Introduction. Binali Çakur 1 İbrahim Şevki Bayrakdar

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1 DOI /s ORIGINAL ARTICLE No proven correlations between bone quality and degenerative bone changes in the mandibular condyle and articular eminence in temporomandibular joint dysfunction Binali Çakur 1 İbrahim Şevki Bayrakdar 1 Received: 31 October 2014 / Accepted: 26 February 2015 Ó Japanese Society for Oral and Maxillofacial Radiology and Springer Japan 2015 Abstract Objectives We aimed to determine whether correlations existed between the bone quality of the mandibular condyle and articular eminence and degenerative bone changes (flattening, osteophytes, erosion, sclerosis, and pseudocysts) of the mandibular condyle and articular eminence in temporomandibular joint dysfunction (TMD). Methods Fifty patients with TMD who underwent conebeam computed tomography examination were retrospectively analyzed. Parasagittal images of the TMJs were evaluated with regard to both bone quality (types I IV) and degenerative bone changes (flattening, osteophytes, erosion, sclerosis, and pseudocysts) of the mandibular condyle and articular eminence. Results No correlations were found between the bone quality index (BQI) and degenerative bone changes in the mandibular condyle or articular eminence of the TMJ. The most common BQI type was type III. The BQI values of the articular eminence and mandibular condyle differed significantly between male and female subjects (p \ 0.05), being slightly higher in male subjects than in female subjects. Conclusions Although no correlations were found between the bone quality types and degenerative bone changes in joints in the TMD patients, all patients had poor-quality bone. & Binali Çakur bcakur@atauni.edu.tr 1 Department of Oral Diagnosis and Radiology, Faculty of Dentistry, Atatürk University, Erzurum, Turkey Keywords Temporomandibular joint dysfunction Bone quality Degenerative bone changes Cone-beam computed tomography Introduction Temporomandibular joint dysfunction (TMD), characterized by intra-articular positional and/or structural abnormalities, affects the temporomandibular joint (TMJ), masticatory muscles, and/or associated structures [1 3]. Joint and muscle pain, mouth-opening limitation, clicking, and crepitation are the most common clinical signs and symptoms of TMD [4]. However, degenerative bone changes involving the bony structures of the TMJ, such as flattening, erosion, osteophytes, sclerosis, and pseudocysts, are frequently observed in TMD [4, 5]. Degenerative bone changes, including destruction of the articular surfaces of the mandibular condyle and glenoid fossa, are often caused by increased loading of the joint [4, 5]. In the literature, there are many articles on TMJ morphology and disorders [1, 6, 7]. Bone quality includes several aspects of bone structure and composition, including bone turnover, micro architecture, degree and distribution of mineralization, extent of micro damage and its repair, and finally the composition of bone matrix and minerals [8]. Lekholm and Zarb [9] classified the jawbone into four types (I IV) based on the amounts of cortical bone versus trabecular bone evident on pantographic films, with types I and IV bone having the best and worst quality, respectively. The bone quality index (BQI) is a four-point index (I IV) that describes four types of bone quality [9, 10]: I, composite of homogeneous and compact bone; II, thick layer of compact bone surrounding a core of dense trabecular bone; III, thin layer of cortical bone surrounding a dense trabecular bone

2 of favorable strength; and IV, thin layer of cortical bone surrounding a core of low-density trabecular bone. This index has been widely applied by clinicians to evaluate patient bone for dental implant placement. Bone quality is an important factor for dental implants, and there are many studies on bone quality related to dental implant placement in the literature [10 13]. Several studies indicated that the success rate of dental implants was highly dependent on the quality of the host bone, and found greater failure rates in dental implants in type IV bone, suggesting that the BQI might have practical use in patient assessment [11 13]. However, how bone quality influences degenerative bone changes in the TMJ remains unclear. The objective of the present study was to determine whether correlations existed among the bone quality of the mandibular condyle and articular eminence and degenerative bone changes (flattening, osteophytes, erosion, sclerosis, and pseudocysts) of the mandibular condyle and