Association between clinical manifestations of occlusal trauma and magnetic resonance imaging findings of periodontal ligament space

Abstract

Objectives:

The purpose of this study was to evaluate the association between clinical manifestations of occlusal trauma of the teeth and maximum signal intensity of periodontal ligament space on MRI.

Methods:

20 subjects (males: 9, females: 11, mean age: 35.9 ± 14.0 years, range: 22–65 years) participated in this study. Subjective symptoms of bruxism, tooth mobility, fremitus, occlusal contact area, occlusal force, widening of the periodontal ligament space, and thickening of the lamina dura were defined as clinical manifestations of occlusal trauma. The total number of clinical manifestations was used to evaluate the degree of clinical occlusal trauma, with a score of 7 indicating the highest degree of occlusal trauma. The maximum signal intensity in the periodontal ligament space was evaluated by a specific T ₂ weighted MRI sequence: IDEAL image.

Results:

Spearman’s rank correlation between the total clinical occlusal trauma score and maximum signal intensity in the periodontal ligament space was 0.529 for all teeth, 0.517 for anterior teeth, and 0.396 for molar teeth (p < 0.001 for all).

Conclusions:

A significant correlation between the degree of occlusal trauma and the signal intensity of the periodontal ligament space suggests a new potential MRI-based method for objectively determining occlusal trauma.

Introduction

Occlusal trauma is defined as “an injury to the attachment apparatus as a result of excessive occlusal forces”. ¹ It is incumbent on the clinician to detect, diagnose, and treat trauma from the occlusion to stabilize the dentition. The effect of occlusal trauma on dental supporting tissues is still debated.

Fan and Caton reported a narrative review of occlusal trauma in 2018. ² Because trauma from the occlusion is defined and diagnosed on the basis of histologic changes in the periodontium, a definitive diagnosis of occlusal trauma is not possible without a block section biopsy. Consequently, multiple clinical and radiographic indicators are used as surrogates to assist in the presumptive diagnosis of occlusal trauma. Clinical diagnostic findings of occlusal trauma may include progressive tooth mobility, fremitus, occlusal discrepancies/disharmonies, wear facets (caused by tooth grinding), tooth migration, tooth fracture, thermal sensitivity, root resorption, cemental tear, and widening of the periodontal ligament space upon radiographic examination. ^3,4

Even though it is difficult to diagnose the presence and the real clinical impact of a traumatic occlusion, there is no question that aspects of occlusal therapy have an empirical base. Furthermore, ethical reasons prevent researchers from conducting prospective clinical trials. ⁵

In a survey conducted in 2018 of 2,330 people, the most common cause of tooth extraction among Japanese was periodontal disease (37.1%), followed by dental caries (29.2%), and then tooth or root fracture (17.8%). Fractures are strongly influenced by occlusal conditions. ¹ Occlusal trauma of the teeth is a term used to describe injury resulting in tissue damages within the attachment apparatus of the teeth, including periodontal ligament, supporting alveolar bone and cementum, as a result of occlusal force. ⁶ Moreover, occlusal trauma has also been associated with periodontitis, an inflammatory disease caused by plaque. ^7–9

Previous studies reported that even in the early stages of excessive occlusal force, the periodontal tissues already show cementum and alveolar bone resorption and an enlarged periodontal ligament in the cervical region and root apices, and that persistent jiggling force causes alveolar bone resorption in the cervical region and root apices even when the periodontal tissues are normal. ^10,11 In a recent study of occlusal trauma, ischemia of the adherent gingiva during clenching was measured using a non-contact laser Doppler velocimetry. ¹²

Edema was reported to occur in the periodontal ligament space of traumatically occluded teeth. ¹¹ MRI can detect the presence of edema sensitively. Because T₂ weighted MRI can produce water image, it was applied for the diagnosis of early stage of osteomyelitis of the jaws and joint effusion of temporomandibular disorder in the maxillofacial region. ^13,14 However, to the best of our knowledge, its application to periodontal disease is limited to the study by Schara et al. ¹⁵ Evaluation of occlusal trauma in clinical practice is limited to clinical manifestations in the use of articulating paper or palpation of fremitus, and its intensity has not been quantified precisely. Quantification of occlusal trauma would allow for more precise occlusal adjustments. No previous studies have quantified and evaluated occlusal trauma using the signal intensity in the periodontal ligament space on MRI examination.

The purpose of this study, therefore, was to evaluate the association between clinical manifestations of occlusal trauma and maximum signal intensity of the periodontal ligament space on MRI. Additionally, this study examined whether MRI can be used to detect teeth that have undergone early-stage occlusal trauma.

