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a r t i c l e i n f o a b s t r a c t
Article history: Objectives: To investigate the correlation between clinical dysfunction index (Di) and condylar bony
Paper received 31 January 2014 changes, glenoid fossa bony changes and joint space changes.
Accepted 8 April 2014 Methods: Clinical data and cone beam computed tomography (CBCT) images of 240 patients with
temporomandibular joint osteoarthritis (TMJ OA) were analyzed. The patients were assigned a score of
Keywords: Helkimo’s clinical Di ranging from 1 to 25 and thereafter divided into 3 groups by the degree of Helkimo’s
Cone beam computed tomography
Di. The condylar bony changes observed with CBCT were graded by the classification method of Koyama
Temporomandibular joint
et al. Glenoid fossa bony changes and joint space changes were both classified as “positive” or “negative”.
Osteoarthritis
Spearman’s rank correlation test was used to correlate the score or degree of Helkimo’s Di with the
maximum condylar bony changes, glenoid fossa bony changes, and joint space changes.
Results: There was a significant correlation between the Helkimo’s Di score and the maximum condylar
bony changes (P 0.0001) and glenoid fossa bony changes (P 0.0001), and there was a poor correlation
between the Helkimo’s Di score and joint space changes (P ¼ 0.184). Furthermore, there was a significant
correlation between the degree of Helkimo’s Di and the maximum condylar bony changes (P 0.0001)
and glenoid fossa bony changes (P 0.0001), but there was a poor correlation between the degree of
Helkimo’s Di and joint space changes (P ¼ 0.346).
Conclusions: Both the score and degree of Helkimo’s Di were highly correlated with maximum condylar
changes and glenoid fossa bony changes, but not with joint space changes.
Ó 2014 European Association for Cranio-Maxillo-Facial Surgery. Published by Elsevier Ltd. All rights
reserved.
1. Introduction 10%e70% of the population presents with some type of TMD, such
as myofascial dysfunction, internal derangement or degenerative
The temporomandibular joint (TMJ), which comprises the joint disease. TMD is epidemic in women between 20 and 40 years
mandibular condyle, the inferior component, and the temporal old (Barros Vde et al., 2009). Osteoarthritis of the TMJ (TMJ OA) is a
bone forming the superior component, is one of the most complex degenerative joint disease and is an age-related disorder charac-
joints in the body (Wu et al., 2012). Temporomandibular disorders terized by the progressive destruction of articular tissues in the
(TMD) are clinically manifested by craniofacial pain, limited mouth mandibular condyle and glenoid fossa often brought about by
opening, and TMJ click occurring in the TMJ, masticatory muscles increased loading on the joint (Okeson, 2008). With advanced
and other relevant structures (John et al., 2007). Approximately degeneration, loss of the subchondral cortical layer, erosion and
other radiographic signs will occur (Stegenga et al., 1989, 1991).
Cone beam computed tomography (CBCT), a new imaging
* Corresponding author. Department of Oral and Maxillofacial Surgery, West modality used in dentistry, is thought to have high dimensional
China School of Stomatology, Sichuan University, No. 14, South Renmin Rd, Chengdu
610041, China.
accuracy in measuring facial structures, including the TMJ (Lascala
E-mail address: shizd_0663@163.com (Z. Shi). et al., 2004) and may be the modality of choice for assessing the
http://dx.doi.org/10.1016/j.jcms.2014.04.001
1010-5182/Ó 2014 European Association for Cranio-Maxillo-Facial Surgery. Published by Elsevier Ltd. All rights reserved.