articular eminence in TMD. Materials and methods This retrospective study was performed using tomographic images obtained from patients who reported a variety of TMJ complaints and were examined by cone-beam computed tomography (CBCT) at our clinic. In total, 50 patients with TMD who underwent CBCT examination were retrospectively analyzed. The age range was years, with a mean age of ± 13.9 years. Of the 50 patients, 37 (74 %) were female and 13 (26 %) were male. All patients underwent CBCT imaging with a NewTom 3G System (Quantitative Radiology, Verona, Italy). The 9-inch field of view included both TMJs. The X-ray parameters (kv, ma) were automatically determined from scout views by the NewTom 3G. The mean axial diameter was 1 mm, mean sagittal diameter was 2 mm, mean coronal diameter was 2 mm, scanning time was 36 s, and voxel size was 0.16 mm. All CBCT scans were performed with the patients resting in the supine position. Positioning of the patient s head was performed using two light-beam markers. The vertical positioning light was aligned with the patient s mid-sagittal line, which helped to keep the head centered relative to the rotational axis. The lateral positioning light was centered at the level of the condyles, indicating the optimized center of the reconstruction area. In addition, the head position was adjusted in such a manner that the hard palate was perpendicular to the floor. The primary reconstruction was restricted to a region of approximately 1 cm in diameter with the TMJ at the center, and a series of axial views were automatically generated. On the axial TMJ images, a line perpendicular to the anteroposterior plane of the examined condyle was drawn, and parasagittal images were generated by NNT Software (version 2.21; Quantitative Radiology). The thickness of the image slices was 1 mm, and the distance between the parasagittal slices was 1 mm. To assess the intra-observer reliability, the reconstructions were assessed twice by an expert oral and maxillofacial radiologist with 7 years of experience in diagnosing changes to TMJ bone surfaces on CBCT images, using a computer with a 17-inch LCD monitor in a darkened room. The minimum interval between evaluations of the same patient was 30 days. The right and left TMJs were evaluated separately, resulting in a total of 100 TMJs. Age, sex, osseous changes, and bone qualities were recorded. To avoid misinterpretation, bone changes had to be found in at least two consecutive slices. The CBCT images of the TMJ were evaluated with regard to both bone quality and degenerative bone changes of the mandibular condyle and articular eminence. The following evaluations of the mandibular condyle and articular Fig. 1 Degenerative bone changes (arrows) in the mandibular condyle and articular eminence. The changes consisted of: no bone changes (a); osteophytes (b); flattening (c); sclerosis (d); erosion (e); and pseudocysts (f)

3 Fig. 2 Classification of the bone quality (arrows) of the mandibular condyle and articular eminence. The classification types were: BQI type I (only observed in the articular eminence) (a); BQI type II (b); BQI type III (c); and BQI type IV (d) eminence were made on parasagittal images obtained from the axial plane: (1) osteophytes, marginal bony outgrowths of the bone arising from a mineralized joint surface [4] (Fig. 1b); (2) flattening: loss of even convexity or concavity of the joint outline and flat bony contour deviating from the convex or concave form [4] (Fig. 1c); (3) sclerosis: area of increased density and thickness of the cortical bone on the joint surface [4] (Fig. 1d); (4) erosion: local area of rarefaction and decreased density in the cortical plate of the joint surface [4] (Fig. 1e); (5) pseudocyst: wellcircumscribed radiolucent area without cortical destruction that could be immediately below the cortical plate or deep in the trabecular bone [4] (Fig. 1f); and (6) BQI: bone quality based on the amounts and proportions of cortical bone and trabecular bone. The four types were defined as follows: I, homogeneous cortical bone (Fig. 2a); II, thick cortical bone with marrow cavity (Fig. 2b); III, thin cortical bone with dense trabecular bone of good strength (Fig. 2c); and IV, very thin cortical bone with low-density trabecular bone of poor strength [9, 10] (Fig. 2d) , substantial agreement; , almost perfect agreement; and 1.00, perfect agreement. Results Descriptive statistics of the parameters used (BQI, flattening, osteophytes, erosion, sclerosis, and pseudocysts) are shown in Tables 1 and 2. Degenerative bone changes a. Condylar bone. On the