Assessment of the relationship between tooth inclination and gingival and alveolar bone dimensions using computed tomography of the maxillary anterior teeth: a cross-sectional study

ABSTRACT Objective: The present study aimed to investigate the relationship between tooth inclination and gingival and bone dimensions in maxillary anterior teeth. Methods: This cross-sectional study included cone-beam computed tomography (CBCT) images of 160 maxillary anterior teeth (30 individuals). Tooth inclination, gingival and bone thickness, and distances from cementoenamel junction to alveolar bone crest and gingival margin were measured in the labial surface. The correlations were analyzed using Pearson and partial correlation tests (p≤0.05). Results: In the central incisors, tooth inclination was positively and significantly related to apical bone thickness (R = 0.34, p= 0.001). In the canines, tooth inclination was negatively and significantly related to cervical bone thickness (R = - 0.34, p= 0.01) and positively associated to apical bone thickness (R = 0.36, p= 0.01) and to gingival margin-cementoenamel junction distance (R = 0.31, p= 0.03). In the lateral incisors, tooth inclination was not associated with gingival or bone dimensions. Conclusions: In the central incisors, the greater the labial tooth inclination, the greater is the apical bone thickness. In the canines, the greater the labial tooth inclination, the smallest is the cervical bone thickness, the greater is the apical bone thickness, and the greater is the gingival margin. Gingival and bone dimensions should be assessed when planning orthodontic treatment involving buccal movement of central incisors and canines.


INTRODUCTION
Understanding the factors that determine gingival and alveolar bone thickness is crucial for successful orthodontic, periodontal, and prosthodontic therapies. Many factors have been suggested to affect gingival and alveolar bone thickness in individuals with a healthy periodontium, such as age and sex; facial growth pattern; tooth shape; and events that occur during tooth eruption, including tooth inclination. [1][2][3][4][5][6][7][8] However, the impact of tooth inclination on gingival and alveolar bone thickness remains poorly understood. While some studies have reported that inclination or protrusion of the incisors is not related to gingival and bone thickness, others have observed an association between these factors. [9][10][11][12][13][14][15][16] These controversial results may be attributed to differences and limitations in the methods used to measure tooth inclination, as well as gingival and alveolar bone dimensions.
Tooth inclination has been evaluated using lateral cephalometry or cone-beam computed tomography (CBCT). [9][10][11][12][13][14][15][16] However, lateral cephalograms only allow evaluation of the maxillary and mandibular central incisors. Overlap between images of the right and left sides is another limitation. On the other hand, when measurements are made on the sagittal slice of CBCT images, there is no overlap of structures, and the buccolingual inclination of each tooth can be measured. Three previous studies evaluated the association between periodontal tissue Montanha-Andrade K, Crusoé-Rebello IM, Barreto M, Neves FS, Santos JN, Cury PR -Assessment of the relationship between tooth inclination and gingival and alveolar bone dimensions using computed tomography of the maxillary anterior teeth: a cross-sectional study 5 dimensions and tooth inclination measured on the sagittal slice of CBCT images. From these, two studies showed that retroclined maxillary central incisors have thinner supporting bone, while the other study found that proclined maxillary central incisors have greater apical bone thickness. 13,14,16 Another study investigated the association between the inclination of all teeth and alveolar bone thickness (BT) in adults with Class III dentofacial deformities, compared to Class I 7 . This study showed that Class III group exhibited greater buccolingual inclination and thinner alveolar bone at the cervical and apical levels than the group with normal occlusion, although the correlation was weak. 7 Another study did not measure BT, but assessed dehiscence and fenestration, and found that tooth inclinations were not related with the frequency of dehiscence. 17 Gingival thickness (GT) has been assessed by means of many methods, including the transparency of the periodontal probe, ultrasonic devices, transgingival probes, and CBCT. Periodontal probe transparency through the free gingiva discriminates between thin and thick biotypes; 18 however, this method does not quantify gingival thickness. Ultrasonic devices are not reliable when GT is >0.5 mm, [18][19][20] while transgingival probes necessitate invasive measurements. 20 In contrast, CBCT can be used to reliably quantify GT in a non-invasive manner. 21,22 With regard to the relationship between the gingival biotype and tooth inclination, previous studies found no association Montanha-Andrade K, Crusoé-Rebello IM, Barreto M, Neves FS, Santos JN, Cury PR -Assessment of the relationship between tooth inclination and gingival and alveolar bone dimensions using computed tomography of the maxillary anterior teeth: a cross-sectional study 6 between maxillary incisor proclination and the thin gingival biotype. 6,10,15 However, none of those studies used CBCT images to measure gingival thickness. With regard to the level of the gingival margin (GM), although a few studies described a positive association between the presence or absence of gingival recession (clinically evaluated) and tooth inclination, 10,15 to the best of our knowledge, the relationship between the GM level and tooth inclination has not been previously evaluated.
Therefore, there is a lack of consensus among previous studies regarding the associations between tooth inclination and gingival and bone dimensions. 10,11,[13][14][15][16] Accordingly, the aim of this study was to investigate the relationship between tooth inclination and gingival and bone dimensions in the maxillary anterior teeth using CBCT, which allows highly accurate measurement of tooth inclination, as well as gingival and bone dimensions on the same image. 23,24 The tested hypothesis was that there is a negative correlation between the inclination of the maxillary anterior teeth and the thickness of the buccal bone and gingiva.
Montanha-Andrade K, Crusoé-Rebello IM, Barreto M, Neves FS, Santos JN, Cury PR -Assessment of the relationship between tooth inclination and gingival and alveolar bone dimensions using computed tomography of the maxillary anterior teeth: a cross-sectional study 7