N. Su et al. / Journal of Cranio-Maxillo-Facial Surgery 42 (2014) 1402e1407 1403
osseous morphology of the TMJ (Hilgers et al., 2005). CBCT is and 4.0 mA and an exposure time of 17.5 s. The voxel size was
increasingly popular for use in TMJ imaging. 0.125 mm, and the slice thickness was 1.0 mm. The field of view
Many authors have noted the need to have a standardized (FOV) size was 120 mm. The images were analyzed with inbuilt
classification for assessing the signs and symptoms of TMD, software (i-Dixel one volume viewer 1.5.0) using a Dell Precision
measuring and comparing the severity of TMJ disorders among T5400 workstation (Dell, Round Rock, TX, USA). Axial, coronal, and
populations, and assessing patients’ condition after treatment; they sagittal 2D sectional images were displayed on a 32-inch Dell LCD
also require a useful implement to study the etiological factors screen with a resolution of 1280 1024 pixels in a dark room. Two
(Miller et al., 2000). Helkimo was a pioneer in developing indexes independent oral and maxillofacial specialists interpreted all of the
to measure the severity of TMJ disorders and pain in TMJ. Helkimo’s images. Any doubt about which classification to assign was deci-
clinical dysfunction index (Di), developed in 1974, is the first such sively evaluated by a third specialist. Based on the CBCT images, the
relevant index (Helkimo, 1974). Di is a functional evaluation of the type of condylar bony changes was classified using the classifica-
masticatory system and classifies individuals on 5 basic signs, tion system of Koyama et al. (Koyama et al., 2007) as follows:
including impaired range of mandibular movement, TMJ function
impairment, pain during mandibular movement, TMJ pain during Type N: No proliferation or thickening on the cortical surface of
palpation, and muscle tenderness (Shahidi et al., 2013). the condyle; displaying typical morphology;
Many researchers have evaluated the correlation between the Type F: Flattened contour at the antero- and/or postero-superior
presence of symptoms or signs of TMD and radiographic changes in portions of the condyle;
the TMJ using different imaging modalities (Crow et al., 2005; Type E: Proliferation or partial hypodense change with or
Palconet et al., 2012; Ohlmann et al., 2006; Huh et al., 2003; without roughening on the cortical surface of the condyle;
Emshoff et al., 2003), and the outcomes were controversial. Some Type D: A deformed contour on the condyle, such as a beak,
studies demonstrated correlations between symptoms or signs without proliferation or partial hypodense change on the
such as pain intensity and the radiographic findings in OA, disc condylar surface;
displacement and joint effusions (Huh et al., 2003; Emshoff et al., Type S: Type D accompanied by Type E.
2003), while others failed to find a correlation (Crow et al., 2005;
Palconet et al., 2012; Ohlmann et al., 2006). Glenoid fossa bony changes were classified as “positive” in the
The aim of this study is to determine whether bony changes, presence of flattening, erosion and/or sclerosis in either joint, or as
including condylar bony changes, glenoid fossa bony changes and “negative” if the glenoid fossa was normal in both joints. Joint space
joint space changes, measured with CBCT are correlated with Hel- changes were classified as “positive” in the presence of the devia-
kimo’s clinical Di in TMJ OA patients. tion of joint space, including increase, reduction or bony contact
between the condyle head and mandibular fossa in either joint, or
2. Materials and methods as “negative” if the joint space was normal in both joints.
The study was approved by the Ethics Committee of the West The statistical analysis was conducted using SPSS 15.0 (SPSS Inc.,
China Hospital of Stomatology at Sichuan University (WCHSIRB-D- Chicago, USA) software. Only the maximum bony change of the
2013-092). CBCT images and clinical records of TMJ OA patients condyle was used as a covariate. Spearman’s rank correlation test
who sought treatment at the Hospital’s Orofacial Pain Clinic from was used to correlate both the scores and degrees of Helkimo’s Di
July 2012 to July 2013 were reviewed in this study. The inclusion with the maximum condylar bony change, glenoid fossa bony
criteria were: diagnosis of TMJ OA according to the Research changes and joint space changes.
Diagnostic Criteria for TMDs (RDC/TMD axis I group IIIb), defined by For testing inter-examiner reliability, the measurements by the
the presence of arthralgia and either TMJ crepitation or CBCT bony two specialists for interpreting the CBCT images were evaluated by
changes, including erosion, flattening or sclerosis of joint surfaces the Kappa test. For testing intra-examiner reliability, 72 subjects
or osteophyte formation (Dworkin and LeResche, 1992). The were randomly selected 2 weeks after the initial review, and their
exclusion criteria were the following: other types of TMD such as radiological reports were reviewed again under the same stan-
myofascial disorder syndrome but normal TMJ structure or rheu- dardized conditions. The consistency between the first and second
matic diseases; a history of TMJ surgery, condylar fracture, jaw measurements of each specialist was also evaluated by the Kappa
trauma or polyarthritis; subjects with missing data. test.