CBCT scans, the following changes were observed (Table 3): erosion (62 %); sclerosis (48 %); flattening (41 %); osteophytes (36 %); and pseudocysts (4 %). b. Articular eminence. On the CBCT scans, the following bone changes were observed (Table 3): sclerosis (32 %); erosion (31 %); flattening (19 %); pseudocysts (13 %); and osteophytes (3 %). Statistical analysis Statistical analyses were performed using SPSS for Microsoft Windows software (version 16.0; SPSS, Chicago, IL, USA). Correlations among the variables (BQI, degenerative bone changes) were established using Spearman s correlation coefficient with the significance set at p \ A t test was used to compare the mean values of female and male patients. Kappa statistics for agreement were used to assess the intra-observer reliability, and interpreted as follows: \0, poor agreement; , slight agreement; , fair agreement; , moderate agreement; BQI a. Condylar bone. BQI type I was not observed. The remaining BQI types were observed in the patients at the following frequencies (Table 3): BQI type II, 22 (22 %); BQI type III, 77 (77 %); and BQI type IV, 1 (1 %). b. Articular eminence. BQI type IV was not observed. The remaining BQI types were observed in the patients at the following frequencies (Table 3): BQI type I, 4 (4 %); BQI type II, 35 (35 %); and BQI type III, 61 (61 %).

4 Table 1 Descriptive statistics of the degenerative bone changes (flattening, osteophytes, erosion, sclerosis, and pseudocysts) Minimum (absence) Maximum (existence) Mean SD CF AF CO AO CE AE CS AS CP AP CF condylar flattening, AF articular eminence flattening, CO condylar osteophyte, AO articular eminence osteophyte, CE condylar erosion, AE articular eminence erosion, CS condylar sclerosis, AS articular eminence sclerosis, CP condylar pseudocyst, AP articular eminence pseudocyst, SD standard deviation Relationships among age, BQI, and degenerative bone changes in TMD No correlations were found among age, BQI, and degenerative bone changes (mandibular condyle and articular eminence) in TMD (Table 4). In other words, there were no direct linear relationships among age, BQI, and degenerative bone changes. The BQI values of the articular eminence and mandibular condyle differed significantly between male and female subjects (p \ 0.05). The mean BQI values of the articular eminence and mandibular condyle were slightly higher in male subjects than in female subjects (Table 5). The intra-observer coefficient values showed high reliability for all degenerative bone changes and the BQI. The intra-observer coefficients were 0.89 (almost perfect agreement) for the degenerative bone changes and 0.87 (almost perfect agreement) for the BQI. Discussion Degenerative bone changes are non-inflammatory focal degenerative disorders of the synovial joints. They are characterized by joint deterioration (loss of articular bone and bone erosion) and proliferation (new bone formation at the articular surface and subchondral region) [14], and are initiated by deterioration of the articular soft-tissue cover and exposure of the underlying bone [15]. In the mild-tomoderate forms of degenerative bone changes, the TMJ is asymptomatic. However, arthritic changes, such as flattening, erosion, osteophytes, sclerosis, and pseudocysts, can be observed by radiographic examination [4, 14, 16]. In previous studies, TMJ degenerative bone changes were found in 40 % of older adults at the microscopic level and in 14 % at the radiographic level [15], and were more frequent in women than in men [4, 17]. In our study, 74 % of the patients were female and 26 % were male, and the observed changes were more common in women. The greater occurrence in women might be explained by the hormonal influences of estrogen and prolactin, which can exacerbate the degradation of cartilage and articular bone, in addition to stimulating a series of immunological responses in the TMJ [4, 18, 19]. However, some investigators have found no sex differences [20, 21]. In this study, there were no significant differences between the sexes in the degenerative changes. Cruzoé-Rebello et al. [22] observed that men and women shared the same characteristics with regard to internal derangements, and further found that hormonal factors did not seem to play a significant role in the manifestation of internal derangements in the TMJ. It was speculated that boys might be less likely to seek Table 2 Descriptive statistics of the bone quality types (I IV) Minimum (BQI types) Maximum (BQI types) Mean SD CBQI (types I IV) ABQI (types I IV) CBQI condylar bone quality index (I IV), ABQI articular eminence bone quality index (I IV), SD standard deviation Table 3 Distribution of bone changes in the condyle and articular eminence (100 TMJs) F (%) O (%) E (%) S (%) P (%) BQI I BQI II (%) BQI III (%) BQI IV Condyle 41 (41) 36 (36) 62 (62) 48 (48) 4 (4) 22 (22) 77 (77) 1 (1 %) Articular eminence 19 (19) 3 (3) 31 (31) 32 (32) 13 (13) 4 (4 %) 35 (35) 61 (61) F flattening, O osteophyte, E erosion, S sclerosis, P pseudocyst, BQI I bone quality index type I, BQI IIbone quality index type II, BQI III bone quality index type III, BQI IV bone quality index type IV