Methods

Subjects

This investigation was performed as a cross-sectional observational study. 20 subjects (males: 9, females: 11, mean age: 35.9 ± 14.0 years, range: 22–65 years), including 10 patients who visited the Department of Periodontology, Matsumoto Dental University Hospital with a chief complaint of bruxism and 10 volunteers who were aware of their bruxism, participated in the study. The selection criteria for this study were: all probing depth (PD) <4 mm without a single site of BOP, at least 20 teeth present except third molars, no dental irregularities, and normal occlusal relationship between upper and lower jaws. In addition, the following conditions were considered to be contraindicated for MRI examinations: claustrophobia, difficulty in maintaining posture for long periods of time, impaired spontaneous breathing, impaired thermoregulation, and pregnant women, ¹⁶ long-span bridges, metal implants, and orthodontic devices. The study protocol of this investigation was reviewed and approved by the ethics committee of the Matsumoto Dental University (No. 0138) and was carried out in accordance with the principles of the Declaration of Helsinki. Comprehensive written informed consent was provided by all patients enrolled in this study.

Oral health examination

The oral health status of the subjects was recorded by one dentist with over 30 years of experience. Subjects were asked whether or not they had subjective symptoms of bruxism (discomfort and pain in the mouth upon awakening and during occlusion), and the degree of tooth mobility was assessed (0: within physiological range, 1: buccolingual movement within 1 mm, 2: mediodistal movement within 1 mm, 3: vertical movement). ¹⁷ Fremitus, which is a palpable or visible movement of a tooth when subjected to occlusal forces, ¹ was evaluated in all teeth (0: no concussion palpable in habitual occlusion or in any of the lateral movements, 1: concussion felt in habitual occlusion or in the lateral movements, 2: concussion palpable in both habitual occlusal position and lateral movement). ³ PD was assessed at six points around all teeth using a periodontal probe (CPUNC 15, Hu-Friedy, Chicago, IL) and recording the presence of bleeding on probing (BOP) to rule out chronic inflammation in all teeth. The occlusal contact area and the occlusal force were measured using the Occluser^® (FPD-707, GC Corporation, Tokyo, Japan) and the Dental Prescale^® (50 H, type R, GC Corporation, Tokyo, Japan) respectively. The headrest was adjusted so that the Frankfurt plane of the head was perpendicular to the floor. The subjects marked their bites at maximum occlusal force for 3 sec. The marking was then analyzed with the Occluser^®. The occlusal contact area and occlusal force were calculated by dividing the contact points for each tooth using the close-up function of the Occluser^®. These values were compared with the previous results ^18–20 ; values exceeding those of healthy teeth were evaluated as having excessive occlusal contact area and occlusal force.

Radiographic examination

Intraoral dental radiographs of all teeth were obtained using a DIGORA^® Optime (Soredex Orion Corp., Tuusula, Finland). The imaging parameters were as follows: tube voltage 70 kVp, tube current 10 mA, and exposure time (changed for each site) 0.03 to 0.8 s. The X-ray tube, subject, and imaging plate were positioned as close as possible to the same position using the CID-3 film holder (Hanshin Technical Laboratory, Nishinomiya, Japan). Intraoral dental radiographs of all teeth were taken by the bisected angle technique. One trained dentist with over 30 years of experience (different from the dentist who performed the clinical evaluation) read the images while blinded to the results of the clinical evaluations and assessed the presence or absence of widening of periodontal ligament space and thickening of the lamina dura.

Evaluation of clinical occlusal trauma

Based on the results of the intraoral examination and dental radiographs, the following seven findings were defined as clinical manifestations of occlusal trauma: (1) subjective symptoms of bruxism, (2) tooth movement, (3) fremitus, (4) excessive occlusal contact area, (5) excessive occlusal force, (6) widening of the periodontal ligament space, and (7) thickening of the lamina dura with reference to the narrative review of occlusal trauma by Fan and Caton. ² The number of clinical manifestations was totaled to evaluate the degree of clinical occlusal trauma, with a score of 7 indicating the highest degree of occlusal trauma.