The clinical signs, including TMJ function impairment, muscle
tenderness during palpation, TMJ pain during palpation, pain during
Table 1
mandibular movement and range of mandibular mobility (5 items), Kappa coefficients of inter- and intra-examiner reliability of different variables.
based on the definition of Helkimo’s clinical Di (Helkimo, 1974),
Variables Kappa value Error P value
were extracted from all included patients. Depending on the pres-
ence and/or severity of these clinical symptoms, each patient was Inter-examiner reliability (N ¼ 240)
assigned a score of 0, 1 or 5 points for each item. Depending on the Specialist 1 vs. Specialist 2
Condylar bony changes 0.847 0.028 0.0001
total score, the individuals were divided into 4 groups: Fossa glenoid bony changes 0.848 0.041 0.0001
Joint space changes 0.943 0.025 0.0001
Di 0: 0 point e absence of clinical symptoms; Intra-examiner reliability (N ¼ 72)
Di 1: 1e4 points e mild dysfunction symptoms; Specialist 1
Condylar bony changes 0.922 0.024 0.0001
Di 2: 5e9 points e moderate dysfunction symptoms;
Fossa glenoid bony changes 0.954 0.020 0.0001
Di 3: 10e25 points e acute/serious dysfunction symptoms. Joint space changes 0.954 0.020 0.0001
Specialist 2
The CBCT images of the bilateral TMJ were obtained with a 3D Condylar bony changes 0.896 0.028 0.0001
Accuitomo CBCT machine (MCT-1 [EX-2F], Morita Manufacturing Fossa glenoid bony changes 0.900 0.028 0.0001
Joint space changes 0.908 0.027 0.0001
Corp, Kyoto, Japan) with image capture parameters set at 85.0 kV
1404 N. Su et al. / Journal of Cranio-Maxillo-Facial Surgery 42 (2014) 1402e1407
Table 2 joint space changes are shown in Table 3. Some examples of find-
Distributions of number of patients based on the Helkimo’s Di scores and degrees. ings of bony changes and joint space changes observed by CBCT and
Helkimo’s Di degrees Helkimo’s Number of their associated scores and degrees of Helkimo’s Di are shown in
Di scores patients Figs. 1e3.
Di 0 0 0 According to Spearman’s rank correlation test, the score for
Di 1 1 7 Helkimo’s clinical Di is significantly associated with maximum
2 18 condylar bony changes (P 0.0001) and glenoid fossa bony changes
3 16
(P 0.0001), but not with joint space changes (P ¼ 0.84). The de-
4 8
Total 49 gree of Helkimo’s clinical Di (Di0eDi3) is significantly associated
Di 2 5 7 with maximum condylar bony changes (P 0.0001) and glenoid
6 17 fossa bony changes (P 0.0001), but not with joint space changes
7 18
(P ¼ 0.346) (Table 4).
8 21
9 21
Total 84 4. Discussion
Di 3 10 6
11 15 OA is defined as a low-inflammatory arthritis condition, either
12 24
primary or secondary to trauma or other acute or chronic overload
13 18
15 3 situations, and it is characterized by the erosion of articular carti-
16 13 lage that becomes soft, frayed and thinned, resulting in eburnation
17 12 of the subchondral bone and outgrowth of marginal osteophytes
20 7
(Lohmander et al., 1996). OA is the most common type of TMD in the
21 7
25 2 clinic. The general symptoms of TMJ OA include pain or stiffness in
Total 107 the face and jaws, pain on wide opening, pain on chewing, inability
to open wide, locking or catching of the mandible, and joint noise
(Zarb and Carlsson, 1999). The clinical signs include tenderness to
3. Results palpation of the TMJ and/or the muscles of mastication, limited or
deviated mandibular movements, pain with movement, locking or
A total of 240 patients (194 females and 46 males) met the in- subluxation, and joint sounds (Zarb and Carlsson, 1999).