MATERIAL AND METHODS
The study protocol was independently reviewed and approved ( tion. An informed consent was obtained from all participants.

STUDY DESIGN, SETTING, AND PARTICIPANTS
This cross-sectional study included a convenience sample of 30 individuals (160 teeth). The primary outcomes were gingival and bone thickness and height, with sex and age as potential A total of 42 patients were screened for the inclusion and exclusion criteria. From these, 12 patients with a history of orthodontic treatment were excluded, and the remaining 30 were considered eligible for analyses. Eighteen teeth were absent.

CBCT SCANNING
At the time of CBCT scanning, the patients wore a plastic lip retractor, and images were acquired using a CS 8100 3D tomography device (Carestream Health Inc., Marne La Vallée, France).
The acquisition protocol was in accordance with the manufacturer's instructions and anatomical profile of the patient, with a voxel size of 0.15 mm and a field of view of at least 100 × 50 mm. 25,26

CBCT IMAGE ANALYSIS
A single examiner, specialized in Orthodontics, trained by an experienced radiologist, performed all measurements using CS 3D Imaging software (version 3.5.18; Carestream Health Inc., Marne La Vallée, France). After the training period, the intraexaminer correlation coefficient was at least 0.8 for all planned linear measurements.
Montanha-Andrade K, Crusoé-Rebello IM, Barreto M, Neves FS, Santos JN, Cury PR -Assessment of the relationship between tooth inclination and gingival and alveolar bone dimensions using computed tomography of the maxillary anterior teeth: a cross-sectional study 9 Changes in brightness and contrast and the zoom function were used for better visual assessment.
For the evaluation of buccolingual inclination, a palatal line was drawn from the anterior nasal spine to the posterior nasal spine on the sagittal images ( Fig 1A). Subsequently, the angle between the long axis of each maxillary anterior tooth and the palatal line was measured ( Fig 1A) on the best image generated in the sagittal view, without any change in the dental inclination on parasagittal or coronal sections. Pearson's correlation analysis was used to evaluate the association between tooth inclination and the periodontal dimensions for each tooth group. When the differences between male and female participants or younger and older individuals were statistically significant (p ≤ 0.05), a partial correlation controlling for sex and/or age was used.
Montanha-Andrade K, Crusoé-Rebello IM, Barreto M, Neves FS, Santos JN, Cury PR -Assessment of the relationship between tooth inclination and gingival and alveolar bone dimensions using computed tomography of the maxillary anterior teeth: a cross-sectional study 12 A significance level of 5% (α=0.05) was adopted for all statistical tests, which were performed using Statistical Package for the Social Sciences software, version 13.0 (SPSS Inc., Chicago, IL, USA).

