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Abstract
Objective To determine the frequency of radiographic changes in the temporomandibular joint, in a representa- tive population of patients with Juvenile Idiopathic Arthritis (JIA) and to compare with findings in healthy controls matched by sex and age. Patients and Methods One hundred and thirty-seven panoramic radiographies (PR) from JIA patients of a pediatric rheumatology outpatient clinic were prospectively evaluated and compared to 137 PR from healthy individuals. Results 102 (74.5%) JIA patients and 47 (34.3%) controls showed at least one radiological alteration (p < 0.001). The following radiographic alterations were more frequently observed in JIA patients than in controls: erosion (p < 0.001), altered condylar morphology (p < 0.001), disproportion between condylar process and the coronoid process (p < 0.001) and accentuated curve in the antegonial notch (p = 0.002). Twenty patients (14.6%) presented the four radiographic alterations simultaneously compared to only two controls (1.5%) (p < 0.001). Conclusion Due to the difference in the frequency of findings in the PR of patients and controls, we concluded that PR has value as a screening tool. In the presence of major changes in the mandible head in the PR of patients with a confirmed diagnosis of JIA, MRI should be considered to detect an active inflammatory process in this joint. Keywords Panoramic radiography, Juvenile idiopathic arthritis, Rheumatic diseases, Diagnostic imaging, Temporomandibular joint Introduction Juvenile Idiopathic Arthritis (JIA) is a chronic inflam - matory disease that develops before age 16 and is char- acterized by persisting arthritis in at least one joint for at least six weeks. JIA is characterized by chronic syno- *Correspondence: vitis and extra-articular manifestations and is diagnosed Vera Lucia Mestre Rosa veramestre.rosa@gmail.com according to the criteria established by the International Department of Pediatrics, Universidade Federal de São Paulo/Escola League of Associations for Rheumatology (ILAR) [1]. JIA Paulista de Medicina (UNIFESP/EPM), Borges Lagoa Street, 802, Vila prevalence in the city of Sao Paulo (Brazil) is 1.96 of 1000 Clementino, São Paulo, SP 04038-001, Brazil Department of Oral Diagnosis/Radiology/Stomatology, Dental School schoolchildren from 1 to 16 years old [2]. in Integrated Clínic of Nove de Julho University, São Paulo, Brazil © The Author(s) 2023. Open Access This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article’s Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article’s Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http:// creat iveco mmons. org/ licen ses/ by/4. 0/. Rosa et al. Advances in Rheumatology (2023) 63:6 Page 2 of 6 Temporomandibular joint (TMJ) involvement Methods has been reported in 17–87% of all JIA patients [3]. Demographic data Although TMJ arthritis can be asymptomatic, it can The following demographic data were obtained from the result in facial growth alterations [4]. patient’s records by a specialist in pediatric dentistry and Panoramic radiography (PR) of the mandible is a temporomandibular disorders (TMD) and orofacial pain two-dimensional imaging method that uses a low dose with experience in rheumatic disease (LMFZ) supervised of radiation and provides an overview of the teeth and by a pediatric rheumatologist (MTT): sex, current age bones of the lower third of the face, including the TMJ at the time of the radiography, age at disease onset, JIA [5]. Unlike other imaging methods, it is inexpensive, subtype classified as polyarticular, oligoarticular and sys - with wide availability, and does not require sedation in temic, disease duration and assessment of disease activ- young children [6]. ity at the time of radiography. Disease activity status was Contrast-enhanced magnetic resonance imaging evaluated as active and inactive, according to Wallace (MRI) is considered the reference standard for detect- et al. [17]. Disease duration was defined as the time from ing early inflammatory changes and other soft tissue the JIA diagnosis, made by a pediatric rheumatologist, to abnormalities in the TMJ, [7, 8] but PR can be used as the date of radiography. an initial screening of TMJ involvement [9]. Several studies have found TMJ alterations in JIA Radiographic images patients using PR as an imaging method [10–15]. How- One hundred and thirty-seven PR (274 TMJ) from JIA ever, the radiographic evaluation of the presence of ero- subjects of a pediatric rheumatology outpatient clinic sion and altered condylar morphology associated with (study group) were evaluated and compared to 137 PR disproportion between condylar process (COP) and the (274 TMJ) from healthy individuals (control group). The coronoid process (CRP) and accentuated curvature in exams in printed films were analyzed using a negatoscope the antegonial notch have not been addressed in the lit- by a radiologist (VLMR) specialized in TMD and orofa- erature. Also, few studies have included a