CBCT Assessment of Gubernacular Canals on Permanent Tooth Eruption in Down’s Syndrome

Background: The gubernacular canal (GC) is an important dental structure that enables the alveolar bone ridge cohesion of permanent teeth, although GC absence may indicate a dental eruption that might be associated with certain syndromes such as Down’s syndrome. This study aims to correlate the eruptive delay of permanent teeth in individuals with Down’s syndrome (Ds) and the gubernacular canal (GC) through cone-beam computed tomography (CBCT). Methods and Results: This cross-sectional study was conducted between January and July 2022 with a total of 31 individuals (G1 = 16 nonsyndromic and G2 = 15 Down’s syndrome) who went through imaging evaluation using CBCT with the following acquisition parameters: tube voltage of 95 kVp, tube current of 7 mA, exposure time of 5.9 s and voxel sizes and field of view 0.15 mm and 0.30 mm, respectively. The imaging evaluation was to assess whether all teeth analyzed had the presence of GC and/or teeth eruption disturbance, with a descriptive statistical analysis of relative frequencies and quantitative variables as well as the p-value (p < 0.005) by G Test. Results: A total of 618 teeth among 31 individuals were analyzed, 475 (76.8%) GC were detected by CBCT in 23/31 patients and of these, 6 belonged to G2. G2 had a decreased GC detection rate (n = 180–37.9%) and the most common tooth with GC detected was the mandibular 1st molar (21 GC/25 teeth—84%) and the absence of GC was most frequently observed in impacted and delayed/unerupted teeth of Ds individuals. Conclusion: We concluded that GC absence was higher among Ds individuals, explaining the increased rates of unerupted or impacted teeth in Ds individuals.


Introduction
Mixed dentition is a stage of growth and development that begins with the dental eruption of the first permanent teeth at about 6 years old and continues until 12 years old [1][2][3]. In this stage, the oral cavity undergoes certain physiologic changes including deciduous teeth root resorption followed by exfoliation of permanent teeth within the gubernaculum dentis, which is made by the gubernacular cord, after which, osteoblastic activity forms the gubernacular canal, which is important in the eruption process, representing an eruption path through maxillary bone [4,5].
As mentioned previously, both the gubernacular canal and cord are intraoral structures very important to the tooth-eruption process, although a small number of studies in the literature about GC and cord demonstrated their influence in permanent teeth eruption physiologic processes, especially in the follicular theory [5,6]. The gubernacular cord is a structure composed of conjunctive tissue which connects the permanent tooth follicle to criteria were (i) individuals with a confirmed diagnosis of Ds; (ii) attended a monthly follow-up at SIDOPE in Pará State; (iii) at least 10 teeth in the mouth and without periodontal disease or cavities for about 1 year; (iv) aged between 10 to 15 years old; (v) resident in Pará State; (vi) both genders; and (vii) teeth completely encased within the alveolar bone.
The exclusion criteria were (i) individuals who were moved to other states; (ii) individuals who started follow-up at SIDOPE but no longer returned to monthly follow-up; (iii) medical records not filled out correctly; (iv) low-quality CBCT images; and (v) CBCT images with motion blurring or metal artifacts. Each participant was physically and orally evaluated in a private SIDOPE location. Clinical data were collected by a single researcher, a specialist in oral pathology, previously calibrated by Kappa test and with previous experience in clinical studies, and the intraoral clinical examination was performed in a dental office, dental chair, under indirect and artificial light, using a dental mirror, Williams periodontal probe (Hu-Friedy, Chicago, IL, USA) and clinical tweezers, all sterile.
After clinical exams, demographic and epidemiological data were obtained through a pretested standardized semi-structured questionnaire and medical records. The individuals were divided into two groups according to the presence or absence of Ds. The groups were formed and organized by nonsyndromic patients as the control group and Ds patients, with the nonsyndromic patients presenting with the GC open: G1 group: 16 patients (control group, GC open); G2 group: 15 (possible GC obstructed).
The study consisted of CBCT examinations for all 31 patients with impacted/unerupted permanent teeth in mixed dentition, for dental planning of orthodontic treatment, periodontal nonsurgical or surgical treatment, impacted teeth location, and identifying dental anomalies. All CBCT images were taken and collected from the Department of Oral and Maxillofacial Radiology of UFPA, the tomography machine was a Pax-i 3D smart (Green Vatech, Seoul, Korea), and acquisition parameters were a tube voltage of 95 kVp, a tube current of 7 mA, an exposure time of 5.9 s (Green Protocol) and voxel sizes and a field of view (FOV) of 0.15 mm (8 × 8 cm and 6 × 6 cm) and 0.30 mm (8 × 8 cm), respectively [19].

