Prevalence of degenerative disease of the temporomandibular joint in anterior open bite patients with different molar relationships: a retrospective observational study

doi:10.21203/rs.3.rs-4922622/v1

Objectives: To assess the prevalence of degenerative disease of the temporomandibular joint in anterior open bite patients with different molar relationships.

Methods: 246 anterior open bite adult orthodontic patients were divided into Class I group (n=65), Class II group (n=116) and Class III group (n=65) based on their sagittal molar relationships, meanwhile, 70 normal subjects were selected as control group. The occurrence of degenerative joint disease was detected by cone beam computed tomography, and the prevalence of degenerative joint disease among groups was compared. Mandibular plane angle and the vertical distance between the upper and lower incisors were also measured.

Results: The overall prevalence of degenerative joint disease in anterior open bite patients and control group was 30.28% and 5.00%, respectively. Class II group showed the significantly highest prevalence of degenerative joint disease (50.43%, P＜0.001), highest frequency of bilateral degenerative joint disease (43.95%，P＜0.001) and highest mandibular plane angle. Among the anterior open bite groups, Class III group exhibited the highest vertical distance between the upper and lower incisors (3.35 ±1.86mm, P＜0.05) but the lowest prevalence of degenerative joint disease(10.77%).

Conclusions: For Class II anterior open bite patients, condylar resorption in degenerative diseases of TMJ may be an important cause of malocclusion.

Temporomandibular joint

Degenerative joint disease

Cone beam computed tomography

Anterior open bite

Molar relationship

Anterior open bite (AOB) patients with Class II molar relationship exhibit the highest incidence of degenerative disease of the TMJ (DJD) and largest mandibular plane angle.
Condylar resorption may be an important cause in Class II AOB patients.

Anterior open bite (AOB) is a challenging malocclusion defined as the absence of vertical contact between the maxillary and mandibular incisors during intercuspal position, with the prevalence of Chinese population varying between approximately 1.5% and 5%, depending on area, age and dentition [1]. Affected patients often show masticatory and phonatory dysfunctions and suffer from considerable facial aesthetic issues [2].

Multiple factors, such as sucking habits, skeletal discrepancy, molar overeruption and condylar resorption, have been implicated in the onset of AOB[1, 3, 4]. Finger sucking and tongue thrust may impede eruption of incisors by mechanical obstruction. Skeletal vertical discrepancy can also exacerbate the extent of AOB, with AOB patients showing an increase in the mandibular plane angle [5]. Moreover, condylar resorption in degenerative diseases of TMJ may lessen the ramus height, leading to a clockwise rotation of the mandible, increase in the front facial height and a class II molar relationship tendency, ultimately resulting in AOB [6, 7]. This issue is particularly pertinent in patients with idiopathic condylar resorption (ICR), a rare and aggressive degenerative disease of the TMJ, which shows condylar resorption and AOB in a short observation period [8, 9]. Given the specific mechanism of which AOB caused by TMJD etiology, Class II AOB patients seem to have a higher prevalence of DJD.

While the etiology of ICR remains unclear, its pathological manifestations exhibit substantially similarities to degenerative joint diseases (DJD), including condylar resorption, osteophytogenesis and subcortical cyst [10]. DJD manifests as a continuous pathological progression characterized by degraded resorption and reparative remodeling of the affected articular tissues, with an occurrence observed in 36.7% of the Chinese TMD population [11–13]. Because of the variability of its symptoms, CBCT is a mandatory examination for the diagnosis of DJD [10, 14]. Radiographically, erosion serves as an indicator of an active destructive process, while osteophyte suggests a stable stage. During the stable phase, the condyle has adapted to the altered condyle-fossa relationship and the presence of subchondral cyst(s) or generalized sclerosis may also be observed [15, 16].

Due to the complexity of AOB etiology, orthodontists should be prudent in treating AOB patients and differentiate the etiologic factor of TMJD in a specific clinic situation. Although several researches had been performed to explore the incidence of TMD in AOB individuals, revealing a higher frequency of TMD in AOB patients compared to general population [17–19], no studies have been conducted to explore the association between degenerative disease of TMJ and molar relationships in AOB patients.