5 Table 4 Results of correlation analyses among age, degenerative bone changes (flattening, osteophytes, erosion, sclerosis, and pseudocysts), and bone quality types (I IV) CF AF CO AO CE AE Age p = p = p = p = p = p = CBQI p = p = p = p = p = p = ABQI p = p = p = p = p = p = CS AS CP AP CBQI ABQI Age p = p = p = p = p = p = CBQI p = p = p = p = p = ABQI p = p = p = p = p = CF condylar flattening, AF articular eminence flattening, CO condylar osteophyte, AO articular eminence osteophyte, CE condylar erosion, AE articular eminence erosion, CS condylar sclerosis, AS articular eminence sclerosis, CP condylar pseudocyst, AP articular eminence pseudocyst, CBQI condylar bone quality index, ABQI articular eminence bone quality index Table 5 Results of the t test Male Female Significance Mean SD Mean SD CBQI (types I IV) ABQI (types I IV) CBQI condylar bone quality index, ABQI articular eminence bone quality index, SD standard deviation treatment than girls and only visit hospitals in more advanced stages of the disease [20]. TMJ osteoarthritis is very common in adults and degenerative arthritis is an age-related disease [17, 20]. However, aging is not a crucial factor in the pathogenesis of osteoarthritis and there are no direct linear relationships between age and radiographic changes in the TMJ morphology [20]. According to Alexiou et al. [17], patients in older age groups are expected to have more frequent and severe bone changes than those in younger age groups. However, Cruzoé-Rebello et al. [22] did not find an association between older age and increased bone changes. In addition, according to Cho and Jung [20], TMJ osteoarthritis is common among children and adolescents. In our study, no correlations between age and the other parameters examined (BQI, flattening, osteophytes, erosion, sclerosis, and pseudocysts) were found. In many published studies on the problems associated with bone changes, one of the TMJ structures that have received the most attention is the mandibular condyle, and another is the articular eminence [1, 4, 10, 14, 15]. Campos et al. [23] and Pontual et al. [4] reported that degenerative bone changes were significantly more frequently observed in the mandibular condyle than in the articular eminence, in agreement with the results of our study. Other studies also found that osseous changes of the mandibular fossa were common in patients with osteoarthritis as a result of progressive joint remodeling [17, 24]. It has been reported that flattening, erosion, and osteophytes were the predominant findings among degenerative bone changes [4, 17, 23, 25]. Minimal flattening of the mandibular condyle and/or articular eminence was observed in 35 % of the TMJs in asymptomatic persons [2]. In the present study, erosion was the predominant finding in the mandibular condyle, and sclerosis was the predominant finding in the articular eminence. This finding for the mandibular condyle was similar to the results of other studies [4, 17, 23, 25]. In our study, the high prevalence of erosion might be explained by the fact that erosion is the initial stage of degenerative changes, indicating that the TMJ is unstable and that the changes in bone surfaces will occur, most likely resulting in changes in occlusion [4, 26]. Sclerosis develops secondarily in more progressive forms of the disease [17]. As a result, although the bone changes in the TMJ have been widely evaluated by clinicians, the issue of how bone quality influences the bone structures of the TMJ has remained unclarified. Although clinicians have widely applied the BQI to evaluate patient s bone for dental implant placement [10], to our knowledge, this study is the first to attempt to use the BQI for the TMJ. Many studies have demonstrated that the implant success rate was greatly affected by the quality of the host bone. Clinical studies have shown good long-term prognoses for dental implants placed in the bone of types I and II, as defined by Lekholm and Zarb [9], with significant increases in the