clusion criteria and were enrolled in the study. Their mean age was Various imaging modalities have been used for evaluating the
36 15.6 years. Strong inter- (Kappa coefficient 0.847e0.943) and morphological bony changes of TMJ OA. Panoramic radiography,
intra- (Kappa coefficient 0.896e0.954) examiner agreements were conventional linear or complex motion tomography, and CT are used
observed for all variables (Table 1). to assess the osseous components of the joints, while magnetic
According to Helkimo’s Di among the total study sample, 0 (0%) resonance imaging (MRI) is used to assess the soft tissue compo-
patients were classified as absent clinical symptoms (Di 0), 49 nents of the TMJ (Barghan et al., 2012). However, panoramic radi-
(20.4%) as mild (Di 1), 84 (35.0%) as moderate (Di 2) and 107 (44.6%) ography has several limitations, such as structural distortion,
as severe (Di 3). The mean score of Helkimo’s Di of the 240 patients superimposition from the zygomatic process, and the inability to
was 9.52 (standard deviation, SD ¼ 5.35). The distribution of pa- show the entire articular surface of the TMJ (Crow et al., 2005).
tients based on the Helkimo’s Di scores and the degrees are shown Panoramic radiographs also have low reliability and low sensitivity
in Table 2. for detecting osseous changes in the TMJ (Ahmad et al., 2009) and
Furthermore, for the maximum condylar bony changes, 0 (0%) thus are of limited value in TMJ assessments. Conventional linear or
patients were classified as Type N, 81 (33.7%) as Type F, 90 (37.5%) complex motion tomography underestimates small bone abnor-
as Type E, 33 (13.8%) as Type D and 36 (15.0%) as Type S. Addi- malities, and the diagnostic accuracy of TMD is limited, although it is
tionally, 54 patients (22.5%) were classified as positive for glenoid superior to panoramic radiographs in sensitivity and specificity for
fossa bony changes, while 186 (77.5%) were negative. Moreover, 185 detecting osseous changes (Flygare et al., 1995). CT has high cost and
patients (77.1%) were classified as positive for joint space changes, relatively high radiation, and there is low access to equipment, all of
while 55 patients (22.9%) were negative. The distributions of scores which limit its use for evaluation of the TMJ (Barghan et al., 2012).
and degrees of Helkimo’s Di and the number of patients based on Helkimo’s Di, which has been widely used in dentistry, espe-
maximum condylar bony changes, glenoid fossa bony changes, and cially in TMD, since 1974, is considered a practical and useful tool
Table 3
Distribution of scores and degrees of Helkimo’s Di and number of patients based on maximum condylar bony changes, fossa glenoid bony changes, and joint space changes.
Fig. 1. Sample images of different types of condylar bony changes according to Koyama et al.’s criteria. Images were from subjects in this study. (a) Female aged 28 years with
maximum bony change of condyle was Type F; the score of Helkimo’s Di was 2, and the degree was 1. (b) Female aged 21 years with maximum bony change of condyle was Type E;
the score of Helkimo’s Di was 5, and the degree was 2. (c) Female aged 40 years with maximum bony change of condyle was Type D; the score of Helkimo’s Di was 9, and the degree
was 2. (d) Female aged 39 years with maximum bony change of condyle was Type S; the score of Helkimo’s Di was 17, and the degree was 3.
for evaluation of TMD and makes between-study comparison be an adaptive alteration (Crusoe-Rebello et al., 2003) and the first
possible (Larsson and Rönnerman, 1981). Hekimo’s Di has been change of progressive disease (Katzberg, 1989). Type F transitions
extensively used to evaluate the clinical or radiographic conditions to Type E as the disease proceeds, indicating that TMJ is unstable
of TMD (Shahidi et al., 2013; Kordass et al., 2012; He et al., 2010; and that the bone surface will change. Moreover, some clinical
Barrera-Mora et al., 2012; Perillo et al., 2011; Rauhala et al., 1999). follow-up studies demonstrated that type E might advance to type
Shahidi et al. (2013) investigated the correlation between articular D or type S because of the progression of condylar resorption, while
eminence steepness measured with CBCT and Helkimo’s Di and type D might advance to type S after the cortical surface is restored
failed to find a correlation. Kordass et al. (2012) investigated the (Koyama et al., 2007). Thus, condylar bony changes were classified
correlation between computer-assisted measurements of mandib- as the progression stage of TMD in the classification of Koyama et al.
ular opening and closing movements and Helkimo’s Di and found a This system of classification was already introduced into the eval-
significant correlation between Helkimo’s Di and frequent popping uation of condylar bony changes observed by CBCT in TMJ OA pa-
sounds in jaw joints and deviation. He et al. (2010) investigated the tients and was proven accurate for diagnosing condylar bony
relationship between centric relationemaximum intercuspation changes (Palconet et al., 2012).
