 That study also indicated that those with bone mar-row edema pattern had more severe pain thanthose with bone marrow sclerosis pattern, al-

though this difference was not significant. In alater study, Sano et al63 found such significanceand reported that patients with a marrow edemapattern had a higher degree of pain. Further, ina study of different imaging manifestations re-corded before and after the performance of ar-throcentesis of the TMJ, it was shown that thisprocedure was clinically successful (resolvingpain) and associated with a significant decreasein the prevalence of TMJ bone marrow edema.64

Figure 9.   Disk displacement, normal cortical bone, and bone marrow edema. MRI of TMJ in TMD patient. (A)Proton-density image. (B) Corresponding T2-weighted image. Anterior disk displacement, normal cortical bone,and marrow edema pattern (see Fig. 6) in entire condyle. (Reprinted with permission from Larheim et al.28)

38   Larheim, Sano, and Yotsui 

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The findings were contradicted by Chiba et al65

in a longitudinal study, demonstrating persis-tence of bone marrow edema in   70% of the joints with a clinically successful arthrocentesis.

In one study, Yajima et al66 demonstrated that a symptomatic osteoarthritic TMJ can accom-pany increased signal of the condylar bone mar-row on proton density-weighted MR images.

 Associations between bone marrow edemaand   joint   pain in other joints, such as the

knee38,67,68 and the hip,69-71 are reported. How-ever, there are also reports showing no signifi-cant correlations between joint   pain and MR findings of the bone marrow.72,73

Joint Effusion

Even more conflicting results have been demon-strated for TMJ effusion, which has been foundto be associated with pain in several cross-sec-tional studies but not in others. In a longitudinalMRI study, TMJ pain was alleviated or resolved

in all joints in which the amount of fluid de-creased.74 It was also stated by Emshoff and Ru-disch75 that presence or absence of effusion may prove to be an important diagnostic determi-nant in successful arthrocentesis. Previously, thesame authors suggested that pain was not reli-able for predicting the presence of effusion in aconsecutive series of patients with TMJ pain.76

Similarly, changes in the amount of joint effu-sion was not related to the patients’ clinical con-

dition, when MRI before and after TMJ ar-throscopic lysis and lavage was compared.77

The definition of joint effusion has varied sub-stantially, and the fact that TMJ fluid is rathercommon in asymptomatic volunteers and that theamount of fluid may be evident 16 should be paidmore   attention. This was also recently empha-sized.78 Knowledge about the amount of joint fluidseen in healthy volunteers is of great importance alsoin the   diagnostic assessment of knee79 and ankle

 joints.80 The latter study demonstrated no significant differences between the amount of fluid in patientsand asymptomatic volunteers. In the knee study, theauthors reported the normal range of variation inasymptomatic volunteers, including the rare cases of more evident fluid. They concluded that joint effu-sion should be expected when the amount of fluidexceeded t he maximum amount observed in healthy  volunteers.79 In a TMJ study where a similar defini-tion was applied,  15% of  500 patients had in-creased amounts of fluid.28 Of the 70 patients with joint effusion, 30% had bone marrow abnormali-

ties, and most of these had complete disk displace-ment without reduction.28

Synovitis

 A more recent study demonstrated that the se- verity of synovitis significantly improved afterarthroscopic surgery with visually guided TMJirrigation.51 However, this improvement did not seem to be associated with the clinical outcome.

Figure 10.  Disk displacement, osteoarthritis, and contrast enhancement. MRI of TMJ in TMD patient (who alsohad rheumatoid arthritis). (A) T1-weighted precontrast image. (B) T1-weighted postcontrast image. Anteriordisk displacement, osteoarthritis, and enhancement of intra-articular   soft tissue around the disk and in theposterior attachment. (Reprinted with permission from Larheim et al.,21 © S. Karger AG, Basel, Switzerland.)

39Changes in the Bone Marrow and Soft Tissues of TMJ 

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In one study comparing i.v. contrast enhance-ment at MRI before and after nonsurgical treat-ment, decreased contrast enhancement of theposterior disk attachment was observed in 7 of 10 joints and was associated with the resolution

or reduction of joint pain.81

The authors statedthat this association “was much stronger thanthe association between the clinical findings andthe anatomy of the disk.”

Disk Position, Morphology, andMobility

In one MRI study of disk position, disk morphol-ogy, and disk mobility before and after 4 differ-ent treatments for closed lock, Ohnuki et al82

found that neither disk position nor morphol-

ogy did improve despite the clinically successfultreatment. The improved mobility of the disk was the only investigated variable that could berelated to clinical success; stuck disk indicatedunsuccessful clinical outcome. The same conclu-sion was made by Kurita et al83 in a long-termfollow-up study of TMD patients: “Patients whoappeared symptomatic at a younger age or whohad a fixed disk were the most likely to haverecurrent or persistent clinical signs/symptomsof TMJ disorder after 8 years.”

Impaired TMJ function with lack of normaldisk mobility seems to be an important cause of 

pain. This is also in accordance with one of theconclusions in a recent systematic literature re- view.84 The calculated odds ratio for the rela-tionship between pain and disk displacement  without reduction was rather high, but the oddsratios for pain were generally low in relation toother MRI findings. This is not unexpected be-cause nonreducing disk displacements occur al-most exclusively in patients, whereas less severeforms of disk displacements also occur in asymp-tomatic volunteers as discussed earlier in ourreview article.

The systematic literature review revealed a vast heterogeneity in study design, clinical exam-ination methods, and diagnostic criteria. Theconclusions concerning the relationship be-tween pain and various MRI findings were con-tradictory, although significant relationships were reported for some studies concerning joint effusion and bone marrow edema.84

There is probably no unique factor that canexplain the joint pain in patients with TMJ

problems.85 Moreover, the subgroup of pa-tients showing joint abnormalities additionalto the internal derangement (disk displace-ment) and osteoarthritis constitutes only a mi-nor portion of TMD   pat ients referred for di-

agnostic TMJ imaging.21

Conclusions

Future studies must use standardized and well-described imaging criteria for TMJ diagnosis. It is mandatory to have knowledge about MR find-ings in asymptomatic healthy volunteers. As im-aging signs of inflammation fluctuate over time,longitudinal studies are needed to evaluate theimportance of MRI in the management of TMD

patients.

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