Consequently, the objective of this investigation was to assess the prevalence of DJD in AOB patients with three types of molar relationships using CBCT. The researchers hypothesized that the prevalence of DJD was different in AOB patients with different molar relationships, and attempted to provide data support for TMD risk assessment in AOB orthodontic patients.

Ethical approval

This study was approved by the Ethics Committee at the Nanjing Stomatological Hospital, Affiliated Hospital of Medical School, Research Institute of Stomatology, Nanjing University, Nanjing, China [2019NL-064(KS)] on July 23, 2019. All participants provided written informed consent to participate in the study and for their data to be published.

Samples

The authors retrospectively reviewed patients who visited the (blinsded) seeking for orthodontic treatment and had completed pre-treatment examinations between July 2017 and December 2022. A total of 9875 participants’ study models were viewed for eligibility via Dolphin Imaging Software (Chatsworth, CA, Version 11.95), and the inclusion criteria of AOB patient were: (1) AOB, the vertical distance between the upper and lower incisors exceeds 0.5mm during intercuspal position; (2) Age over 18 years old; (3) Pre-treatment examination contains a CBCT of good quality with TMJ included in the field of view (FOV). The exclusion criteria were: (1) Damaged CBCT data with artifacts or distortion; (2) History of orthodontic treatment or anterior teeth restoration; (3) History of extra oral trauma, cleft lip, temporomandibular joint tumor and palate. Finally, 246 AOB patients were enrolled in this study, and the screening flow is shown in Fig.1. According to their molar relationships, 246 AOB patients were then divided into Class I group (n=65), Class II group (n=116) and class III group (n=65).

Furthermore, 70 normal subjects were selected as the control group according to the following inclusion criteria: (1) Age over 18 years old; (2) Normal anterior overjet and overbite in the intercuspal position; (3) Class I molar relationship with normal dentition alignment; (4) No history of orthodontic treatment or anterior teeth restoration; (5) No history of extra oral trauma, temporomandibular joint tumor, cleft lip and palate, or surgery in the craniofacial and joint region.

Sample size was calculated based on the study of Linda et al, which reported a prevalence of condylar degeneration of 27% for skeletal open bite and 8% for dental open bite [20]. The calculation was conducted by PASS software (Version 15.0, NCSS, LLC) with a power level (1-β) of 90% at a 5% significance level (α=0.05) and effect size (W=0.25), based on 1:1 ratio between groups, result showed that a total of 228 participants were needed and a total of 316 subjects participated in the present study.

Radiographic examination

All CBCT (NewTom VG, Italy) scans were obtained with the following radiological parameters: 110 kV, 25 mA, voxel size of 0.25 mm, 16 cm×16 cm field of view, exposure time of 20-25 seconds. Then, the CBCT volumetric data was import into the Dolphin Imaging 11.9 software (Chatsworth, Calif) in Digital Imaging and Communications in Medicine (DICOM) mode to evaluate of the joints’ CBCT images.

Two experienced radiologists performed all examinations and the detailed procedures were shown in Fig.2. Multi-layer reconstruction was performed on the axial image (AIm), coronal image (CIm) and sagittal image (SIm), with a slice interval and slice thickness of 0.5mm each. Evaluation was conducted to assess the presence of DJD according to the criteria used for radiographic diagnosis defined by the DC/TMD Validation Project [14]. Diagnosis can only be confirmed by simultaneous observation of images on two consecutive slices, TMJ degenerative changes include: erosion(s), osteophyte(s), subchondral cyst(s) or generalized sclerosis (Fig.3). The presence of any of the aforementioned changes in the radiographic image indicates DJD. In addition, we also evaluated the distribution of laterality of DJD，when DJD was present in both joints, the patient was classified as bilateral degenerative TMJ, when degenerative changes occurred on only one side, patient was classified as unilateral degenerative TMJ, and patient was classified bilateral normal TMJ if degenerative changes occurred in neither joint.