discrepancy and Helkimo’s Di in pre-treated orthodontic patients The results in this study showed that the score and degree of
and found CReMI discrepancy in most of the pre-treated patients Helkimo’s Di were both significantly associated with maximum
with signs and symptoms of TMD. This discrepancy may be a factor condylar bony changes and glenoid fossa bony changes evaluated
contributing to the development of TMD in these patients. by CBCT. The development of the OA symptomatology has already
The above-mentioned barriers have been overcome with the been described clinically (Rasmussen, 1983). In the initial stage, the
advent of CBCT. CBCT has several advantages over CT, such as lower diagnosis of OA was difficult to separate from other types of TMD,
cost, better access to equipment, lower radiation, and diagnostic such as internal derangement of the TMJ, by clinical or radiographic
efficacy as high as CT, but superior to those of panoramic radiog- examination. That is, extremely few patients had symptoms of pain
raphy and linear tomography (Barghan et al., 2012). CBCT is also or abnormal function at this stage. Instead, patients might have
superior to CT for visualizing bony changes in TMJ patients, clicking or periodic locking of the TMJ. Therefore, the score and
analyzing lateral slices in isolation, and combining coronal and degree of Helkimo’s Di were low. In the second stage, TMJ pain
lateral slices (Koyama et al., 2007; Honey et al., 2007). Therefore, occurred. The pain may be caused by the soft tissues around the
CBCT was the imaging method used in this study. affected joint under tension and the masticatory muscles in pro-
In this study, the condylar bony changes were detected using the tective reflex co-contraction as a result of Hilton’s Law (Mercuri,
classification of Koyama et al., which was more practical and 2008). Moreover, the procession of OA can lead to degradation on
convenient for the evaluation of bone changes in TMD patients the surface of the articular soft tissue. When there were large
compared with other classifications (Koyama et al., 2007). In this quantities of degraded products that could not be efficiently
classification, types F and E are comparatively the initial stages of resorbed from the joint cavity by the synovial membrane, an in-
bony changes. Flattening, which is a typical change of Type F, may flammatory response might be elicited to develop synovitis and
Fig. 2. Sample images of different types of glenoid fossa bony changes classified into “negative” and “positive”. Images were from subjects in this study. (a) Female aged 25 years
with negative glenoid fossa bony change; the score of Helkimo’s Di was 7, and the degree was 2. (b) Male aged 48 years with positive glenoid fossa bony change; the score of
Helkimo’s Di was 20, and the degree was 3. (c) Female aged 49 years with positive glenoid fossa bony change; the score of Helkimo’s Di was 17, and the degree was 3. (d) Female
aged 30 years with positive glenoid fossa bony change; the score of Helkimo’s Di was 11, and the degree was 3.
1406 N. Su et al. / Journal of Cranio-Maxillo-Facial Surgery 42 (2014) 1402e1407
Fig. 3. Sample images of different types of joint space changes classified into “negative” and “positive”. Images were from subjects in this study. (a) Female aged 33 years with
negative joint space change; the score of Helkimo’s Di was 9, and the degree was 2. (b) Male aged 35 years with positive joint space change (anterior joint space was increased); the
score of Helkimo’s Di was 9, and the degree was 2. (c) Female aged 45 years with positive joint space change (posterior joint space was increased); the score of Helkimo’s Di was 7,
and the degree was 2. (d) Female aged 52 years with positive joint space change (joint space was decreased); the score of Helkimo’s Di was 13, and the degree was 3.
cause pain (Saxne et al., 1993). Pain also arose from the subchondral 2012; Ohlmann et al., 2006). Poor correlation was reported be-
bone undergoing destruction as a result of the arthritic process tween CBCT-observed condylar changes classified by Koyama’s
(Mercuri, 2008). In the late stage of OA, a reduced normalization of classification and pain, mouth opening, protrusion, or lateral
mandibular function or even late-stage ankylosis and joint insta- movement of the mandible in TMJ OA patients (Palconet et al., 2012).