MRI examination

An MRI system (Signa HDx^® 1.5T, GE Healthcare UK Ltd., Amersham, UK) at Matsumoto Dental University Hospital was used for the MRI examinations. Two 3-inch 2-channel surface coils for temporomandibular joint imaging were used and placed close to the subject’ s bilateral cheeks to minimize image quality degradation due to air and other intervening factors (Figure 1). For accurate slice positioning, T ₁ weighted images were taken in three directions (occlusal, sagittal, and coronal planes). T ₂ weighted water imaging with an iterative decomposition of water and fat with echo asymmetry and least-squares estimation (IDEAL) was performed to evaluate the signal intensity of the periodontal ligament space with the following parameters: TR 2,500 ms; effective TE 107 ms; matrix 256^*256; field of view 24 cm; section thickness 5.0 mm; intersection gap 1.0 mm; receiver bandwidth 30 Hz; flip angle 90°; and imaging time 4 min 33 s.

Figure 1.

Three inches 2-channel surface coil and setting to the subject. (a) Detailed images can be acquired within a 3-inch circle. (b) Positioning of the coil for periapical imaging. The coil was positioned as close as possible to the buccal area of the subject.

The occlusal plane was determined by translating the plane connecting the subnasal point and the upper margin of the auricle (Camper plane) on the MR image to a position including the most proximal point where the occlusal surfaces of the maxillary first molars contacted. The evaluation plane was set parallel to the occlusal plane 12 mm closer to the root apex than the occlusal plane because the slice thickness and slice interval were set in units of 6 mm to ensure image quality for evaluation (Figure 2a).

Figure 2.

MRI image. (a) Positioning of imaging range by T ₁ weighted images. (b) Image of the mandible obtained by the IDEAL method. (c) Image obtained by extracting only the periodontal ligament equivalent based on the image in b.

Image analysis

The MRI images were analyzed using Photoshop^® (CS3, Adobe Systems Inc., San Jose, CA). Only the periodontal ligament equivalent areas of the upper and lower jaws were extracted from the evaluation plane at the full circumference of the root (Figure 2b and c), and the 256 grayscale values of the area were measured pixel by pixel as the signal intensity. Analysis was performed one tooth at a time, and the highest signal intensity of the pixel for each tooth was used as the maximum signal intensity.

Statistical analysis

The association between the clinical evaluation and maximum signal intensity was determined using Spearman’s rank correlation. The evaluation points and mean maximum signal strength were also analyzed using the Kruskal–Wallis test and the Mann–Whitney U test as a post-test. A p-value < 0.05 was regarded as indicative of statistical significance. SPSS ver. 18.0 (IBM Japan, Tokyo, Japan) was used for the analyses.

Results

Subjects

There were 20 subjects, 9 males and 11 females. The mean weight was 62.4 ± 10.9 kg (range: 47–90 kg). The mean number of teeth per subject was 27.3 ± 1.2 (range: 24–28 teeth, excluding third molars). Although some subjects had missing teeth or congenitally deficient teeth, no subjects had dental malpositioning (Table 1).

Table 1.

Characteristics of the subject

	Mean ± SD, N (%)	Range
Age (years)	35.9 ± 14.0	22－65
Gender
Male	9 (45%)
Female	11 (55%)
Weight (kg)	62.4 ± 10.9	47－90
Number of present teeth (teeth)	27.3 ± 1.2	24－28

SD, standard deviation.

Clinical manifestations of occlusal trauma of the teeth

Occlusal trauma was observed in all 20 subjects by clinical examination and intraoral dental radiographs. Clinical condition of the periodontal tissues revealed no areas of PD ≥4 mm or BOP in all subjects. Clinical scores for occlusal trauma were 0: 90 teeth (16.4%), 1: 143 teeth (26.2%), 2: 113 teeth (20.6%), and 3: 126 teeth (23.1%). In the anterior and molar teeth, a high percentage of the subjects scored between 0 and 3 (Table 2). Clinical scores ranged from 0 to 4 points for anterior teeth and from 0 to 6 points for molars.

Table 2.

Clinical scores of occlusal trauma by tooth type

	No. of present teeth (teeth)	Clinical scores of occlusal trauma (point)
		0	1	2	3	4	5	6	7
Central incisor	80	29	24	13	13	1	0	0	0
Lateral incisor	75	23	30	14	7	1	0	0	0
Canine	80	21	31	14	11	3	0	0	0
Subtotal of anterior teeth	235	73	85	41	31	5	0	0	0
First premolar	80	9	22	22	17	9	1	0	0
Second premolar	77	3	11	18	27	14	3	1	0
First molar	80	2	16	14	30	9	7	2	0
Second molar	74	3	9	18	21	15	6	2	0
Subtotal of posterior teeth	311	17	58	72	95	47	17	5	0
Total	546	90	143	113	126	52	17	5	0

No. of present teeth; Number of present teeth.