GENERAL CHARACTERISTICS
The study sample comprised 160 maxillary anterior teeth from 30 adult patients, including 19 women and 11 men, aged 18 to 66 years (mean ± standard deviation = 39.40 ± 12.06 years).

Central incisors / Tooth third Lateral incisors / Tooth third
The mean CEJ-BC and GM-BC distances showed no significant differences among the tooth groups (p ≥ 0.06), whereas the mean GM-CEJ was significantly greater for the lateral incisors (1.34 ± 1.22 mm) than for the canines (0.70 ± 1.11 mm, p = 0.01) ( Table 1). Men and women showed differences in the gingival and bone dimensions for the central incisors and canines. In the central incisor group, the bone in the cervical region was significantly thicker for women than for men (p = 0.01); moreover, the GM-CEJ was greater in women than in men (p = 0.04). In the canine group, the bone in the middle and apical regions was significantly thicker for men than for women (p ≤ 0.02).

Montanha-Andrade
The other differences were not statistically significant (   Montanha-Andrade K, Crusoé-Rebello IM, Barreto M, Neves FS, Santos JN, Cury PR -Assessment of the relationship between tooth inclination and gingival and alveolar bone dimensions using computed tomography of the maxillary anterior teeth: a cross-sectional study 15 With regard to age, the GM-CEJ for all tooth groups was significantly smaller in individuals aged ≥50 years than in those aged <50 years (p ≤ 0.02). The GT for the central incisors was significantly smaller in the older group than in the younger group (p = 0.05; Table 3). Other differences were not statistically sig-  Table 3: Gingival and bone dimensions (in mm) according to age (mean ± standard deviation).  Table 4).  Therefore, the tested hypothesis was partially accepted.
The present study demonstrated that greater labial inclination (proclination) was associated with greater BT in the apical region of the central incisors and canines, in agreement with previous reports on central incisors. 14,26 Conversely, in the present investigation, greater labial inclination of canines was associated with smaller BT in the cervical region. Previous studies also found reduced BT for the maxillary canines, and speculated that this finding was associated with greater prominence of their roots. 7,26-28 However, those studies did not evaluate the impact of tooth inclination. In divergence to the findings of the present study, the results of two previous studies did not reveal significant differences in the cervical BT according to the tooth inclination for maxillary central incisors. 13,14 In contrast, another study described that retroinclined maxillary central incisors showed thinner bone at the cervical level than did normal or proclined central incisors. 16 The increased BT in the apical region and decreased BT in the cervical region of more Montanha-Andrade K, Crusoé-Rebello IM, Barreto M, Neves FS, Santos JN, Cury PR -Assessment of the relationship between tooth inclination and gingival and alveolar bone dimensions using computed tomography of the maxillary anterior teeth: a cross-sectional study 18 proclined central incisors and canines can be explained by the retroposition of the tooth apices and anteroposition of the cervical area, due to the tooth inclination.
In the current study, there was a significant direct association between tooth inclination and the GM-CEJ distance for the canines. In a systematic review, most studies showed that the incidence or severity of gingival recession was greater for more proclined teeth than for less proclined or orthodontically untreated teeth. 11 However, it should be noted that there are no high-quality studies regarding this topic, and the low level of evidence in the studies included in the former review and the present results indicate that further clinical studies controlling for dental plaque amount are necessary to clarify the relationship between tooth inclination and the GM position.
In the present study no association between GT and maxillary anterior tooth inclination was found, in accordance with the results of previous studies. 10,12,15 Although these investigations assessed the buccolingual inclination of the maxillary central incisors through cephalometric analysis and GT through clinical inspection, no relation was found between the two variables. Thus, GT in the maxillary arch seems to be related to factors other than tooth inclination, such as age -as confirmed here-, dental arch location, tooth type, gingival width and inherited condition. 