control group cial pain, who was blind to which group the participants that helps in the assessment of pathological changes belonged. These aspects were observed in a dichotomous [16]. way: (1) the condylar morphology classified as altered or Because PR is routinely used during dental care in preserved [14], (2) the presence or absence of disconti- pediatrics, it would be important to determine the iden- nuity in the condyle cortical classified as presence or tifiable characteristics in this type of imaging that could absence of erosion [18], (3) the proportion between the indicate TMJ alterations resulting from an inflammatory height of the condylar process (COP) and the coronoid process. Therefore, this study aimed to determine the process (CRP) classified as preserved or altered [19], frequency of radiographic changes in the TMJ in a repre- and (4) the curvature of the antegonial notch classified sentative population of subjects with JIA and to compare as accentuated or not according to the literature (Fig. 1) with findings in healthy controls matched by sex and age. [20]. Statistical analysis Patients and methods The frequency of radiographic changes was estimated This was an observational study that included JIA from the rate of presence and absence of findings in both patients, according to the ILAR criteria [1], classified as groups using the chi-square or Fisher test for categorical polyarticular, oligoarticular, and systemic JIA subtypes variables. Calculations of sensitivity, specificity, positive regardless of treatment and disease activity status, who and negative predictive values were performed. Multiple were followed between 2007 and 2017 and had a PR in logistic regression analysis was presented with the vari- their medical records. The control group was composed ables to verify statistical significance in the association of healthy individuals that underwent a routine dental test. The estimated risk measure was the odds ratio (OR) examination in a private clinic. Individuals in the control (SPSS Package, GLM, v22.0 for Windows; SPSS Inc., Chi- group were matched by age and sex. Participants with cago, IL). The level of statistical significance was p ≤ 0.05. a previous history of orthodontic treatment or orthog- nathic surgery, facial trauma, were excluded, as well as Results those whose PR did not allow a complete view of both Table 1 shows the demographic and clinical data of TMJ. The control group participants who presented any patients and controls. systemic disease or, facial trauma were also excluded. The following radiographic alterations were more fre - (Diagram 1). The Research Ethics Committee of our quently observed in JIA patients than in controls: ero- institution approved this study. sion (p < 0.001), altered condylar morphology (p < 0.001), R osa et al. Advances in Rheumatology (2023) 63:6 Page 3 of 6 Fig. 1 a demonstrated the erosion in mandibular head; b totally disform mandibular head; and c the depth of the curvature of the antegonial notch and the disproportion between the height of the condylar process (COP) and the coronoid process (CRP) Table 1 Demographic data of patients with juvenile idiopathic Table 2 Radiographic changes in panoramic radiographs of arthritis and control group and clinical data of patients patients with juvenile idiopathic arthritis and control group Female N (%) Patients (137) Controls p value Patients Controls p Value (137) (137) (137) 106 (77.4) 106 (77.4) 1.000 N % N % Age at evaluation mean (± SD) 12.07 (± 4.4) 12 (± 4.3) 0.97 Erosion 46 33.6 12 8.8 < 0.001 Age at diagnosis mean (± SD) 4 (± 3.6) Altered condylar morphology 72 52.6 10 7.3 < 0.001 a b Disease duration mean 7 (± 4.3*) Disproportion between COP and CRP 75 54.7 25 18.2 < 0.001 (± SD)** Accentuated antegonial notch 47 34.3 24 17.5 0.002 JIA subtype Polyarticular N (%) 88 (64.2) Presence of any alteration 102 74.5 47 34.3 < 0.001 JIA subtype Oligoarticular 37 (27.0) Presence of all alterations 20 14.6 2 1.5 < 0.001 N (%) No alterations 35 25.5 90 65.7 < 0.001 JIA subtype Systemic N (%) 12 (8.8) a b condylar process (COP) and the coronoid process (CRP) Disease Activity N (%) 75 (54.7) *in one patient the data was unknown JIA —Juvenile Idiopathic Arthritis **in years values (PV) of the presence of radiographic changes, either alone or in association. The radiographic find - ing with the highest sensitivity was the disproportion disproportion between COP and CRP (p < 0.001) and between the COP and CRP (53% and positive PV 74%). accentuated curve in the antegonial notch (p = 0.002). The most specific result was the altered condylar mor - The patients showed a higher frequency of presence of phology (92% and negative PV 66%). However, the pres- any radiographic alteration (74.5% vs. 34.3%, p < 0.001). ence of the four changes showed a 98% specificity and a Twenty patients (14.6%) presented the four radiographic sensitivity of 14%. alterations simultaneously compared to only two controls Table 4 shows the logistic regression of the variables (1.5%) (p < 