In order to ensure the impartiality and objectivity of the examination, we blinded the presence of AOB patients' molar relationships to the examiners. Two oral maxillofacial radiologists performed twice calibrations before examination. They evaluated a random selection of 30 TMJ images, and achieved a concordance rate over 80% in their examination results at the end of the second calibration. The calibration cases for AOB patients were not included in the 316 experimental CBCT series. Following the completion of the calibration phase, the examiners assessed each TMJ image presented in a randomized sequence for Class I, Class II, Class III and control group separately. The complete array of images was displayed on a singular monitor, and the assessment was executed by two calibrated examiners. In instances when the two evaluations yielded inconsistent results, a third senior and experienced maxillofacial radiologist was requested to deliver a conclusive verdict. Two weeks later, 75% of TMJs in the four groups were randomly selected for a second morphological evaluation by one of the examiners. Meanwhile, MP-SN angle, MP-FH angle and the vertical distance between the upper and lower incisors were measured on lateral cephalogram.

Statistical Analysis

The Cohen's kappa statistic was utilized to assess the inter-examiner reliability between the two examiners and the consistency of a single examiner's two evaluations in the DJD assessment. Intra-class correlation Coefficients (ICC) were employed to evaluate the reliability of the mandibular plane angle measurements. Chi-square was performed to test the differences of prevalence of DJD among the four groups. When the chi-square analysis revealed a significant difference among four groups, a Bonferroni-adjusted post-hoc pairwise test would be employed. For quantitative data, Kolmogorov-Smirnov test was applied to test the normality, one-way analysis of variance (ANOVA) and Tukey's post hoc test would be supplied if the variables satisfy the normal distribution, and non-parametric tests were used for non-normal distribution data. SPSS software (version 23; IBM, Armonk, NY) was used for statistical analyses and statistical significance was defined as p < 0.05.

The K value for the consistency of condyle morphological evaluation between two calibrated examiners is 0.769, and the K value evaluated by one of the examiners twice was 0.826. The ICC between two examiners for the measurement results of MP-SN, and MP-FH angles were 0.989 and 0.972, which indicated excellent reliability.

Basic characteristics of the subjects

A total of 246 AOB patients were consisted of 177 female (72.0%) and 69 male (28.0%) patients, and Class II Group of 116 subjects (47.15%) constitute the majority among AOB patients. A control group comprising 46 female (65.7%) and 24 male (34.3%) subjects was matched to AOB patients in terms of gender and age. No difference was found regarding the age distribution among four groups (P=0.199), whereas the proportion of males in Class III group was higher than that in Class I group and Class II group (P<0.001). (Table I)

Table I. Basic characteristics of AOB groups and control group

Group Variables		Class I group 65	Class II group 116	Class III group 65	Control group 70	*P-value*
Sex n(%)	Female	46(70.8%)	97(83.6%)	34(52.3%)	46(65.7%)	*<0.001^a**
	male	19(29.2)	19(16.4%)	31(47.7%)	24(34.3%)
	Total	65(100%)	116(100%)	65(100%)	70(100%)
Age(year)		24.77±6.39	23.66±5.58	22.57±4.18	23.66±4.2	0.199^b

^ap-value was determined using chi-square test;^bp-value was determined using Kruskal–Wallis test;

^*P < 0.05

Prevalence of DJD among four groups

The chi-square test indicated a statistically significant difference among the four groups concerning the frequency of DJD (P<0.001), including erosion (P<0.001), osteophyte (P<0.001), subchondral cyst (P=0.009) and generalized sclerosis (P<0.001). The incidence of DJD in the AOB group was significantly higher compared to the control group (30.28% vs. 5.00%; P<0.001). The results of the inter-groups comparison of AOB patients are presented below. The occurrence of DJD was higher in Class II group compared to both Class I and III group, and this difference was statistically significant (13.85% vs. 50.43% vs. 10.77%; P<0.001). For subtypes of DJD, pairwise post hoc tests adjusted by Bonferroni showed that the incidence of erosion and osteophyte in Class II group was significantly higher than that in Class I and III group (P<0.001), while no statistically significant differences were found between Class I and III group. (P=0.126, P=0.141). The incidence of generalized sclerosis in group II was significantly higher than that in group I (P=0.001), meanwhile, no significant difference were observed across the three AOB groups in terms of subchondral cyst. (Table II)

