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Article

Clinical and Instrumental Temporomandibular Joint Evaluation in Children and Adolescents with Juvenile Idiopathic Arthritis: A Medium-Term Follow-Up

by
Federica Maria Migliore
1,
Luciana Breda
2,
Erica Di Maria
1,
Francesca Battestini
1,
Beatrice Di Carlo
1 and
Michele D’Attilio
1,*
1
Department of Innovative Technologies in Medicine & Dentistry, University of Chieti-Pescara, 66100 Chieti, Italy
2
Pediatric Rheumatology Unit, Department of Pediatrics, University of Chieti-Pescara, 66100 Chieti, Italy
*
Author to whom correspondence should be addressed.
Appl. Sci. 2023, 13(24), 13036; https://doi.org/10.3390/app132413036
Submission received: 29 October 2023 / Revised: 30 November 2023 / Accepted: 4 December 2023 / Published: 6 December 2023
Versions Notes

Abstract

:
(1) Background: The aim of the study was to assess the potential effectiveness of clinical diagnostic examinations, such as muscle palpation, and instrumental examinations, such as electromyography, in the early detection of TMJ involvement in patients with juvenile idiopathic arthritis (JIA), as early diagnosis of these disorders can reduce the risk of developing facial growth anomalies and dento-skeletal malocclusions. (2) Methods: Evaluations were conducted on a cohort of 15 people with juvenile idiopathic arthritis (JIA) and a comparison group of 15 healthy participants at the start of the trial (T0) and after 18 ± 6 months (T1). Data were obtained through clinical examination, involving muscle palpation of the anterior temporalis, masseters, and sternocleidomastoids, and by instrumental analysis using electromyography. The parametric student’s t-test was used to evaluate group comparisons for data that were normally distributed, whereas the nonparametric Mann–Whitney U test was employed for parameters that did not follow a normal distribution. (3) Results: In the JIA group, higher levels of pain were recorded in the sternocleidomastoid muscles on both sides as compared to the control group (p < 0.05) at both T0 and T1. Electromyography revealed no statistically significant variances both in the JIA group and in the control group, except for the IMP index, characterized by a significant improvement over time for the JIA group. (4) Conclusions: According to the methodology employed in this study, all JIA patients had TMD symptoms, mainly muscle disorders. The existence of statistically significant parameters suggests the potential to regard muscle palpation and electromyography as predictive indicators of TMJ involvement in JIA subjects. Additional research is required to validate their reliability.

1. Introduction

The term “Juvenile Idiopathic Arthritis” (JIA) refers to a set of medical disorders in which people under the age of sixteen develop arthritis that lasts for at least six weeks but has no apparent cause [1]. JIA includes seven subtypes, according to the International League of Rheumatology Associations (ILAR), depending on the number of affected joints and the existence of extra-articular, systemic, or serum symptoms: systemic onset (sJIA), juvenile psoriatic arthritis (PsA), oligoarticular (persistent and extensive), polyarticular rheumatoid factor (RF)-positive, polyarticular RF-negative, and undifferentiated arthritis [2]. Several autoantibodies seem to be linked to JIA, including anti-nuclear antibodies (ANAs), rheumatoid factor (RF), anti-citrullinated protein antibodies (ACPAs), and others. According to some authors, these can influence the onset of symptoms as well as the response to therapy and the remission of inflammatory episodes [3]. Recent molecular research, particularly genome-wide association studies (GWASs) on systemic JIA (sJIA), challenges this classification by suggesting an interaction between innate immune system dysfunction and autoinflammation rather than the development of autoantibodies observed in the majority of JIA categories. The International Consensus of the International Organization for Rheumatology Trials (PRINTO) has taken the first step to refine these categories, including sJIA, RF-positive JIA, enthesitis/spondylitis-related JIA, and early-onset ANA-positive JIA. While these categories await formal validation, they highlight the evolving nature of knowledge in this field [4,5]. JIA is among the most common chronic pediatric diseases globally and certainly the most prevalent rheumatic condition in children. The incidence rate is 23 per 10,000 in Europe and 14 per 100,000 in the USA, with a prevalence ranging from 3.8 to 400/100,000 in Europe and 96 per 100,000 in the USA [6]. JIA shares common features with other forms of arthritis, characterized by joint inflammation resulting in swelling, reduced range of motion, and pain when moving [7]. JIA can range from mild and self-limiting to chronic with severe symptoms, including joint erosion [8]. Notably, the JIA inflammatory processes can also affect the temporomandibular joint (TMJ). Its involvement ranges from 40 to 96%, depending on the diagnostic methods and the subtype considered [9]. TMJ issues may manifest early or through the course of JIA [10,11]. Evaluating if the TMJ is involved can be difficult because there is not any obvious joint swelling and there are not any symptoms when arthritis first appears, but if left undetected, it can lead to various functional issues, including reduced jaw mobility and muscle disorders [12]. JIA patients show impaired mandibular range of motion compared to healthy children, including active (45.7 mm in JIA patients and 49 mm in healthy subjects) and passive maximum interincisal openings (47.4 mm in JIA patients and 50.4 mm in healthy subjects) and protrusion (7.5 mm in JIA patients and 8.5 mm in healthy subjects) [13]. When involved, TMJ inflammation causes lesions in chondral and subchondral bones, which results in condylar resorption [14]. The effects of orofacial conditions can be unilateral or bilateral, ranging from morphological dysfunction and deformity to clinically asymptomatic conditions. [15,16,17]. From an orthodontic perspective, TMJ arthritis can severely impact sagittal and vetical jaw growth, causing micrognathia and an open bite with aesthetic and functional consequences [12]. From a muscular point of view, myalgia in the head and neck muscles may occur due to untreated TMJ involvement; pain mainly occurs during mouth opening and mastication, mainly in the articular area and in the masseter area [18,19,20,21]. Early detection of TMJ disorders in JIA patients is crucial to prevent future facial growth and dental problems, moderate the TMJ damage, and increase the patients’ quality of life [22]. Diagnostic steps include collecting patient history, analyzing TMJ and masticatory muscle function, and using magnetic resonance imaging (MRI) to confirm joint involvement during the active inflammatory phase [23,24]. Despite the limitations of clinical examinations in diagnosing TMJ arthritis in JIA patients, they remain a critical part of the overall clinical assessment, including treatment evaluation and monitoring [25]. In 2022, Schmidt et al. published guidelines for the early diagnosis and management of TMJ in JIA subjects, in which regular clinical evaluation of the joint is needed in order to intercept any symptoms [26]. Moreover, a correct differential diagnosis is important; JIA could be confused with rheumatoid arthritis or with SAPHO syndrome, given that they too can manifest symptoms of the masticatory system. However, the former occurs in patients over the age of sixteen, while the latter is a pathology that mainly affects bone tissue in which inflammation of the TMJ arises as a secondary symptom in a limited circle of cases [27,28,29]. Since early detection of TMJ involvement and continued follow-up can be useful to improve the patient’s general condition, this observational study was carried out [22]. The study’s objective is to determine if clinical and instrumental parameters obtained through muscle palpation and electromyographic examination can serve as reliable, non-invasive functional prognostic indicators of potential TMJ involvement in JIA patients. The null hypothesis to be tested is whether there is a statistically significant difference between the recorded values in JIA patients and healthy subjects.