MR image analysis and the correlation coefficient between score of clinical occlusal trauma and maximum signal intensity

The mean maximum signal intensity for the whole jaw was 49.6 ± 11.8, 45.1 ± 9.7 for anterior teeth and 53.0 ± 11.9 for molars in the maxilla and mandible (Table 3). Teeth with high scores in the clinical assessment of occlusal trauma also had higher maximum signal intensity on MRI examination. The mean maximum signal intensity of MRI for each of these clinical occlusal trauma scores was 0: 40.0 ± 5.9, 1: 46.7 ± 8.8, 2: 49.6 ± 9.9, 3: 53.3 ± 11.9, 4: 57.6 ± 12.0, 5: 65.7 ± 15.8, 6: 73.4 ± 1.5, indicating that the mean maximum signal intensity increased with higher scores (Figure 3). Comparing anterior and molar teeth, the scores for anterior teeth were 0: 39.5 ± 6.1, 1: 46.2 ± 9.1, 2: 47.9 ± 9.7, 3: 51.9 ± 11.4, and 4: 57.6 ± 8.0, respectively (Figure 4), and for molars: 0: 42.2 ± 4.2, 1: 48.6 ± 8.4, 2: 50.6 ± 10.0, respectively (Figure 5). The mean maximum signal intensity increased with increasing clinical evaluation scores for both anterior and posterior teeth (Figure 4 and 5).

Table 3.

Maximum signal intensities by tooth type on MRI

	Mean	SD
Central incisor	44.1	10.2
Lateral incisor	45.4	10.0
Canine	45.9	9.0
Subtotal of anterior teeth	45.1	9.7
First premolar	49.8	9.6
Second premolar	53.0	13.2
First molar	55.3	12.5
Second molar	53.9	12.5
Subtotal of posterior teeth	53.0	11.9
Total	49.6	11.8

SD, standard deviation.

Figure 3.

Clinical scores of occlusal trauma and mean maximum signal intensities (All teeth). Mean ± standard deviation, ＊＊: p < 0.01, ＊＊＊: p < 0.001

Figure 4.

Clinical scores of occlusal trauma and mean maximum signal intensities (Anterior teeth). Mean ± standard deviation, ＊＊: p < 0.01, ＊＊＊: p < 0.001

Figure 5.

Clinical scores of occlusal trauma and mean maximum signal intensities (Posterior teeth). Mean ± standard deviation, ＊＊: p < 0.01, ＊＊＊: p < 0.001

Spearman’s rank correlation (ρ) between clinical occlusal trauma scores and maximum signal intensity on MRI was 0.529 for all teeth, 0.517 for anterior teeth, and 0.396 for molar teeth, all showing significant correlation (p < 0.001). Regarding the association between the evaluation points of clinical occlusal trauma and mean maximum signal intensity, the results of the Mann–Whitney U test showed no significant difference in the five combinations of 1 and 2 points, 2 and 3 points, 3 and 4 points, 4 and 5 points, and 5 and 6 points for all the teeth; however, significant differences were observed in all other combinations (p < 0.05, Figure 3). In the analysis of anterior teeth only, four combinations (1 and 2 points, 2 and 3 points, 2 and 4 points, and 3 and 4 points) were not significantly different, and in the analysis of molars only, six combinations (1 and 2 points, 1 and 3 points, 2 and 3 points, 3 and 4 points, 4 and 5 points, and 5 and 6 points) were also not significantly different. However, all other combinations showed significant differences (p < 0.05, Figures 4 and 5).

Discussion

The significant correlation between clinical assessment of occlusal trauma and maximum signal intensity of the periodontal ligament on MRI examination suggests the possibility of a new MRI-based method of examining occlusal trauma. Ariji et al reported the evaluation of edema of the masseter muscle during sustained biting using the IDEAL method. ²¹ In this study, the IDEAL method used by Ariji et al was also applied to delineate edema of periodontal ligament tissue. ²¹ In this study, we modified these conditions to be suitable for periodontal tissue imaging and to obtain good image quality in the shortest possible time.