0.001). (Table 2). assessed on the PR. We observed that the presence of Table 3 shows the different sensitivities and specifi erosion, altered condylar morphology, disproportion cities, as well as the positive and negative predictive between COP and CRP, and accentuated curve in the Rosa et al. Advances in Rheumatology (2023) 63:6 Page 4 of 6 Table 3 Sensitivity, specificity, positive predictive value and negative predictive value of radiographic changes in patients with juvenile idiopathic arthritis and control group c d c d Sensitivity CI 95% Specificity CI 95% + PV CI 95% - PV CI 95% Erosion 0.34 (0.25–0.42) 0.91 (0.85–0.95) 0.79 (0.66–0.88) 0.58 (0.50–0.64) Altered condylar morphology 0.52 (0.43–0.61) 0.92 (0.86–0.96) 0.87 (0.78–0.93) 0.66 (0.58–0.72) a b Disproportion between COP and CRP 0.53 (0.46–0.63) 0.81 (0.74–0.87) 0.74 (0.65–0.83) 0.64 (0.56–0.71) Accentuated antegonial notch 0.34 (0.26–0.42) 0.82 (0.75–0.88) 0.66 (0.53–0.77) 0.55 (0.48–0.62) Presence of all alterations 0.14 (0.09–0.21) 0.98 (0.94–0.99) 0.90 (0.70–0.98) 0.53 (0.47–0.59) No alterations 0.25 (0.18–0.33) 0.34 (0.26–0.35) 0.28 (0.20–0.35) 0.31 (0.24–0.39) a b c d d condylar process (COP) and the coronoid process (CRP) CI—confidence interval; + PV—positive predictive value and - PV—negative predictive value Table 4 Logistic regression of the variables assessed on the sequelae of previous inflammatory status. This study panoramic radiograph of patients with juvenile idiopathic tried to answer questions that are still poorly defined: arthritis and control group How often these frequent alterations in PR of JIA sub- jects are present in healthy children? Which changes or Variable OR IC95% p combinations among them are specifically associated Erosion 5.26 (2.64–10.50) < 0.001 with TMJ involvement in JIA? Once these alterations Altered condylar morphology 14.07 (6.80–29.07) < 0.001 or combinations are present, in which cases is there a a b Disproportion between COP and CRP 5.42 (3.13–9.38) < 0.001 justification for a referral to a pediatric rheumatologist? Accentuated antegonial notch 2.46 (1.39–4.32) 0.002 We observed that alterations in the PR of subjects condylar process (COP) and the with JIA are persistent findings. When comparing to coronoid process (CRP) the control group, we found a difference in all the evalu - ated findings, which shows that these changes are rarely present in images of healthy individuals. This observa - antegonial notch, increases from 2.4 to 14 times the tion agrees with other studies that found PR alterations likelihood of these findings being related to JIA. in only 6 to 20% of the control participants [11, 16]. We found low sensitivity and high specificity of the Discussion presence of these radiographic alterations. This trend This study shows that several changes in the PR of JIA is accentuated when we associated two, three, and even subjects (erosion, altered condylar morphology, the dis- four findings in the same participant. It means that proportion between COP and CRP, and accentuated many patients with JIA will not have identifiable altera - curve of antegonial notch) were statistically more fre- tions in their PR, but when these findings are present quent in patients than in control subjects. We observed there is a higher likelihood of being related to JIA. Our different sensitivities and specificities depending on the findings are in agreement with those of Im et al. [21]. radiographic alteration; however, the disproportion and They demonstrated in adult individuals that PR had the altered condylar morphology were the most sensitive limited diagnostic accuracy and acceptable reliability in findings, and the presence of altered condylar morphol - the TMJ’s detection of bone lesions [21]. ogy and erosion the most specific. The presence of sev - In the logistic regression, it is evident that alterations eral alterations in the PR increased the likelihood of these in PR are factors to be considered since individuals with findings being related to JIA, to varying degrees. the presence of erosion, altered condylar morphology, These TMJ changes are often asymptomatic, which disproportion between CRP and COP and accentuated means that they could not be considered as involved in curve of antegonial notch are more likely to be patients the JIA patient’s clinical evaluations. This can lead us than controls. We propose that PR should be used as to classify the patient as having oligoarticular JIA when, a diagnostic tool for assessing TMJ, always consider- in reality, he would present polyarticular subtype if we ing its limitations, but using it as an important tool that consider this involvement or to classify the patient as indicates a higher likelihood of being a patient than a inactive when he presents TMJ active involvement. variation in normality. However, it is worth noting that even if alterations are The rationale of this study was based on the advan - present on the patient’s PR, this should not be consid- tages of PR (low cost, low dose of radiation exposure, ered