2. Materials and Methods

2.1. Study Design

The study was conducted following the model of the STROBE statement for observational studies [30]. The bioethical approval of the protocol “MGB_AIG” was stated by the local ethical committee, “Comitato Etico delle Province di Chieti e Pescara”.

2.2. Settings

The subjects of the case group were recruited from the Pediatric Department of the SS. Annunziata Hospital in Chieti, Italy. Patients who underwent two consecutive clinical-instrumental examinations during a 12- to 24-month follow-up were selected. Control group data were obtained from the EMG database and the medical records of the Department of Orthodontics of the University of Chieti, Italy.

2.3. Subjects

The JIA group was composed of 15 subjects (14 females and 1 male), aged between 10 and 26 years (16 ± 4.21 years). Before the beginning of the study, the patients—or their parents, if underage—signed informed consent for the handling of the data and the execution of the tests. Participants in this research had the freedom to discontinue their involvement at any point, without any negative impact on their participation. The specific criteria for inclusion and exclusion can be found in Table 1.
Affected patients were compared to an equal number of healthy control subjects (9 females and 6 males) belonging to the same age group.

2.4. Method of Clinical Examination

The clinical evaluation of the patients was realized starting with the acquisition of general medical and dental anamnesis data; the orthodontic records were then filled out, and a gnathological examination was performed following the DC/TMD protocol [31]. All subjects—both case and control groups—underwent an examination with muscle palpation, performed by the same examiner, in order to avoid any inter-examiner distortions and to make the collected data as consistent as possible. The muscles examined were the anterior temporalis (TA), superficial masseters (MMs), and sternocleidomastoid (SCM). Before performing the examinations, the patients were instructed about the difference between pain and pressure sensations. Muscle palpation was performed symmetrically for the same muscles on both sides by exerting a firm but not too energetic pressure with the middle finger, while the second and fourth fingers tested the surrounding areas. The pressure stimulus lasted 10 s, during which the patients were asked if they felt pain and, if present, to quantify it through a range from 0 to 10.

2.5. Electromyographic Examination

Surface electromyography (sEMG) is a significant diagnostic test to analyze muscular activity as well as the pathophysiological alterations in muscles, joints, and related structures. SEMG could, therefore, take part in the diagnostic process of muscle pain referred to as damage to the TMJ. The Teethan BTS TTMJOINT (SpA, Garbagnate Milanese, Italy, https://teethan.com/teethan-software/) software was used for the study, and a wireless surface electromyograph (EMG) was used to record the electrical activity of a muscle during its contractile activity with the use of six pairs of pre-gelled electrodes in order to process the data and graphically represent the biological phenomenon of contraction. Further information is available about the functioning of the electromyograph in the study by D’Attilio et al. [18]. Following the main orientation of the muscular fibers, the electrodes were positioned on the belly of the sternocleidomastoid (SCM), superficial masseter (MM), and anterior temporalis (TA) of the left and right sides. The tests were executed by the same clinician on all subjects, following the standardized protocols of Dr. Ferrario [32,33,34]. The patients were seated upright on a chair without a headrest in a quiet room, with a natural and comfortable head posture, hands on their legs, and feet on the floor. Data recording started 5 min after electrode application to allow the conductive gel to adapt to skin moisture [35]. Three tests were performed as follows: the cotton test (COT6), the clenching test (CLE6), and the rotation test (ROT6). The first two—both lasting 5 s—allowed for the measurement of muscle activity in the maximum intercuspidation. COT6—also called the calibration test—was performed by positioning two cotton rolls occlusally between the back teeth, starting from the second premolars, so that the maximum strength of the muscles without dental contact is expressed and the Teethan software is calibrated for the individual patient. CLE6—or the acquisition test—was performed in normal intercuspidation, so that the changes in neuromuscular activity during dental contact are evaluated by the software and compared with those obtained with COT6. The third test, ROT6, which lasted for an indefinite time and detected sternocleidomastoid activity, consisted of having the patient rotate his head on one side and then on the other, making sure that no head tilting or teeth clenching and no slightly forced rotation occurred during and at the end of the movement, respectively.
All tests were then processed by the software, thus extracting the following parameters:
  • POC: percentage overlapping coefficient (normal values: 83% ≤ X ≤ 100%), identifying which of the pairs of homologous muscles are prevalent. The ideal value was 100%, indicating perfect symmetry between the muscles on the two sides. POC values of the anterior temporalis (POC TA), superficial masseter (POC MM), and sternocleidomastoid (POC SCM) were calculated. The POC TA and POC MM are related to the contacts between the anterior teeth and the posterior teeth, respectively.
  • BAR: occlusal center of gravity (normal values: 90% ≤ X ≤ 100%), indicating whether the masseter or temporal muscles prevail in the patient. Normally, the posterior muscles prevail; therefore, the masseters should prevail in normal conditions.
  • TORS: torsion (normal values: 90% ≤ X ≤ 100%), expressing the torsional attitude on the horizontal plane or the laterodeviation of the jaw. The greater the torqueing effect, the more the TORS approaches zero, since there is no symmetrical activation of the muscle pair.
  • IMP: impact index (normal values: 85% ≤ X ≤ 115%), indicating the muscular workload during the clench. The impact index is influenced by occlusal stability since there is a close relationship between muscle activity and the number of occlusal contacts. The greater the number of occlusal contacts and the greater their area, the better the muscular activity [36].
  • ASIM: right or left asymmetry (normal values −10% ≤ X ≤ +10%) [37], identifying the dominant side by comparing the activity of the right pair (right TA and right MM) to the left pair (left TA and left MM). A value of zero represents the perfect symmetry of the two pairs of muscles; negative values conventionally show a left-pair predominance, whereas positive values show a right-pair predominance.