Table II. Frequency of DJD in Class I, II, III group and control group

Group Variables	Class I group 130	Class II group 232	Class III group 130	Control group 140	*P-value*	Pairwise post hoc tests with the Bonferroni adjustment
Group Variables	Class I group 130	Class II group 232	Class III group 130	Control group 140	*P-value*	I-C	II-C	III-C	I-II	I-III	II-III
erosion(s)	15(11.54%)	81(34.91%）	8(6.15%)	3(2.14%)	<0.001*	0.002*	<0.001*	0.096	<0.001*	0.126	<0.001*
osteophyte(s)	16(12.31%)	91(39.22%)	9(6.92%)	3(2.14%)	<0.001*	0.001*	<0.001*	0.057	<0.001*	0.141	<0.001*
subchondral cyst(s)	2(1.54%)	23(9.91%)	5(3.85%)	3(2.14%)	0.009*	1.000	0.004*	0.642	0.002*	0.387	0.038*
generalized sclerosis	0(0.00%)	18(7.76%)	3(2.31%)	0(0.00%)	<0.001*	1.000	0.001*	0.220	0.001*	0.245	0.033*
DJD	18(13.85%)	117(50.43%)	14(10.77%)	7(5.00%)	<0.001*	0.012*	<0.001*	0.077	<0.001*	0.450	<0.001*

p-value was determined using chi-square test; DJD Degenerative joint disease;

^*P < 0.05

Comparison of the extent of AOB and the mandibular plane angle

The vertical distance between the upper and lower incisors in Class III group was significantly greater than that in Class I (P=0.008) and II (P=0.005) group. Statistically significant differences were also observed in the mandibular plane angle between AOB group and control group (P<0.001). Class I group had an average MP-SN (°) of 39.03°±7.61° and MP-FH (°) of 32.25°±6.96°, Class II group had an average MP-SN (°) of 44.39°±7.02° and MP-FH (°) of 35.68°±6.74°, and Class III group had an average MP-SN (°) of 38.12°±8.25° and MP-FH (°) of 31.32°±8.11°. In Class II group, both MP-SN (°) and MP-FH (°) were significantly larger than both Class I group (P<0.001, P=0.007) and Class III group (P<0.001, P<0.001). (Table III)

Table III. Extent of AOB in the AOB groups and the mandibular plane angle in four groups

Group Variables	Class I group 65	Class II group 116	Class III group 65	Control group 70	*P-value*	Pairwise post hoc tests
Group Variables	Class I group 65	Class II group 116	Class III group 65	Control group 70	*P-value*	I-C	II-C	III-C	I-II	I-III	II-III
MP-SNA (°，mean±sd)	39.03±7.61	44.39±7.02	38.12±8.25	32.69±5.91	*<0.001^a**	<0.001*	<0.001*	<0.001*	<0.001*	0.89	<0.001*
MP-FHA (°，mean±sd)	32.25±6.96	35.68±6.74	31.32±8.11	26.57±5.34	*<0.001^a**	<0.001*	<0.001*	<0.001*	0.007*	0.86	<0.001*
ULD (mm)	2.39±1.19	2.48±1.32	3.35±1.86	-	*0.002^b**	-	-	-	1.00	0.008*	0.005*

^ap-value was determined using One-way analysis of variance (ANOVA) ; ^bp-value was determined using Kruskal–Wallis test; SD: Standard deviation; ULD: vertical distance between the upper and lower incisors;

^*P < 0.05

Comparison of the distribution of laterality of DJD

Bilateral DJD occurred in 8 of the 65 AOB patients in Class I group (12.31%), 51 of the 116 patients in Class II group (43.95%), 6 of 65 patients in Class II group (9.23%) and 1 of 70 patients in control group (1.43%). The distribution of the frequency of laterality of DJD among the four groups was significantly different, and Post hoc analysis revealed that the frequency of bilateral DJD was significantly higher in the Class II group than in other three groups (P < 0.001). (Table IV)

Table IV. Distribution of laterality of DJD among subjects

Group variables	Class I group	Class II group	Class III group	Control group	P-value
Bilateral degenerative TMJ	8(12.31%)	51(43.95%)	6(9.23%)	1(1.43%)	<0.001*
Unilateral degenerative TMJ	2(3.08%)	12(10.33%)	2(3.08%)	5(7.14%)
Bilateral normal TMJ	55(84.61%)	52(44.82%)	57(87.69%)	64(91.43%)
Total	65(100.00%)	116(100.00%)	65(100.00%)	70(100.00%)

p-value was determined using chi-square test;