The clinical evaluation scores for occlusal trauma ranged from 0 to 4 points in the anterior teeth (mostly one point), and from 0 to 6 points in the molars (mostly 2 and 3 points) among the molars. The mean maximum signal strength was 45.1 for the anterior teeth and 52.9 for the molars. The higher degree of occlusal trauma in the molars compared with the anterior teeth may be due to the higher occlusal pressure in the molars resulting from their structure and function. ²² However, the correlation coefficients for molars were slightly lower than those for anterior teeth and all teeth. The reason may be that the maximum signal intensity for each evaluation point of clinical occlusal trauma in molars was distributed over a wide range for evaluation points 3 and above, and the standard deviation for evaluation point 5 was larger than that for other evaluation points. In the future, the number of teeth should be increased to eliminate these problems and to make the data more statistically significant when establishing the standard values. Additionally, by examining subjects with a variety of pathological conditions, it was necessary to closely examine teeth with a clinical score of 6 or higher, of which there were few.

Currently, the methods used to assess clinical occlusal trauma are mainly qualitative assessments. ^3,4,17,23,24 This is because the pathophysiology of occlusive trauma is complex and the clinical manifestations are diverse, making it difficult to integrate and weight them. In this study, a clinical evaluation method was devised to integrate the number of findings thought to be caused by occlusal trauma and to classify the severity of occlusal trauma, which was clinically evaluated.

Although there are severity classifications for tooth sway and fremitus, the degree of classification is not proportional to the degree of occlusal trauma. ^3,24 Kundapur et al reported the evaluation of occlusal trauma in order to simplify the qualitative evaluation of tooth sway and fremitus. In the present study, similarly, the presence or absence of tooth movement and the presence or absence of fremitus were evaluated. ²⁴

The first limitation of this study was that, by examining subjects with various pathological conditions, close examination of teeth with a clinical evaluation point of 6 or higher was required, and the number of teeth in this category was particularly small. For this purpose, the subjects of this study should be observed to analyze whether the subjects who showed signal intensity above the standard value later exhibit clinical signs and whether the signal intensity changes at that time. The correlation between the maximum signal intensities of MRI and the digital occlusal force measuring device in this study has not been analyzed and will be discussed in a future study. Second, although the presence of plaque is associated with occlusal trauma, this study did not examine plaque adhesion. Third, because of the wide age range of the participants and because those with 20 or more teeth tend to be younger, we plan to increase the number of participants and conduct analysis by age in future research. The subjects of this study were selected only for subjective symptoms of bruxism, i.e. patients with asymptomatic occlusal trauma were not included. In addition, when adapted to cases of more severe occlusal trauma, the subjects in this study did not count symptoms in serious cases such as root fracture, which may lead to a larger error rate. Fourth, this method cannot be used in patients with contraindications to MRI. Additionally, patients with vascular stents, artificial joints, dental implants, and orthodontic appliances cannot undergo MRI if these prostheses cannot be removed. Although we did not calculate signal-to-noise ratio in this study, IDEAL compared favorably with fat-suppressed spoiled gradient-echo imaging, with high reproducibility. ²⁵ In future studies, we would like to further increase the sample size and analyze signal-to-noise ratio.

The strength of this study is that the presence of individual test teeth with signal intensities that exceeded the mean plus standard deviation in their clinical occlusal trauma scores may be the result of only increased edema of the periodontal ligament and high signal intensity, although the clinical manifestations were not marked. In other words, our results suggest that the presence of early occlusal trauma may be inferred even in the absence of clinical manifestations. Until now, traumatic occlusion could not be detected by us without intraoral dental radiographic findings, tooth movement, or plexus. Current occlusal treatment should not be prophylactic in principle, because removal of teeth in cooperative contact with other teeth may result in new premature contacts. ^26–29 However, in this study, it is possible to perform prophylactic occlusal treatment on the subject teeth with signal intensities greater than the MRI signal intensity standard value. For this purpose, it is necessary to follow the progress of the subjects imaged in this study and analyze whether the clinical manifestations of the subject teeth with signal intensities higher than the reference value in this study become apparent, and whether the signal intensity changes at that time.

Since this method uses MRI, there is no X-ray exposure, and compared to clinical examinations and intraoral dental X-ray examinations, it is possible to express the state of the periodontal ligament numerically in a more concrete manner. Furthermore, since changes in the condition of the periodontal ligament can be detected even in teeth without obvious clinical manifestations, it is suggested that this method can lead to early detection and early treatment of occlusal trauma. In order to improve the accuracy and reliability of this method, we plan to conduct more detailed analysis of the clinical examination while testing the method on subjects with various pathological conditions.

In conclusion, there was a significant correlation between the total clinical occlusal trauma scores and the maximum signal intensity of the periodontal ligament space. T ₂ weighted IDEAL water imaging is a promising method for the rapid evaluation of the morphologic and physiologic characteristics of the periodontal ligament space. Future studies of patients with occlusal trauma are necessary to validate this technique.