2.6. Statistical Analysis

The Prism-GraphPad software (Graphpad software, LLC, San Diego, CA, USA, https://www.graphpad.com/) was used for the statistical analysis. The Kolmogorov–Smirnov normality test was employed to assess the normality of the data for each variable. For each muscle, mean and standard deviation values were calculated. The parametric Student’s t-test was used for normally distributed data, while the nonparametric Mann–Whitney U test was applied for variables that did not follow a normal distribution. The statistical significance level was 0.05.
Comparisons were made between the palpation data of the case group and the control group at baseline and at a subsequent observation and between the first and second detection data for the case group and the control group. The same process was conducted for the analysis of electromyographic data, comparing the left and right muscles.

3. Results

3.1. Muscle Palpation Values

According to the statistical analysis, statistical significance emerged in the comparisons made between cases and controls at T0 (Table 2) and T1 (Table 3) at the right and left sternocleidomastoid muscles. This indicates that these muscles are characterized by greater pain sensitivity in JIA patients compared to healthy subjects and that this pain hypersensitivity is maintained over time. No statistically significant differences were found for the other muscles, as well as no statistically significant differences were found in JIA patients (Table 4) and healthy subjects (Table 5) comparing T0 and T1.

3.2. Analysis of Electromyographic Data

The results obtained from the analysis of electromyographic data do not show evident muscle imbalances in any of the pairs of homologous muscles evaluated. These data emerge in the comparison between JIA patients and healthy subjects carried out at baseline (Table 6) and at T1 (Table 7), as well as in the single comparisons between the two examinations of the JIA patients (Table 8) and healthy subjects (Table 9). The only statistically significant findings are related to the IMP index, which appears to be better in the control subjects than in the case patients at the first examination. This value, however, does not show significant differences between JIA patients and healthy subjects at the second examination. Therefore, there is a statistically significant improvement in the IMP index value in the JIA patients between the first and second examinations.

4. Discussion

The aim of the current study was to assess the potential use of electromyography and muscle palpation in identifying early TMJ involvement in JIA patients. These are both routine, non-invasive tests commonly performed during gnathological examinations to verify the health of the TMJ. The electromyographic examination, in particular, is a very powerful tool for TMJ diagnosis and has also been proven useful in polysomnographic studies, highlighting a significant relationship between tonic electromyographic pathways in sleeping bruxism episodes and sleep-related breathing disorders [38]. Moreover, the electromyographic evaluation associated with polysomnography could provide important information on sleep habits, which may have implications for the onset of TMJ disorders, as stated by the study by Topaglu-Ak et al. [39].
The results obtained from the interpretation of muscle palpation data suggest that the conditions of masticatory muscles for JIA patients and healthy controls are similar, except for the sternocleidomastoid muscle group, which shows increased pain that persists over time. The same statistical evidence at the SCM level was found by D’Attilio et al. in a study conducted at G. D’Annunzio University in 2019 [18]. As suggested by Tanaka, the sternocleidomastoid is a postural muscle conditioning the balance of the muscles of the stomatognathic system [40]. The significant difference found in pain sensitivity on SCM palpation in JIA patients could, thus, be explained by the postural implications of this muscle. Moreover, the literature demonstrated an increased instability of postural balance in children with JIA [41]. On the other hand, the non-significance of the other palpation values investigated suggests that in JIA patients with no TMJ symptoms and a good rheumatological follow-up, it is possible to maintain palpation values of head and neck muscles comparable to those of healthy subjects. On the contrary, it is reasonable to think that there is a difference in pain sensitivity indices on palpation between patients with and without TMJ involvement.
The electromyographic results suggest that the masticatory musculature seems to not be involved in the systemic pathology. The significant difference in IMP values between JIA patients and healthy subjects at baseline is confirmed by a previous case-control study conducted by Caroccia et al. in 2022, in which the greater muscular activity of the investigated muscles is due to muscular compensation following the joint deficit [42]. Moreover, statistically significant differences in IMP values were found in JIA subjects between baseline and the second examination, showing an improvement in the muscular workload during the clench. However, IMP values for the case and control groups did not show significant differences at T1; this could be attributable to the onset of compensatory mechanisms or growth-related anatomical or drug therapy changes (which were not considered in the current study) occurring between the first and second examinations in JIA patients.
Furthermore, comparing the muscle palpation results—subjective examination—and electromyographic examination—objective examination—JIA patients show a higher pain sensitivity of muscles on palpation than the general population, but the instrumental measurement of the head and neck muscle functionality does not confirm these subjective findings. The alteration of pain perception with a decreased pain threshold in JIA subjects was also found in a cross-sectional study conducted by Leegaard et al., in which JIA patients showed a lower pain threshold even in areas not usually characterized by arthritis [43].
In conclusion, palpation during clinical examination and electromyographic instrumental tests cannot replace the diagnostic gold standard represented by nuclear magnetic resonance. However, they can constitute valuable tools for clinicians in identifying JIA patients at increased risk of involvement with TMJ, as well as identifying those who may benefit from timely screening or from a therapeutic intervention. Evaluating these parameters in diseased subjects and comparing them with healthy subjects outlined that the test group had a majority of altered parameters and data with respect to the normal physiological condition. However, after analyzing these data and carrying out the statistics, not all proved to be significant for the purposes of our study. This could be due to some limitations of the current study, such as the small sample size, in which the patients were selected on the basis of positivity to JIA without specifying the subtype they belonged to, and the lack of patients with objective signs of TMJ involvement (the only ones reported were occasional clicks, thus insufficient for a diagnosis). Furthermore, our JIA patients come from the Pediatric Rheumatology Unit of Chieti Hospital, where they are included in another follow-up shorter than ours. The more frequent checks allow their unit to detect any potential flare-ups of the inflammation and eventually modify the therapy before our gnathological follow-up at 18 months, thus reducing the objective signs at electromyography.