^*P < 0.05

Function, aesthetics, and balance are the ultimate goals of orthodontic treatment. The health and stability of the temporomandibular joint has a crucial impact on orthodontic treatment. As hypothesis, the present study clearly showed that AOB patients with distal occlusion had the highest incidence of DJD among the three AOB groups. This phenomenon can be explained by the pathogenesis of Class II AOB. Temporomandibular joint degenerative disorders lead to the decrease in mandibular ramus height, causing clockwise rotation of the mandible and consequently resulting in AOB and Class II molar relationship [21].

Other explanations for the different incidence of DJD in AOB patients with different molar relationships are the varying craniofacial structures and joint loading. Studies found that AOB patients with different sagittal jaw relationships showed various skeletal morphologies [22, 23]. Joint loading is a critical factor that influences the health of the TMJ [24]. The shape and function of TMJ is closely related and TMJs with different shapes have various joint pressures, which can be influenced by occlusion characteristics [25-27]. Compared to Class II patients, Class III patients tend to have a wider and flatter glenoid fossa [28]. AOB patients with different molar relationships can potentially impact the morphology and pressure within the TMJ, thereby resulting in varying rates of DJD incidence. Moreover, Class II malocclusion may also be a risk factor for TMD. Skeletal Class II has a high possibility of TMJ disk displacement and osteoarthrosis in normal population [29-31].

Identifying the etiology of AOB and selecting the optimal timing for treatment are crucial to orthodontic management. If AOB patient has a history of TMD and is accompanied by a Class II molar relationship, it should be considered that the AOB may be caused by ICR or other degenerative diseases of the temporomandibular joint. Moreover, the patient's bite, mandibular posture, and facial pattern are also worthy of attention, as a persistent decrease in overbite, mandibular retraction and dolichofacial pattern may indicate the occurrence of condylar resorption [32].

Analysis of the subtype of DJD in AOB patients showed a higher incidence of osteophyte compared to erosion, indicating that patients seeking orthodontic treatment may be in a stable phase. On imaging, erosion images indicate that TMJ is in the active phase of DJD, during which the TMJs are particularly sensitive to biomechanical pressure, and patients may suffer pain, limited condylar movement and other TMJ symptoms [33]. In the active period, joint load caused by orthodontic treatment can aggravate the resorption of articular fibrocartilage and underlying subchondral bone [34].

For Class II AOB patients caused by ICR, orthodontic treatment should be postponed until the stable phase is reached. However, assessing the stability of ICR based solely on clinical symptoms is highly unreliable, as even during active condylar resorption stage, only about 25% of patients suffer symptoms such as pain or dysfunction [35, 36]. Thus, conducting imaging examination such as CBCT to complement the clinical evaluation for determining the optimal timing of treatment is essential. Hatcher et al. recommend conducting a radiographic reevaluation 6-12 months after the appearance of end-stage imaging (osteophytes and sclerosis). Orthodontic treatment should proceed once the TMJ components' volume, shape, and quality remain stable [34].

The incidence of DJD in the control group was 5.00%, which was consistent with previous study results of 5.2% [37]. It is worth noting that the overall incidence rate of DJD in AOB patients in this study was 30.28%, exceeding the result studied by Phi, L. et al. (18.8%) [20]. The disparity in findings may be attributed to two reasons: The first reason is the differences in the occurrence rates of TMD between Asian and Western populations. The second may be the difference of the scanning parameters and observation methods utilized in two studies. In this study, scans were conducted at a slice thickness of 0.5mm, with observation of all sections, while in Phi's research, they only tested ten sections of the TMJ, with each slice measuring 1mm in thickness.

A high mandibular plane angle is characterized by open-bite skeletal patterns while a low mandibular plane angle by closed-bite skeletal patterns [38]. Among the three groups of open bite patients, Class II group showed the highest mandibular plane angle and incidence of DJD, which consistent with the study conducted by Phi. et al [20]. A high mandibular plane angle can be considered as one of the etiological factors contributing to the occurrence of DJD in AOB patients.

