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 Table of Contents  
ORIGINAL ARTICLE
Year : 2022  |  Volume : 17  |  Issue : 1  |  Page : 41-46

Cone-Beam Computed Tomography: Fractal Analysis of Osseous Changes in Temporomandibular Joint for Rheumatoid Arthritis Patients: A Retrospective Study


Department of Oral Medicine and Radiology, Tamil Nadu Government Dental College and Hospital, Affiliated to Tamil Nadu Dr. M.G.R. Medical University, Chennai, Tamil Nadu, India

Date of Submission22-Nov-2020
Date of Acceptance27-May-2021
Date of Web Publication22-Jan-2022

Correspondence Address:
Dr. Nivethitha Nagarajan
Department of Oral Medicine and Radiology, Tamil Nadu Government Dental College and Hospital, Chennai 600 003, Tamil Nadu; Tamil Nadu Dr. M.G.R. Medical University, Chennai 600 032, Tamil Nadu
India
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Source of Support: None, Conflict of Interest: None


DOI: 10.4103/injr.injr_315_20

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  Abstract 


Background: Rheumatoid arthritis (RA) is a chronic systemic disorder which is autoimmune, inflammatory, and erosive joint disease affecting all the joints in the body. Temporomandibular joint (TMJ) is involved in advanced cases. Trabecular bone of TMJ has higher metabolic activity and shows higher alterations in RA.
Aim and Objectives: This study evaluated and compared the trabecular bone changes of TMJ in patients with RA using fractal dimension (FD) analysis on cone-beam computed tomography (CBCT).
Materials and Methods: A total of 25 (n = 25) CBCT images of RA patients were included for the study. Mid-sagittal section image was selected, and FD assessment of TMJ was done in the bilateral condylar head, condylar neck, and articular eminence.
Statistical Analysis: SPSS® 25.0 (Statistical Package for the Social Sciences) – independent t-test, one-way ANOVA followed by Tukey's post hoc test was used.
Results: The condylar head had lowest FD values and condylar neck had highest FD values on both the sides. The overall mean values of FD of condylar head, condylar neck, and articular eminence were lower for female than males.
Conclusion: Fractal analysis showed that trabecular bone density was altered in condylar head, condylar neck, and articular eminence. Condylar head was the most affected region followed by articular eminence. Condylar neck was the least affected region in both the sides. Hence, FD analysis of CBCT can potentially be considered as an aid in evaluating osseous changes in trabecular bone architecture of the TMJ and to assess the severity of disease.

Keywords: Cone-beam computed tomography, fractals, rheumatoid arthritis, temporomandibular joint


How to cite this article:
Jayachandran S, Nagarajan N, Archana M. Cone-Beam Computed Tomography: Fractal Analysis of Osseous Changes in Temporomandibular Joint for Rheumatoid Arthritis Patients: A Retrospective Study. Indian J Rheumatol 2022;17:41-6

How to cite this URL:
Jayachandran S, Nagarajan N, Archana M. Cone-Beam Computed Tomography: Fractal Analysis of Osseous Changes in Temporomandibular Joint for Rheumatoid Arthritis Patients: A Retrospective Study. Indian J Rheumatol [serial online] 2022 [cited 2022 Oct 1];17:41-6. Available from: https://www.indianjrheumatol.com/text.asp?2022/17/1/41/336279




  Introduction Top


Rheumatoid arthritis (RA) is a chronic autoimmune disease characterized by symmetrical, inflammatory arthritic changes of small and large joint.[1] It produces a persistent inflammatory synovitis of the joints that leads to erosive joint damage.[2] The prevalence rate ranges from 0.5% to 1% of the population with regional variation.[3] RA usually affects the metacarpophalangeal, proximal interphalangeal, and metatarsophalangeal joints commonly, but it can also affect other joints. Temporomandibular joint (TMJ) is usually involved in advanced cases.[3] About 80% of the rheumatoid patients are seropositive for rheumatoid factor.[2] Orthopantamogram, TMJ tomogram, computed tomography (CT), magnetic resonance imaging (MRI), and cone-beam CT (CBCT) are the radiographic modalities used for diagnostic and prognostic relevance.[4] Patients with RA are at high risk for secondary osteoporotic changes. A change in the bony architecture provides information for the diagnosis of osteoporosis.[5],[6] Fractal dimension (FD) analysis is a statistical tissue analysis used to describe complex shapes and structural patterns based on fractal mathematics.[7] The fractal characteristics which are measured from the radiographs reveal the trabecular bone structure by means of density, microstructure, connectivity, and anisotropy. Higher FD value represents complex bony architecture with denser and less porous trabeculae.[8],[9] The trabecular bone is more eligible for the evaluation of changes in TMJ because it has higher metabolic activity than the cortical portion of alveolar bone.[8] In our study, we analyzed, evaluated, and compared the trabecular bone changes in the condylar head, condylar neck, and articular eminence in patients with RA using fractal analysis on CBCT.