5. Conclusions

The ultimate goal of this work remains to have an early and functional prognostic JIA indicator that is not invasive and can be implemented repeatedly; obtaining a diagnosis of suspected JIA through a gnathological examination rather than a hospital check-up would improve the number of early diagnoses and, consequently, bring forward the start of therapy, avoiding the onset of irreversible joint alterations. Hence, a larger and more statistically specific sample is needed, made up of patients with objective signs of joint involvement, in order to compare them to JIA patients with no TMJ involvement and healthy subjects. Furthermore, the results of this kind of follow-up with a longer observation time remain to be clarified. Palpation and electromyography can, thus, be considered functional indicators of muscular activity, as they tend to support the experimental hypotheses, but they fail in sensitivity for most of the parameters, probably due to the large variability of the parameters and the small sample size. Nonetheless, the existence of statistically significant parameters and the proximity of others to achieving significance suggest the potential for validating the effectiveness of these diagnostic aids.

Author Contributions

Conceptualization, M.D.; methodology, M.D.; software, F.B.; validation, L.B. and M.D.; formal analysis, F.B.; investigation, F.B.; resources, L.B. and M.D.; data curation, F.B.; writing—original draft preparation, F.B., E.D.M. and F.M.M.; writing—review and editing, F.M.M., B.D.C. and E.D.M.; visualization, F.M.M., E.D.M., L.B., and M.D.; supervision, L.B. and M.D. All authors have read and agreed to the published version of the manuscript.

Funding

This research received no external funding.

Institutional Review Board Statement

The study was conducted in accordance with the Declaration of Helsinki and approved by the local ethical committee of the University of Chieti (protocol no. MGB_AIG).

Informed Consent Statement

Informed consent was obtained from all subjects involved in the study.

Data Availability Statement

The data presented in this study are available upon request from the corresponding author. The data are not publicly available due to privacy and ethical reasons.

Conflicts of Interest

The authors declare no conflict of interest.