6 failure rate for implants in poor-quality bone, particularly type IV [10, 27]. Hsu et al. [10] evaluated the effects of bone quality on the stability of and stress in an artificial TMJ condylar prosthesis, as well as on the stress and strain distributions in the bone. They stated that the bone quality of the mandible had only minor effects on the stability of and stress in artificial TMJ implants and cortical bone, but greatly affected the microstrain in cancellous bone [10]. In this study, we found that the bone quality types were not correlated with the degenerative bone changes in the joint in TMD. The BQI values of the articular eminence and mandibular condyle differed significantly between males and females (p \ 0.05). The mean BQI values of the articular eminence and mandibular condyle were slightly higher in male patients than in female patients. In other words, the female patients had a slightly thicker layer of compact bone surrounding a core of higher-density trabecular bone than the male patients. In our study, BQI type III was the predominant finding in both the mandibular condyle and the articular eminence. It therefore appears that the patients with TMD had poor-quality bone. The diversity among the prevalences of degenerative bone changes in different studies can be attributed to differences in age groups, sample sizes, and compositions (TMD and non-tmd patients), and the number of examiners, as well as the diagnostic criteria and techniques used. In addition, decreased adaptive capacity of the articulating structures of the joint or excessive or sustained physical stress on the TMJ articular structures that exceed the normal adaptive capacity are risk factors in the development of the disease [2, 28, 29]. The former is a host-adaptive capacity factor, associated with the host s general condition. Advancing age, systemic illness, and hormonal factors can define the host-adaptive capacity of the TMJ. This factor can contribute to dysfunctional remodeling of the TMJ, even when the biomechanical stresses are within normal physiologic ranges [2]. Mechanical factors can also cause changes in the TMJ structure. Despite host-adaptive capacity, excessive or unbalanced mechanical loading in the TMJ can cause overload of articular tissues, resulting in the onset and progression of TMD and degenerative bone changes. Furthermore, internal derangement of the TMJ can be induced by excessive or unbalanced stress on the TMJ. It was shown that fibrocartilaginous tissues, including the disk and articular cartilage, have important functions in stress distribution. In a review of etiological mechanical events in TMJ internal derangement and osteoarthritis, trauma, parafunction, unstable occlusion, functional overloading, and increased joint friction were found to play roles [2, 28 30]. These factors can occur alone or be interrelated, interdependent, and/or coexistent. In conclusion, female patients had a greater predisposition toward degenerative bone changes in the TMJ. Degenerative bone changes were more frequent in the mandibular condyle than in the articular eminence. Erosion and sclerosis were the most prevalent types of degenerative bone changes. Although BQI type III was the most common type in both male and female patients, the bone quality was better in male subjects than in female subjects. However, all patients with TMD had poor-quality bone. The bone quality types did not have an influence on the degenerative bone changes in the joint in TMD. Conflict of interest Binali Çakur and İbrahim Şevki Bayrakdar declare that they have no conflict of interest. Human rights statements and informed consent All procedures followed were in accordance with the ethical standards of the responsible committee on human experimentation (institutional and national) and with the Helsinki Declaration of 1964 and later versions. Informed consent was obtained from all patients for being included in the study. The study was approved by the Ethics Boards of The Faculty of Dentistry, Atatürk University (Protocol No. 27/2014). References 1. Etoz M, Ozdemir ST, Sıgırlı D, Demirbaş AE, Ercan I, Etoz OA, et al. Evaluation of bony structures on panoramic radiographs with statistical shape analysis in patients with temporomandibular joint pain and limited mouth opening. E-J Dent. 2013;3: Tanaka E, Detamore MS, Mercuri LG. Degenerative disorders of the temporomandibular joint: etiology, diagnosis, and treatment. J Dent Res. 2008;87: de Leeuw R. Orofacial pain. Guidelines for assessment, diagnosis, and management. 4th ed. 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