sufficient to change their status from “inactive dis - and ease of access), turning this imaging into an impor- ease” to “active disease”. The changes found on the PR tant screening tool. However, it has limitations related may reflect disease activity, or alternatively, represent R osa et al. Advances in Rheumatology (2023) 63:6 Page 5 of 6 Marcelo Eduardo Pereira Dutra holds D.D.S., M.S. and Ph.D. degrees from the to early structural changes, as it can only detect them at Department of Oral Diagnosis, Radiology School of Dentistry, São Paulo Uni- a later stage. versity (USP) and is a professor of Department of Oral Diagnosis/ Radiology/ In a survey of 87 centers on how pediatric rheuma- Stomatology, Dental School in Integrated Clinic of Nove de Julho University, São Paulo, Brazil. tologists diagnosed TMJ involvement in JIA subjects, 33 Gleice Clemente Souza Russo holds M.D., M.S. and Ph.D. degrees from the centers answered that they still used PR, although the Paulista Medical School, São Paulo Federal University (UNIFESP) and is assistant low sensitivity of this imaging modality to identify early doctor in the Pediatric Rheumatology unit at the Department of Pediatrics, São Paulo Federal University, Paulista Medical School, Brazil. changes in TMJ arthritis is well known [22]. This study Wellington Douglas R. Rodrigues holds M.D., M.S. degrees from the Paulista showed that for 24.6% of the professionals, PR was the Medical School, São Paulo Federal University (UNIFESP) and is nutritionist in first imaging option. the Pediatric Rheumatology unit at the Department of Pediatrics, São Paulo Federal University, Paulista Medical School, Brazil. Although MRI is considered the gold standard in the Maria Teresa Terreri holds M.D., M.S. and Ph.D. degrees from the Paulista Medi- diagnosis of early TMJ involvement in JIA patients [7, 8], cal School, São Paulo Federal University (UNIFESP) and is associate professor the study of Abramowicz et al. [23] shows that the pres- in the Pediatric Rheumatology unit at the Department of Pediatrics, São Paulo Federal University, Paulista Medical School, Brazil. ence of alterations in the condylar morphology in PR is highly sensitive and specific and could reflect the occur - Funding rence of synovitis in MRI. These authors compared PR None. findings with TMJ contrast-enhanced MRI findings. The Availability of data and materials combination of altered condylar morphology and accen- The datasets used and/or analyzed during the current study are available from tuated curve of antegonial notch in the PR was correlated the corresponding author on reasonable request. with the presence of synovitis in the MRI. It confirms the importance of using this imaging modality [23]. The use Declarations of MRI in detecting active inflammatory process in this Ethical approval and consent to participate joint is essential, in the presence of significant changes The Research Ethics Committee of our institution approved this study (Ethics in the mandible head, on the PR of subjects with a con- Committee Number: 1.658.738). firmed diagnosis of JIA. Consent for publication We have as strengths of this study the sample size, its Not applicable. prospective nature, and the presence of a control group. Competing interests The authors declare that they have no competing interests related to the Conclusions content of this manuscript. We conclude that PR has value as a screening tool for JIA subjects due to the difference in the frequency of findings Received: 10 June 2022 Accepted: 19 January 2023 in the PR of patients and controls. Although this type of image cannot demonstrate any active inflammatory pro - cess [10], it can be useful in patients with JIA because it allows an assessment of the morphology of the TMJ’s References mineralized structures. In the presence of significant 1. Petty RE, Southwood TR, Manners P, Baum J, Glass DN, Goldenberg J, et al. International league of associations for rheumatology classification of changes in the mandible head in the PR of subjects with a juvenile idiopathic arthritis: second revision, Edmonton, 2001. 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Are rapid publication on acceptance panoramic radiographs predictive of temporomandibular joint synovitis support for research data, including large and complex data types in children with juvenile idiopathic arthritis? J Oral Maxillofac Surg. • gold Open Access which fosters wider collaboration and increased citations 2014;72(6):1063–9. https:// doi. org/ 10. 1016/j. joms. 2013. 11. 021. maximum visibility for your research: over 100M website views per year Publisher’s Note At BMC, research is always in progress. Springer Nature remains neutral with regard to jurisdictional claims in pub- lished maps and institutional affiliations. Learn more biomedcentral.com/submissions
Journal
Advances in Rheumatology – Springer Journals
Published: Feb 13, 2023
Keywords: Panoramic radiography; Juvenile idiopathic arthritis; Rheumatic diseases; Diagnostic imaging; Temporomandibular joint