References

  1. Aeschlimann, F.A.; Quartier, P. Juvenile idiopathic arthritis. Rev. Prat. 2019, 69, 188–194. [Google Scholar]
  2. Barut, K.; Adrovic, A. Juvenile Idiopathic Arthritis. Balk. Med. J. 2017, 5, 90–101. [Google Scholar] [CrossRef] [PubMed]
  3. Mahmud, S.A.; Binstadt, B.A. Autoantibodies in the Pathogenesis, Diagnosis, and Prognosis of Juvenile Idiopathic Arthritis. Front. Immunol. 2019, 9, 3168. [Google Scholar] [CrossRef] [PubMed]
  4. McCurdy, D.; Parsa, M.F. Updates in Juvenile Idiopathic Arthritis. Adv. Pediatr. 2021, 68, 143–170. [Google Scholar] [CrossRef] [PubMed]
  5. Martini, A.; Ravelli, A. Pediatric Rheumatology International Trials Organization (PRINTO). Toward New Classification Criteria for Juvenile Idiopathic Arthritis: First Steps, Pediatric Rheumatology International Trials Organization International Consensus. J. Rheumatol. 2019, 46, 190–197. [Google Scholar] [CrossRef]
  6. Thierry, S.; Fautrel, B.; Lemelle, I. Prevalence and incidence of juvenile idiopathic arthritis: A systematic review. Jt. Bone Spine 2014, 81, 112–117. [Google Scholar] [CrossRef] [PubMed]
  7. Petty, R.E.; Southwood, T.R.; Manners, P.; Baum, J.; Glass, D.N.; Goldenberg, J.; He, X.; Maldonado-Cocco, J.; Orozco-Alcala, J.; Prieur, A.-M. International League of Associations for Rheumatology classification of juvenile idiopathic arthritis: Second revision, Edmonton, 2001. J. Rheumatol. 2004, 31, 390–392. [Google Scholar]
  8. Cimaz, R. Systemic-onset juvenile idiopathic arthritis. Autoimmun. Rev. 2016, 15, 931–934. [Google Scholar] [CrossRef]
  9. Stoll, M.L.; Kau, C.H.; Waite, P.D.; Cron, R.Q. Temporomandibular joint arthritis in juvenile idiopathic arthritis, now what? Pediatr. Rheumatol. Online J. 2018, 16, 32. [Google Scholar] [CrossRef]
  10. Rongo, R.; Alstergren, P.; Ammendola, L.; Bucci, R.; Alessio, M.; D’Antò, V.; Michelotti, A. Temporomandibular joint damage in juvenile idiopathic arthritis: Diagnostic validity of diagnostic criteria for temporomandibular disorders. J. Oral Rehabil. 2019, 46, 450–459. [Google Scholar] [CrossRef] [PubMed]
  11. Ringold, S.; Cron, R.Q. The temporomandibular joint in juvenile idiopathic arthritis: Frequently used and frequently arthritic. Pediatr. Rheumatol. Online J. 2009, 29, 7–11. [Google Scholar] [CrossRef]
  12. Niibo, P.; Pruunsild, C.; Voog-Oras, Ü.; Nikopensius, T.; Jagomägi, T.; Saag, M. Contemporary management of TMJ involvement in JIA patients and its orofacial consequences. EPMA J. 2016, 7, 12. [Google Scholar] [CrossRef] [PubMed]
  13. De Sonnaville, W.F.C.; Speksnijder, C.M.; Zuinoff, N.P.A.; Verkouteren, D.R.C.; Wilffraat, N.W.; Steenks, M.H.; Rosenberg, A.J.W.P. Mandibular range of motion in children with juvenile idiopathic arthritis with and without clinically estabilished temporomandibular joint involvement and in healthy children: A cross-sectional study. Pediatr. Rheumatol. Online J. 2021, 3, 106. [Google Scholar] [CrossRef] [PubMed]
  14. Billiau, A.D.; Hu, Y.; Verdonck, A.; Carels, C.; Wouters, C. Temporomandibular joint arthritis in juvenile idiopathic arthritis: Prevalence, clinical and radiological signs, and relation to dentofacial morphology. J. Rheumatol. 2007, 34, 1925–1933. [Google Scholar] [PubMed]
  15. Stoustrup, P.; Pedersen, K.T.; Norholt, S.E.; Resnick, C.M.; Abramowicz, S. Interdisciplinary Management of Dentofacial Deformity in Juvenile Idiopathic Arthritis. Oral Maxillofac. Surg. Clin. N. Am. 2020, 32, 117–134. [Google Scholar] [CrossRef] [PubMed]
  16. Lo Giudice, A.; Ortensi, L.; Farronato, M.; Lucchese, A.; Lo Castro, E.; Isola, G. The step further smile virtual planning: Milled versus prototyped mock-ups for the evaluation of the designed smile characteristics. BMC Oral Health 2020, 20, 165. [Google Scholar] [CrossRef] [PubMed]
  17. Lerario, F.; Roncati, M.; Gariffo, A.; Atorresi, E.; Lucchese, A.; Galanakis, A.; Palaia, G.; Romeo, U. Non-surgical periodontal treatment of peri-implant diseases with the adjunctive use of diode laser: Preliminary clinical study. Laser Med. Sci. 2016, 31, 1–6. [Google Scholar] [CrossRef]
  18. D’Attilio, M.; Di Carlo, B.; Caroccia, F.; Moscagiuri, F.; D’Angelo, D.M.; Chiarelli, F.; Festa, F.; Breda, L. Clinical and Instrumental TMJ Evaluation in Children and Adolescents with Juvenile Idiopathic Arthritis: A Case-Control Study. Appl. Sci. 2021, 11, 5380. [Google Scholar] [CrossRef]
  19. Twilt, M.; Mobers, S.M.L.M.; Arends, L.R.; ten Cate, R.; van Suijlekom-Smit, L. Temporomandibular involvement in juvenileidiopathic arthritis. J. Rheumatol. 2004, 31, 1418–1422. [Google Scholar] [PubMed]
  20. Kjellberg, H.; Kiliaridis, S.; Thilander, B. Dentofacial growth in orthodontically treated and untreated children with juvenile chronic arthritis (JCA). A comparison with Angle Class II division 1 subjects. Eur. J. Orthod. 1995, 17, 357–373. [Google Scholar] [CrossRef] [PubMed]