  Materials and Methods Top


This study was carried out at the Department of Oral Medicine and Radiology (Oral radiology unit), Tamil Nadu Government Dental College and Hospital. It was a retrospective study conducted over a period of 2 years from November 2017 to November 2019. The study included the archived CBCT images of patients who were referred for various other purposes to the oral radiology unit. A total of around fifty CBCT images of RA patients were reviewed and evaluated, and 25 (n = 25) CBCT images were scrutinized and included for the study. Five normal CBCT images of otherwise normal patients were retrieved and were used as a standard control for comparison. Study was approved by IERB of Tamil Nadu Government Dental College and Hospital, 4/IERB/2021.

The CBCT images with clearly visible condylar region, subcondylar region, condylar neck region, articular eminence, mandibular fossa, and posterior ramus region with clearly demarcated cortical bone and trabecular bone were included for the study. The CBCT images of patients with a history of RA who were undergoing various treatments (e.g.,: implant procedure) in the hospital were included. Developmental anomalies, structural deformities, syndromes affecting the temporomandibular region, internal derangement, TMJ dislocation, and tumor/fracture in and around the TMJ were excluded from the study. The CBCT images with artifacts, image noises, and altered orientation were excluded from the study. The only difference in the inclusion/exclusion criteria for the standard control and the study groups was that the patients in control group had no history of RA.

CBCT images were obtained using CS 9300 select (Carestream) with 85 kV, 4.0 mA, and 8.01 s. The voxel size was 850 at 8 × 8 with a 0 offset with an exposure of 392 mGy cm2. While undergoing the CBCT, patients were in the standing/natural head position and in the maximum intercuspation. The positioning was done, and scout radiograph was made to standardize and adjust the positioning. CS 3D Imaging- Carestream Dental LLC, 3625 Cumberland Blvd.Ste.700. Atlanta, GA 30339, was used for visualization. The images were viewed in HP Compaq LA1956 ×19-inch light-emitting diode backlit liquid-crystal display (LCD) monitor-a 48.3 cm (19 inches) with viewable area display of 1280 × 1024. The 3D reconstruction was obtained; the axial, coronal, and sagittal slicing of the CBCT was made. The TMJ region was examined completely through all the views to eliminate any abnormalities, and the left/right condylar region and articular eminence were assessed. The TMJ was viewed by 180 μm thickness in Averaging – Integration mode (AVG), 1 × 1 at a zoom level of 0.96. The midsagittal section was selected by adjusting the axes through the axial and the coronal views in the widest dimension possible. The images of midsagittal section were saved in JPEG format for fractal analysis [Figure 1]. A total of sixty images were obtained which included bilateral TMJ region of study and control group. All the saved CBCT images were evaluated, and the assessment of FD of condylar head [Figure 2]a, articular eminence [Figure 2]b, and condylar neck [Figure 2c] was made by a single investigator.
Figure 1: The temporomandibular joint was viewed by 180 um thickness in AVG, 1 × 1 at a zoom level of 0.96. The cone-beam computed tomography image of midsagittal section saved in jpeg format for fractal analysis

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Figure 2: The condylar head (a), articular eminence (b), and condylar neck (c) marked for fractal dimension analysis