8,29,30 Montanha-Andrade K, Crusoé-Rebello IM, Barreto M, Neves FS, Santos JN, Cury PR -Assessment of the relationship between tooth inclination and gingival and alveolar bone dimensions using computed tomography of the maxillary anterior teeth: a cross-sectional study 19 The associations between tooth inclination and periodontal dimensions were separately analyzed for each tooth group On the contrary, other studies did not find significant differences in the gingival and bone thickness among the maxillary anterior teeth. 4,31 The discrepancy between studies might be associated with differences in the evaluation technique. While the present study recorded gingival measurements using CBCT images, the former studies used transgingival probing. 4,31 To test for confounders, differences between sexes and age groups were evaluated. Differences in BT and the GM-CEJ distance for the central incisors and canines between men and women were found, as opposed to the findings in previous studies. 26,32,33 For the central incisors, women showed thicker bone in the cervical region than men. On the other hand, men showed thicker bone in the middle and apical thirds of canine roots than women. The GM-CEJ was also greater in women than in men. These contrasting results may have occurred because of differences in the methodology and populations studied.
With regard to age, the GM-CEJ distance for all tooth groups Montanha-Andrade K, Crusoé-Rebello IM, Barreto M, Neves FS, Santos JN, Cury PR -Assessment of the relationship between tooth inclination and gingival and alveolar bone dimensions using computed tomography of the maxillary anterior teeth: a cross-sectional study 20 was significantly smaller in individuals aged ≥50 years than in those aged <50 years, while GT for the central incisors was smaller in the older group. This result is in accordance with a previous investigation and can be attributed to thinning of the epithelium in relation to age. 8 The strengths of the present study are related to its methodology. CBCT allows simultaneous evaluation of the soft and hard tissues through the use of a single tool; moreover, it shows high accuracy and is a non-invasive and reproducible method. 23,24 The images exhibited a high resolution because they were acquired using a small voxel size. Furthermore, tooth inclination was measured for all maxillary anterior teeth, and the entire labial root surface was screened on axial slices for determining the smallest gingival and bone thickness in the cervical, middle, and apical thirds. Despite the diagnostic advantages, however, it is known that the radiation dose delivered by CBCT is higher than the dose delivered by diagnostic modern digital panoramic and cephalometric imaging combined. 34 This study also had some limitations. First, the cross-sectional design did not allow obtaining information on the sequence of events, which precludes a conclusion regarding the causal rela- Considering the existence of an association between tooth inclination and bone thickness, evaluation of the periodontium using tomographic images is especially useful for treatment planning, and should be performed particularly when a change in tooth inclination of central incisors and canines is being considered for orthodontic therapy, or the region to be treated already shows thin alveolar bone or evidence of periodontal support loss. 36 Patients who require orthodontic treatment involving labial movement of the central incisors and canines should undergo a periodontal evaluation before any orthodontic procedure, because the facial alveolar bone of maxillary teeth is thin. 37 Respecting the biological limits of the patient's alveolar bone anatomy is of utmost importance to avoid future periodontal problems such as dehiscence. 36 During orthodontic treatment Montanha-Andrade K, Crusoé-Rebello IM, Barreto M, Neves FS, Santos JN, Cury PR -Assessment of the relationship between tooth inclination and gingival and alveolar bone dimensions using computed tomography of the maxillary anterior teeth: a cross-sectional study 22 planning, the final canine position should be given special consideration, because it can affect the soft tissue contour and influence the aesthetic outcome.
Further research on the effects of orthodontic changes in tooth inclination on the periodontium may provide more information on the cause/effect relationship between tooth inclination and gingival and bone dimensions.

CONCLUSIONS
In summary, these results suggest that: » Greater labial inclination is associated with greater apical BT in the central incisors and canines.
» Greater labial inclination is associated with thinner cervical bone and a smaller GM-CEJ distance in canines.
» For the lateral incisors, there is no correlation between tooth inclination and gingival and bone dimensions.