  21. Engström, A.L.; Wänman, A.; Johansson, A.; Keshishian, P.; Forsberg, M. Juvenile arthritis and development of symptoms of temporomandibular disorders: A 15-year prospective cohort study. J. Orofac. Pain 2007, 21, 120–126. [Google Scholar] [PubMed]
  22. Tonni, I.; Fossati, G.; Garo, M.L.; Piancino, M.G.; Cattalini, M.; Visconti, L.; Borghesi, A. Temporomandibular joint involvement in patients with Juvenile Idiopathic Arthritis: Comparison of ultrasonography and magnetic resonance imaging in assessing the periarticular space width. Oral Radiol. 2023, 39, 750–758. [Google Scholar] [CrossRef] [PubMed]
  23. Muller, K.C.L. Early Diagnosis of Temporomandibular Joint Involvement in Juvenile Idiopathic Arthritis: A Pilot Study Comparing Clinical Examination and Ultrasound to Magnetic Resonance Imaging. Rheumatology 2009, 48, 680–685. [Google Scholar] [CrossRef] [PubMed]
  24. Stoustrup, L.T. The Temporomandibular Joint in Juvenile Idiopathic Arthritis. Rheum. Dis. Clin. N. Am. 2021, 47, 607–617. [Google Scholar] [CrossRef] [PubMed]
  25. Abramowicz, S.; Levy, J.M.; Prahalad, S.; Travers, C.D.; Angeles-Han, S.T. Temporomandibular joint involvement in children with juvenile idiopathic arthritis: A preliminary report. Oral Surg. Med. Oral Pathol. Oral Radiol. 2019, 127, 19–23. [Google Scholar] [CrossRef] [PubMed]
  26. Scmidt, C.; Ertel, T.; Arbogast, M.; Hügle, B.; Von Kalle, T.; Neff, A. The Diagnosis and Treatment of Rheumatoid and Juvenile Idiopathic Arthritis of the Temporomandibular Joint. Clin. Pract. Guidel. 2022, 119, 47–54. [Google Scholar]
  27. Małgorzata, R.-O.; Du’s-Ilnicka, I.; Richards, P.; Thomsen, A.M.; Rasmussen, C. Evaluation of oral health status and oral care of patients with rheumatoid arthritis. Int. J. Dent. 2020, 2020, 8896766. [Google Scholar]
  28. Wasserman, A. Diagnosis and Management of Rheumatoid Arthritis. Am. Fam. Physician 2011, 84, 1245–1252. [Google Scholar]
  29. Więckiewicz, M.; Paradowska, A.; Kawala, B.; Więckiewicz, W. SAPHO Syndrome as a possible cause of masticatory system anomalies—A review of the literature. Adv. Clin. Exp. Med. 2011, 20, 521–525. [Google Scholar]
  30. Von Elm, E.; Altman, D.G.; Egger, M.; Pocock, S.J.; Gøtzsche, P.C.; Vandenbroucke, J.P.; STROBE Initiative. The Strengthening the Reporting of Observational Studies in Epidemiology (STROBE) statement: Guidelines for reporting observational studies. J. Clin. Epidemiol. 2008, 61, 344–349. [Google Scholar] [CrossRef]
  31. Schiffman, E.; Ohrbach, R.; Truelove, E.; Look, J.; Anderson, G.; Goulet, J.-P.; List, T.; Svensson, P.; Gonzalez, Y.; Lobbezoo, F. Diagnostic Criteria for Temporomandibular Disorders (DC/TMD) for Clinical and Research Applications: Recommendations of the International RDC/TMD Consortium Network and Orofacial Pain Special Interest Group. J. Oral Facial Pain Headache 2014, 28, 6–27. [Google Scholar] [CrossRef] [PubMed]
  32. Ferrario, V.F.; Tartaglia, G.M.; Luraghi, F.E.; Sforza, C. The use of surface electromyography as a tool in differentiating temporo- mandibular disorders from neck disorders. Man. Ther. 2007, 12, 372–379. [Google Scholar] [CrossRef]
  33. Ferrario, V.F.; Sforza, C.; Serrao, G. The influence of crossbite on the coordinated electromyographic activity of human masticatory muscles during mastication. J. Oral Rehabil. 1999, 26, 575–581. [Google Scholar] [CrossRef]
  34. Ferrario, V.F.; Tartaglia, G.M.; Galletta, A.; Grassi, G.P.; Sforza, C. The influence of occlusion on jaw and neck muscle activity: A surface EMG study in healthy young adults. J. Oral Rehabil. 2006, 33, 341–348. [Google Scholar] [CrossRef] [PubMed]
  35. Berni, K.C.; Dibai-Filho, A.V.; Pires, P.F.; Rodrigues-Bigaton, D. Accuracy of the surface electromyography RMS processing for the diagnosis of myogenous temporomandibular disorder. J. Electromyogr. Kinesiol. 2015, 25, 596–602. [Google Scholar] [CrossRef] [PubMed]
  36. MacDonald, J.W.; Hannam, A.G. Relationship between occlusal contacts and jaw-closing muscle activity during tooth clenching: Part I. J. Prosthet. Dent. 1984, 52, 718–728. [Google Scholar] [CrossRef] [PubMed]
  37. Botelho, A.L.; Silva, B.C.; Gentil, F.H.; Sforza, C.; da Silva, M.A. Immediate effect of the resilient splint evaluated using surface electromyography in patients with TMD. Cranio J. Craniomandib. Pract. 2010, 28, 266–273. [Google Scholar] [CrossRef]
  38. Smardz, J.; Martynowicz, H.; Wojakowska, A.; Michalek-Zrabkowska, M.; Mazur, G.; Wieczorek, T.; Wieckiewicz, M. The meaning of the masticatory muscle tonic-type electromyographic pathway correlated with sleep bruxism and sleep-related breathing disorders—A polysomnographic study. Sleep Med. 2020, 68, 131–137. [Google Scholar] [CrossRef] [PubMed]
  39. Topaloglu-Ak, A.; Kurtulmus, H.; Basa, S.; Sabuncuoglu, O. Can sleeping habits be associated with sleep bruxism, temporomandibular disorders and dental caries among children? Dent Med. Probl. 2022, 59, 517–522. [Google Scholar] [CrossRef]