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The obtained images were analyzed by the ImageJ software (Image J - Rasband, W.S., ImageJ, U. S. National Institutes of Health, (Bethesda, Maryland, USA) (1.46r-National Institute of Health, USA – Java 1.6.0_20 (32-bit); 428 commands; 58 macros) using computer with configuration including Windows 7 operating system, Intel Core i3-380M, 15.6” 16:9 HD LCD, and HD graphics. The images were converted to binary images, and fractal analysis was performed using the method created by White and Rudolph.[10] The region of interest (condylar head, condylar neck, or articular eminence) was obtained from the original image. The region of interest (84 × 84 pixel) was selected inside the trabecular bone within the cortical boundaries to eliminate changes due to cortical density variations. The images were converted to 8-bit type [Figure 3]a because only 8-bit images can be segmented with ImageJ. This image was duplicated and blurred by Gaussian filter [Figure 3]b to remove the brightness variations due to varying thickness of the bone and overlying soft tissues. This step also removed all the fine-scale and medium-scale structures and retained only larger variations in density. The resultant image was blur type and was subtracted [Figure 3]c from the original image. The value of 128 was added at each pixel location which generated an image of value 128 regardless of the initial image intensity [Figure 3]d. The image was transformed to binary thresholding [Figure 3]e on a brightness value of 128 which revealed the bone marrow spaces and the trabecular outline. The resultant image was eroded and dilated [Figure 3]f to produce an image with reduced noise. The image was skeletonized [Figure 3]g. FD of all skeletonized images was calculated using fractal box count method which included box values (C2, C3, C4, C6, C8, C12, C16, C32, and C64). A graph was obtained between box count and box size in log values which showed the FD value [Figure 3]h.
Figure 3: The images converted to 8-bit type (a). This image was duplicated and blurred by Gaussian filter (b). The resultant image was blur type and was subtracted (c). The value of 128 was added (d). The image transformed to binary thresholding (e). The resultant image was eroded and dilated (f). The image was skeletonized (g). Fractal dimension FD of skeletonized images was calculated using fractal box count (h)

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Statistical analysis

SPSS® 25.0 (Statistical Package for the Social Sciences) (IBM Corp. Released 2017. IBM SPSS Statistics for Windows, Version 25.0. Armonk, NY(New York): IBM Corp.) was used for statistical analysis. Comparison of cases with standard controls (for each side) was done using independent samples t-test. Comparison of variables between the left and right side was performed by independent samples t-test. The comparison of variables within the group (left side/right side) was done using one-way ANOVA followed by Tukey's post hoc test.


  Results Top


Out of the total 25 patients, 18 patients were female and seven patients were male. The mean age of the patients was 42.68 ± 3.567. The mean FD value for left/right condylar head, condylar neck, and articular eminence of the study group through 20–40 years of age and 40–60 years of age is tabulated in [Table 1]. The mean FD value was lowest for left condylar head (41–60 years) and highest for left condylar neck (20–40 years) in females. The mean FD value was lowest for left condylar head (41–60 years) and highest for right condylar neck (20–40 years) in males. The overall mean values of FD of condylar head, condylar neck, and articular eminence were lower for female than males.
Table 1: The mean fractal dimension value for left/right condylar head, condylar neck, and articular eminence of the study group through 20-40 years of age and 40-60 years of ages

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The mean value of the FD (left TMJ) in the cases for condylar head, condylar neck, and articular eminence was 0.995, 1.095, and 1.040, respectively. The mean value of the FD (right TMJ) in the controls for condylar head, condylar neck, and articular eminence was 1.087, 1.103, and 1.094 [Table 2]. The maximum FD value of the condylar head was 0.9946 (left) and 1.0957 (right), whereas the minimum FD value was 0.8729 (left) and 0.8866 (right). The maximum FD value of the condylar neck was 1.0989 (left) and 1.198 (right), whereas the minimum FD value was 0.9956 (left) and 0.9882 (right). The maximum FD value of the articular eminence was 1.0403 (left) and 1.1649 (right), whereas the minimum FD value was 0.9189 (left) and 0.927 (right). The comparison of cases with the standard controls for each side was done using independent samples t-test. The P value for the left condylar head, condylar neck, and articular eminence was 0.002, 0.77, and 0.09, respectively. The P value for the right condylar head, condylar neck, and articular eminence was 0.002, 0.93, and 0.056, respectively.
Table 2: The comparison of fractal dimension of cases with standard controls for both the sides

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The mean value of the FD of the left condylar head, condylar neck, and the articular eminence for cases was 0.99, 1.09, and 1.04, respectively [Table 3]. The mean value of the FD for the right condylar head, condylar neck, and the articular eminence for cases was 1.00, 1.09, and 1.04, respectively. The comparison of variables between the left and right side was performed by independent sample t-test. The P value for condylar head, condylar neck, and articular eminence was 0.95, 0.99, and 0.97, respectively.
Table 3: Comparison of fractal dimension of condylar head, condylar neck, and articular eminence between the left and right side