bility occurred, while radiography revealed increased bone defor- The reasons may be attributed to differences in inclusion criteria;
mation (Mercuri, 2006). Therefore, in the last stage, the score and previous studies (Crow et al., 2005; Ohlmann et al., 2006) included
degree of Helkimo’s Di might be high and reasonably significantly patients with TMD and some subtypes diagnosed by RDC/TMD,
associated with condylar bony changes. while our study included only patients with TMJ OA diagnosed by
Meanwhile, bony changes of the glenoid fossa might occur RDC/TMD. Additionally, the sample sizes in these studies were
because the cases with more severe OA frequently had perforation limited, and the power might be low. Second, the symptoms and
or erosion of discs belonging to the most advanced group of ab- signs were considered separately in these studies, but signs or
normalities (Honda et al., 2001). That is, when bony changes of the symptoms alone may be insignificantly correlated with radio-
glenoid fossa were positive, OA was in the late stage, and the score graphic findings. In our study, therefore, we used a widely used
and degree of Helkimo’s Di were high with the disc perforation or index to evaluate TMJ OA, which considered the symptoms and signs
erosion. Therefore, that may explain why the score and degree of as a whole. Moreover, the methods of pain evaluation were different.
Helkimo’s Di were both significantly associated with bony changes Palconet et al. (2012) used a verbal rating scale (VRS) in which 0 was
of the glenoid fossa. However, little attention has been paid to these “no pain” and 10 was “the worst pain possible”, and the pain was
bony changes in previous clinical studies. evaluated by the patients. In our study, the pain was evaluated as the
We did not find an association between the score or degree of number of pain sites in muscle palpation, TMJ palpation and
Helkimo’s Di and joint space changes. Some clinical studies showed mandibular movements. The pain was evaluated by the doctors, and
that chronic disk displacement was a common cause of OA, and the assessment might be more objective. Furthermore, the imaging
reduced joint space was the most common finding in OA patients modalities used in these studies, including panoramic radiography
(Alexiou et al., 2009). Joint space was found to be normal in only 24% (Crow et al., 2005) and MRI (Ohlmann et al., 2006), were different
of the joints, while it was reduced in 50%, increased in 4%, and bony from ours. These reasons explain the differences.
contact was observed between the condylar head and mandibular However, this study was subject to some limitations. The in-
fossa in 22% of TMJ OA patients (Alexiou et al., 2009). Bony contact clusion criteria of a small number of cited references (Honda et al.,
was expected to be observed in groups of older patients (Alexiou 2001) used for the explanation of the outcomes was not totally the
et al., 2009). In our study, joint space changes occurred in 77% of same as ours, and this might cause some bias. Additionally, the TMJ
OA patients, which included increase, reduction or bony contact is a bilateral articulation with movements on each side. We only
between the condyle head and mandibular fossa in either of the considered the side with maximum condylar bony changes, which
patient’s joints. Therefore, we conclude that the occurrence of joint might cause some deviation in the outcomes. Furthermore, the
space variation is not an indication of OA severity. glenoid fossa bony changes and joint space changes were only
Some clinical studies suggested no significant correlation classified into two categories of “positive” and “negative”. Although
between the presence of symptoms or signs and the degree of this classification is convenient and has been used in other clinical
radiographic changes in the TMJ (Crow et al., 2005; Palconet et al., studies (Palconet et al., 2012), it may be not detailed enough for
evaluating the changes that occur in OA.
Table 4
Correlation of the scores or degrees of Helkimo’s Di with maximum condylar bony 5. Conclusions
changes, fossa glenoid bony changes, or joint space changes (N ¼ 240).
Variables Scores of Helkimo’s Di Degrees of Helkimo’s In conclusion, the results showed that both the score and degree
Di of Helkimo’s Di were highly correlated with maximum condylar
r P value r P value
changes and glenoid fossa bony changes, but not with joint space
changes.
Maximum condylar 0.561 0.0001 0.500 0.0001
bony changes
Fossa glenoid bony 0.245 0.0001 0.235 0.0001 Acknowledgments
changes
Joint space changes 0.086 0.184 0.061 0.346 The authors declare no potential conflicts of interest with
r, correlation coefficient. respect to the authorship and/or publication of this article.
N. Su et al. / Journal of Cranio-Maxillo-Facial Surgery 42 (2014) 1402e1407 1407