  40. Uemura, T.K. Study on Motor Learning of Sternocleidomastoid Muscles during Ballistic Voluntary Opening. J. Jpn. Prosthodont. Soc. 2008, 52, 494–500. [Google Scholar] [CrossRef]
  41. Patti, A.; Maggio, M.C.; Corsello, G.; Messina, G.; Iovane, A.; Palma, A. Evaluation of Fitness and the Balance Levels of Children with a Diagnosis of Juvenile Idiopathic Arthritis: A Pilot Study. Int. J. Environ. Res. Public Health 2017, 14, 806. [Google Scholar] [CrossRef] [PubMed]
  42. Caroccia, F.; Passanello, L.; Pipitone, R.; Moscagiuri, F.; Asperio, P.; Lucchese, A.; Breda, L.; D’Attilio, M. Electromyographic Activity of Masticatory Muscles in Subjects with Juvenile Idiopathic Arthritis: A Case—Control Study. Symmetry 2022, 14, 962. [Google Scholar] [CrossRef]
  43. Leegaard, A.; Lomholt, J.J.; Thastum, M.; Herlin, T. Decreased pain threshold in juvenile idiopathic arthritis: A cross-sectional study. J. Rheumatol. 2013, 40, 1212–1217. [Google Scholar] [CrossRef] [PubMed]
Table 1. Inclusion/exclusion criteria.
Table 1. Inclusion/exclusion criteria.
Inclusion CriteriaExclusion Criteria
Patients with a JIA diagnosis of at least six months earlier by the Pediatric Department of the SS. Annunziata Hospital in Chieti, Italy
Age range 10–26 years
No ongoing or previous orthodontic treatments
Compliance and ability to reliably report the manifestation of pain and perform instrumental examinations		Lacking medical history
Diagnosis of inborn craniofacial syndrome
Presence of maxillofacial bone fracture or surgery in medical history
Previous TMJ treatment medical history
Diagnosis of other systemic diseases
Table 2. Muscle palpation analysis of JIA patients and healthy subjects at baseline. Mean and standard deviation of right and left TA, MM, and SCM values.
Table 2. Muscle palpation analysis of JIA patients and healthy subjects at baseline. Mean and standard deviation of right and left TA, MM, and SCM values.
MuscleGroupMean ± SDp-Value
case0.5333 ± 1.125
Right Temporaliscontrol0.2667 ± 0.45770.9999 a
case0.4667 ± 0.994
Left Temporaliscontrol0.2667 ± 0.45770.9999 a
case3.067 ± 3.195
Right Massetercontrol1.067 ± 1.6680.0638 a
case1.933 ± 2.520
Left Massetercontrol1.067 ± 1.6680.4393 a
case5.333 ± 2.845
Right Sternocleidomastoidcontrol3.200 ± 1.7810.0203 b,*
case5.467 ± 2.850
Left Sternocleidomastoidcontrol3.133 ± 1.8460.0128 b,*
Legend: TA: anterior temporalis; MM: superficial masseter; SCM: Sternocleidomastoid; SD:standard deviation; a: Mann–Whitney U test, b: student’s t-test, *: p < 0.05.
Table 3. Analysis of muscle palpation of case group and control group at second examination. Mean and standard deviation values of right and left TA, MM, and SCM.
Table 3. Analysis of muscle palpation of case group and control group at second examination. Mean and standard deviation values of right and left TA, MM, and SCM.
MuscleGroupMean ± SDp-Value
case0.9333 ± 1.944
Right Temporaliscontrol0.1333 ± 0.35190.2008 a
case0.8667 ± 1.727
Left Temporaliscontrol0.1333 ± 0.35190.2008 a
case2.733 ± 3.058
Right Massetercontrol1.400 ± 1.5020.3513 a
case2.467 ± 3.159
Left Massetercontrol1.267 ± 1.3870.5433 a
case5.133 ± 3.482
Right Sternocleidomastoidcontrol2.133 ± 1.9950.0116 a,*
case4.733 ± 3.712
Left Sternocleidomastoidcontrol2.133 ± 1.9950.0439 a,*
Legend: SD: standard deviation; a: Mann–Whitney U test, *: p < 0.05.
Table 4. Muscle palpation analysis of JIA patients: comparison between baseline and second examination data.
Table 4. Muscle palpation analysis of JIA patients: comparison between baseline and second examination data.
MuscleObservationMean ± SDp-Value
baseline0.5333 ± 1.125
Right TemporalisT10.9333 ± 1.9440.7734 a
baseline0.4667 ± 0.9904
Left TemporalisT10.8667 ± 1.7270.6688 a
baseline3.067 ± 3.195
Right MasseterT12.733 ± 3.0580.8079 a
baseline1.933 ± 2.520
Left MasseterT12.467 ± 3.1590.6388 a
baseline5.333 ± 2.845
Right SternocleidomastoidT15.133 ± 3.4820.8645 a
baseline5.467 ± 2.850
Left SternocleidomastoidT14.733 ± 3.7120.5488 a
Legend: SD: standard deviation; a: Mann–Whitney U test.
Table 5. Muscle palpation analysis of healthy subjects: comparison between baseline and second examination data.
Table 5. Muscle palpation analysis of healthy subjects: comparison between baseline and second examination data.
MuscleObservationMean ± SDp-Value
baseline0.2667 ± 0.4577
Right TemporalisT10.1333 ± 0.35190.6513 a
baseline0.2667 ± 0.4577
Left TemporalisT10.1333 ± 0.35190.6513 a
baseline1.067 ± 1.668
Right MasseterT11.400 ± 1.5020.5015 a
baseline0.9333 ± 1.580
Left MasseterT11.267 ± 1.3870.3981 a
baseline3.200 ± 1.781
Right SternocleidomastoidT12.133 ± 1.9950.137 a
baseline3.133 ± 1.846
Left SternocleidomastoidT12.133± 1.9950.1892 a
Legend: SD: standard deviation; a: Mann–Whitney U test.