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The comparison of variables within the group was done using one-way ANOVA followed by Tukey's post hoc test with 95% confidence interval for mean [Table 4] and [Figure 4]. The lower bound value was 0.97, 1.07, and 1.02 for condylar head, condylar neck, and articular eminence, respectively. The upper bound values were 1.02, 1.12, and 1.06 for condylar head, condylar neck, and articular eminence, respectively. The P = 0.014 for the left side and 0.016 for right side.
Table 4: Comparison of fractal dimension within the group (left side and right side)

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Figure 4: The comparison of variables within the group done using one-way ANOVA followed by Tukey's post hoc test with 95% confidence interval for mean

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  Discussion Top


RA is a chronic systemic disorder which is autoimmune, inflammatory, and erosive joint disease affecting all the joints in the body.[11] The primary pathogenesis of rheumatoid factor in RA as an initiator of immune complex-mediated disease was formulated during the 1960s and described by Zvaifler in 1973.[12],[13] RA arises more frequently in females than males, being predominantly observed in the elderly.[3] The above study assessed and compared the FD values of condylar head, condylar neck, and articular eminence of both the TMJ in RA patients. The mean FD values of various region of TMJ revealed that the condylar head had the lowest FD values compared to the other regions. The overall mean values of FD (study group) of the condylar head, condylar neck, and articular eminence were lower in females than males in this study suggestive of females being more affected. The condylar head of the females was the most affected, followed by articular eminence and condylar neck both in males and females.

The TMJ is usually involved in advanced cases.[3] About 50% of patients with RA will present with TMJ complaints.[14] Inflammation of the TMJ has high correlation (>17%) with the late stages of RA.[15] MRI is commonly used to assess the intra-articular processes and CT for osseous structures of TMJ.[16] CBCT for RA is newer modality for diagnostic and prognostic purpose. It has advantages over CT for assessment of the trabecular and cortical bone alterations. The trabecular bone is more eligible for the evaluation of changes in TMJ because it has higher metabolic activity than the cortical portion of alveolar bone.[3] The fractal analysis of various region of TMJ can aid in assessing the trabecular bone in specific portion of TMJ.

Comparing the mean FD values of various region of TMJ, the condylar head had the lowest FD values and the condylar neck had the highest FD values on both the sides suggestive of lowest bone density in condylar head and highest bone density in the condylar neck. The comparison of FD values of cases with standard controls using independent samples t-test on both the sides showed that the FD values of condylar head were significantly lower with a P = 0.002 which was statistically significant. The condylar neck and the articular eminence were not statistically significant on comparison in both the groups. Hence, condylar head was affected more than condylar neck/articular eminence in RA patients in both the sides.

The comparison of FD values of condylar head, condylar neck, and articular eminence between the left and right side revealed that there was no significant difference in FD values between the sides. Hence, both the sides of TMJ are equally affected in the RA, and alteration is evident in the trabecular bone. The comparison of FD values of condylar head, condylar neck, and articular done revealed that there was a significant difference in the values of condylar head, condylar neck, and articular eminence with each other eminence within the group left side/right side. Hence, there were trabecular bone alterations in different regions of TMJ in RA patients. The bone density was altered in the condylar head, condylar neck, and articular eminence. The condylar head was the most affected region, and the condylar neck was the least affected region in both the sides.

Yesiltepe et al. studied CBCT images of 17 female RA patients and evaluated the FD values for trabecular bone structures. RA patients had lower FD values than healthy individuals for each side.[6] This study revealed that the RA had lower FD values. Arsan et al. evaluated the changes in trabecular bone of mandibular condyle in 100 patients with temporomandibular disorders using fractal analysis. Lower FD values were associated with more severe degenerative changes. This study revealed that the condylar head showed significant alterations in FD values with disease entity. The trabecular structure of mandibular condyles in patients with TMD exhibited decreased complexity when sclerotic and erosive changes were evident.[8] This study revealed that the trabecular bone can be as an analytical tool for changes in the severity of the disease. Kayipmaz et al. evaluated the potential changes in condylar trabecular bone structure in the patients with temporomandibular osteoarthritis using fractal analysis. The patients with osteoarthritis had lesser FD values compared to health patients.[17] Doyle et al. evaluated osteoporotic changes by fractal analysis and reported that mandibular FD measurements in postmenopausal women were lower than those in the premenopausal women.[18]

The main limitations of this study were lack of comparison of clinical status with radiographic features, degenerative changes were not analyzed, and cortical bone was not included. CBCT with 3D reconstruction is an imminent imaging modality evaluation of the bony changes of TMJ including the flattening/erosion of bone, reduction in joint space, and other condylar anomalies.[19],[20] This study evaluated the FD of three different region in the TMJ to analyze the changes in RA using CBCT. Hence, FD analysis can potentially be considered as an aid in evaluating osseous changes in the trabecular bone architecture of the TMJ.