Patients with bilateral degenerative TMJ present a decreased ramus height, downward and backward rotation of the mandible, class II tendency, and AOB with high mandibular plane angle. When unilateral joint degeneration occurred, mandibular deviation and facial asymmetry usually be observed [35]. AOB patients with Class II molar relationship showed a significantly higher frequency of bilateral DJD in the present study. The authors speculated that in partial Class II patients, the AOB is a consequence of bilateral condylar resorption.

Research has shown that females are more susceptible to TMJ disorders than males in the general population [39]. In this study, Class III AOB patients showed the lowest proportion of female and the lowest incidence of DJD, which consisted with previous studies, moreover, it is possible that Class II AOB patients may exhibit a higher incidence of DJD due to the higher proportion of females in this group. Study indicated that the severity of open bite can significantly influenced the condyle position and TMJ morphology [40]. Patients with different severity of open bite may exhibit various incidence of DJD due to their different TMJ morphology. However, the results of this study showed that the Class III group presented the highest severity of AOB, yet the lowest incidence of DJD. This suggests that the extent of open bite does not necessarily exacerbate the joint symptoms experienced by patients.

Limitations

Despite the present study indicates a higher incidence of DJD in Class II AOB patients, this retrospective study has some limitations. (1) There may exist selection bias: patients presenting to hospital may have a higher incidence of DJD than that observed in patients with AOB in the general population. (2) The specific reasons for the higher incidence of DJD in Class II AOB patients remain unclear, factors such as TMJ morphology, maxillofacial morphology, bite force as well as condylar motion may all have an impact on the TMJ health. Further research studies are required to determine whether the above factors affect the occurrence of DJD in AOB patients, so as to deepen our understanding of TMD in AOB patients, control the risk more scientifically and accurately, and improve the success rate and stability of AOB treatment.

Class II AOB patients exhibit the highest incidence of DJD and largest mandibular plane angle. Condylar resorption in degenerative diseases of TMJ may be an important cause in Class II AOB patients. The results of the present study emphasized the importance for orthodontists to implement routine imagining examinations (CBCT or comparable imaging) to assess TMJ status and rule out potential undesirable risks before initiating any treatment for Class II AOB patients.

CBCT: Cone beam computed tomography; DJD: Degenerative joint disease; TMJ: Temporomandibular joint; TMD: Temporomandibular joint disease; AOB: Anterior open bite; ULD: Vertical distance between the upper and lower incisors; MP-SN: The angel between mandibular plane to cranial base (sella nasion); MP-FH: The angle between the mandibular plane and the Frankfort plane; ICR: Idiopathic condylar resorption; AIm: Axial image; CIm: Coronal image; AIm: Sagittal image; ICC: Intra-class correlation coefficients; ANOVA: One-way analysis of variance

Ethics Declarations

This study was reviewed and approved by the Ethics Committee at the Nanjing Stomatological Hospital, Affiliated Hospital of Medical School, Research Institute of Stomatology, Nanjing University, Nanjing, China with the approval number: [2019NL-064(KS)], dated [July 23, 2019]. All participants provided written informed consent to participate in the study and for their data to be published.

Authors' contributions

Chenxu Wang: Conceptualization; Data curation; Formal analysis; Investigation; Methodology; Project administration; Software; Supervision; Visualization; Roles/Writing - original draft; and Writing - review & editing. Feng Guo: Project administration; Software; Supervision; and Visualization. Hengyu Hu: Data curation; Formal analysis; Investigation; and Software. Chenghuan Liu: Data curation and Formal analysis. Lang Lei: Conceptualization; Funding acquisition; Investigation; Methodology; Resources; Supervision; Validation; and Writing - review & editing.

Funding statement

This work was supported by the Natural Science Foundation of China (number 82371007); and the China Oral Health Foundation-Smiling Children (Adolescent growth and oral health prevention and treatment) Grant.

Declaration of competing interest

The authors declare that they have no known competing financial interests or personal relationships that could have appeared to influence the work reported in this paper.

Data availability statement

The datasets used and analyzed during the current study are available from the corresponding author on reasonable request.

Acknowledgements

Not applicable.

Disclosure statement

The authors report there are no competing interests to declare.

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No competing interests reported.

Prevalence of degenerative disease of the temporomandibular joint in anterior open bite patients with different molar relationships: a retrospective observational study

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