Table 6. sEMG parameters in JIA and control groups at baseline.
Table 6. sEMG parameters in JIA and control groups at baseline.
IndexNormal RangeJIA Group
(Mean ± SD)		Control Group
(Mean ± SD)		p-Value
POC TA83% ≤ X ≤ 100%82.04 ± 7.80084.11 ± 6.1260.4256 b
POC MM83% ≤ X ≤ 100%80.10 ± 15.6580.44 ± 14.780.8702 a
POC SCM83% ≤ X ≤ 100%81.92 ± 5.66179.34 ± 9.3980.3703 b
BAR90% ≤ X ≤ 100%85.63 ± 6.67185.76 ± 7.0780.9263 a
TORS90% ≤ X ≤ 100%88.65 ± 3.46888.73 ± 4.3630.9528 b
IMP85% ≤ X ≤ 115%155.1 ± 77.00119.8 ± 99.920.0264 a,*
ASIM−10% ≤ X ≤ +10%2.347 ± 17.700.4833 ± 15.420.4363 a
Legend: POC TA: percentage overlapping coefficient of anterior temporalis muscles; POC MM: percentage overlapping coefficient of masseter muscles; POC SCM: percentage overlapping coefficient of sternocleidomastoid muscles; BAR: percentage overlapping coefficient of contact between posterior and anterior teeth; TORS: torsion index; IMP: impact index; ASIM: asymmetry index; SD: standard deviation; a: Mann–Whitney U test; b: t-test; *: p < 0.05.
Table 7. sEMG parameters in JIA patients and healthy subjects at second examination.
Table 7. sEMG parameters in JIA patients and healthy subjects at second examination.
IndexNormal RangeJIA Group
(Mean ± SD)		Control Group
(Mean ± SD)		p-Value
POC TA83% ≤ X ≤ 100%78.69 ± 11.3181.59 ± 8.6520.6827 a
POC MM83% ≤ X ≤ 100%75.63 ± 16.4077.62 ± 18.060.5949 a
POC SCM83% ≤ X ≤ 100%83.88 ± 4.37281.36 ± 9.9200.9349 a
BAR90% ≤ X ≤ 100%77.74 ± 19.1584.10 ± 5.3940.574 a
TORS90% ≤ X ≤ 100%83.19 ± 12.7489.16 ± 3.1630.0814 a
IMP85% ≤ X ≤ 115%91.06 ± 51.7377.07 ± 29.880.3724 b
ASIM−10% ≤ X ≤ +10%8.100 ± 21.555.073 ± 19.170.6875 b
Legend: POC TA: percentage overlapping coefficient of anterior temporalis muscles; POC MM: percentage overlapping coefficient of masseter muscles; POC SCM: percentage overlapping coefficient of sternocleidomastoid muscles; BAR: percentage overlapping coefficient of contact between posterior and anterior teeth; TORS: torsion index; IMP: impact index; ASIM: asymmetry index; SD: standard deviation; a: Mann–Whitney U test; b: t-test.
Table 8. sEMG parameters in JIA patients at baseline and at second examination.
Table 8. sEMG parameters in JIA patients at baseline and at second examination.
IndexNormal RangeJIA Group Baseline
(Mean ± SD)		JIA Group T1
(Mean ± SD)		p-Value
POC TA83% ≤ X ≤ 100%82.04 ± 7.80078.69 ± 11.310.713 a
POC MM83% ≤ X ≤ 100%80.10 ± 15.6575.63 ± 16.400.3046 a
POC SCM83% ≤ X ≤ 100%81.92 ± 5.66183.88 ± 4.3720.2975 b
BAR90% ≤ X ≤ 100%85.63 ± 6.67177.74 ± 19.150.3096 a
TORS90% ≤ X ≤ 100%88.65 ± 3.46883.19 ± 12.740.237 a
IMP85% ≤ X ≤ 115%155.1 ± 77.0091.06 ± 51.730.0124 b,*
ASIM−10% ≤ X ≤ +10%8.100 ± 21.552.347 ± 17.700.3892 a
Legend: see legend at Table 6.
Table 9. sEMG parameters in healthy subjects at baseline at second examination.
Table 9. sEMG parameters in healthy subjects at baseline at second examination.
IndexNormal RangeCTL Group Baseline
(Mean ± SD)		CTL Group T1
(Mean ± SD)		p-Value
POC TA83% ≤ X ≤ 100%84.11 ± 6.12681.59 ± 8.6520.3892 a
POC MM83% ≤ X ≤ 100%80.44 ± 14.7877.62 ± 18.060.6236 a
POCSCM83% ≤ X ≤ 100%79.34 ± 9.39881.36 ± 9.9200.5125 a
BAR90% ≤ X ≤ 100%85.76 ± 7.07884.10 ± 5.3940.1703 a
TORS90% ≤ X ≤ 100%88.73 ± 4.36389.16 ± 3.1630.9025 a
IMP85% ≤ X ≤ 115%119.8 ± 99.9277.07 ± 29.880.2017 a
ASIM−10% ≤ X ≤ +10%0.4833 ± 15.425.073 ± 19.170.2496 a
Legend: POC TA: percentage overlapping coefficient of anterior temporalis muscles; POC MM: percentage overlapping coefficient of masseter muscles; POC SCM: percentage overlapping coefficient of sternocleidomastoid muscles; BAR: percentage overlapping coefficient of contact between posterior and anterior teeth; TORS: torsion index; IMP: impact index; ASIM: asymmetry index; SD: standard deviation; a: Mann–Whitney U test.
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Migliore, F.M.; Breda, L.; Di Maria, E.; Battestini, F.; Di Carlo, B.; D’Attilio, M. Clinical and Instrumental Temporomandibular Joint Evaluation in Children and Adolescents with Juvenile Idiopathic Arthritis: A Medium-Term Follow-Up. Appl. Sci. 2023, 13, 13036. https://doi.org/10.3390/app132413036

AMA Style

Migliore FM, Breda L, Di Maria E, Battestini F, Di Carlo B, D’Attilio M. Clinical and Instrumental Temporomandibular Joint Evaluation in Children and Adolescents with Juvenile Idiopathic Arthritis: A Medium-Term Follow-Up. Applied Sciences. 2023; 13(24):13036. https://doi.org/10.3390/app132413036

Chicago/Turabian Style

Migliore, Federica Maria, Luciana Breda, Erica Di Maria, Francesca Battestini, Beatrice Di Carlo, and Michele D’Attilio. 2023. "Clinical and Instrumental Temporomandibular Joint Evaluation in Children and Adolescents with Juvenile Idiopathic Arthritis: A Medium-Term Follow-Up" Applied Sciences 13, no. 24: 13036. https://doi.org/10.3390/app132413036

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