  Conclusion Top


Fractal analysis is an emerging tool for analyzing the bone density and can aid as an early diagnostic and prognostic tool. In our study, the fractal analysis of the TMJ (condylar head, condylar neck, and articular eminence) was evaluated which revealed that the trabecular bone was most affected in condylar head, followed by articular eminence and condylar neck. The fractal value was lower in females compared to the males suggestive that the trabecular bone changes were predominant due to RA in females. Hence, FD analysis of CBCT can potentially be considered as an aid in evaluating osseous changes in the trabecular bone architecture of the TMJ to assess the severity of the disease.

Financial support and sponsorship

Nil.

Conflicts of interest

There are no conflicts of interest.



 
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Mupparapu M, Oak S, Chang YC, Alavi A. Conventional and functional imaging in the evaluation of temporomandibular joint rheumatoid arthritis: A systematic review. Quintessence Int 2019;50:742-53.  Back to cited text no. 4
    
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Sanchez-Molina D, Velazquez-Ameijide J, Quintana V, Arregui-Dalmases C, Crandall JR, Subit D, et al. Fractal dimension and mechanical properties of human cortical bone. Med Eng Phys 2013;35:576-82.  Back to cited text no. 5
    
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Yeşiltepe S, Yılmaz AB, Kurtuldu E, Sarıca I. Fracatal analysis of temporomandibular joint trabecular bone structure in patients with rheumatoid arthritis on cone beam computed tomography images. Meandros Med Dent J 2018;19:345-51.  Back to cited text no. 6
    
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Arsan B, Köse TE, Çene E, Özcan İ. Assessment of the trabecular structure of mandibular condyles in patients with temporomandibular disorders using fractal analysis. Oral Surg Oral Med Oral Pathol Oral Radiol 2017;123:382-91.  Back to cited text no. 8
    
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Geraets WG, van der Stelt PF. Fractal properties of bone. Dentomaxillofac Radiol 2000;29:144-53.  Back to cited text no. 9
    
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White SC, Rudolph DJ. Alterations of the trabecular pattern of the jaws in patients with osteoporosis. Oral Surg Oral Med Oral Pathol Oral Radiol Endod 1999;88:628-35.  Back to cited text no. 10
    
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Firestein GS. Evolving concepts of rheumatoid arthritis. Nature 2003;423:356-61.  Back to cited text no. 12
    
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Zvaifler NJ. The immunopathology of joint inflammation in rheumatoid arthritis. Adv Immunol 1973;16:265-336.  Back to cited text no. 13
    
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Tabeling HJ, Dolwick MF. Rheumatoid arthritis: Diagnosis andtreatment. Fla Dent J 1985;56:16-8.  Back to cited text no. 14
    
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Aletaha D, Neogi T, Silman AJ, Funovits J, Felson DT, Bingham III CO, et al. Rheumatoid arthritis classification criteria: an American College of Rheumatology/European League Against Rheumatism collaborative initiative. Arthritis & rheumatism. 2010;62:2569-81.  Back to cited text no. 15
    
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Savtekin G, Şehirli AÖ. Rheumatoid arthritis in temporo-mandibular joint: A review. Niger J Clin Pract 2018;21:1243-6.  Back to cited text no. 16
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Kayipmaz S, Akçay S, Said S, Çandirli C. Trabecular structural changes in the mandibular condyle caused by degener-ative osteoarthritis: A comparative study by cone- beam computed tomography imaging. Oral Radiol 2019;35:51-8.  Back to cited text no. 17
    
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Doyle MD, Harold R, Suri JS. Fractal analysis as a means for the quantification of intramandibular trabecular bone loss from dental radiographs. Proceed SPIE 1991;1380:227-35.  Back to cited text no. 18
    
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  [Figure 1], [Figure 2], [Figure 3], [Figure 4]
 
 
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