Imaging Procedures
After the CBCT images were acquired, they were converted to the digital imaging communication in medicine (DICOM) file format, uploaded to an independent storage software (Dropbox Inc., San Francisco, CA, USA, EUA), and then opened with opensource DICOM viewer software OsiriX 12.0 (Pixmeo, Geneva, Switzerland). All DICOM file evaluations were carried out by a single examiner, an oral radiologist with twenty years of experience, and a standardized CBCT view procedure (distance view, diagnostic screen, dimmed room, image magnification, contrast, brightness, and slice thickness) was established by the examiner [19].
All CBCT teeth images were visualized in axial, coronal, sagittal, cross-sectional, and panoramic views in the X, Y, and Z axes. The parameters analyzed included the presence or absence of GC, permanent eruption stages, the presence of physical obstructions in the eruption path or pathological conditions, root formation stage, angulation, and dilaceration [19]. Radiographically standard GC parameters were three-dimensional images with low-density, narrow diameter, corticated tract, and continuous with unerupted tooth dental follicle.

Statistical Analysis
The statistical analysis was performed using JAMOVI Statistics for Windows, Version 3 (Jamovi project, Sydney, Australia) statistical software. A descriptive analysis of the data was performed, with a distribution of absolute and relative frequencies, using the minimum and maximum value, mean and standard deviation as well as the p-value (p < 0.005) by G Test for the selected groups; additionally, the odds ratio (OR) and associated 95% confidence interval (CI) were used as measures of the strength of dependent association between GC absence (outcome) and Ds individuals.

Sample Demographic and Epidemiological Characteristics
A total of 40 individuals were invited, although only 31 participated in the present study due to not satisfying the inclusion criteria or not agreeing to sign the consent term; therefore, the final analyzed sample consisted of 15 individuals diagnosed with Ds and 16 nonsyndromic individuals.

Discussion
To the best of the authors' knowledge, the present study is one of the few studies that have focused on the use of CBCT imaging to study GC characteristics and its role in teeth eruption associated with pathological conditions among Ds individuals and is the first study evaluating this population in northern Brazil. According to Kaplan et al. [20], the first citation of gubernacular cord and GC was made in 1778 by John Hunter and was supported in 1887 by Charles Malassez in a microscopic evaluation. The overall concept of GC details that it is a radiolucent/hypodense corticated structure, directly connected to the dental follicle space, which is an eruption pathway for permanent teeth.
Through the years, studies demonstrated that GC structures can be visualized on panoramic and dental radiographs, although some diagnoses propose that the two-dimensional characteristics of dental radiographs would make it difficult to visualize or measure some GC aspects such as length, diameter, pathway, deformation, and/or obliteration. Therefore, recent studies introduced CBCT as a justified imaging examination to evaluate GC presence and its possible disturbances such as impacted or delayed/unerupted teeth that will influ-ence clinical pediatric dentistry, orthodontics planning, and oral and maxillofacial surgical treatment due to its specificity in different images [21][22][23].
In the general literature, some studies such as Koc et al. [19] and Nishida et al. [24] correlated GC detection and its prevalence with chronological age, and in confirming their results, a correlation between these parameters could not be found. Nishida et al. [24] found a higher prevalence of GC, and GC was clearly visualized on CBCT in patients even with unerupted permanent teeth during a normal eruption, except when maxillary central supernumerary teeth were present causing an eruption disturbance, which will obstruct GC; Koc et al. [19] had similarly low GC detection rate results to Nishida et al. [24] when eruption disturbances, as supernumerary teeth, were present. This study made a different correlation with sociodemographic data, to understand if other variables other than age could influence GC formation and prevalence, although no association was found.
Further, among studies that correlated GC detection and its prevalence with age, Oda et al. [22] identified that while patients were aging, the GC shape was modifying with chronological age, and according to Oda et al. [22], the progression forms of GC defined by authors were sprouting form groove form, imperfect-tubular form, tubular form, and hole form. Unfortunately, in our study, the first limitation we had was that we selected only CBCT images that did not contain abnormal GC shape findings; therefore, no correlation to GC shape could be made [21].
Of all the few studies regarding GC detection rates, our study was the first to evaluate a Ds population. The main reason why this sample was selected was that individuals with this genetic disorder may present various oral cavity alterations and specific oral/craniofacial characteristics such as class III malocclusions, maxillary hypoplasia, periodontal disease, dental caries, missing teeth, and some dental abnormalities such as microdontia, taurodontism, impacted teeth or hypodontia, and tongue disorders such as macroglossia that will affect their oral and respiratory functions, decreasing their oral quality of life [15][16][17][18]. Furthermore, due to these oral cavity alterations and Ds craniofacial characteristics, some parafunctional habits can be seen in these individuals such as tongue thrusting, bruxism, mouth breathing, and obstructive sleep apnea [25][26][27][28].
Regarding the dental eruption state, there were 280 (45.3%) normal positioned teeth, 203 (32.8%) impacted teeth and 135 (21.9%) delayed/unerupted in a total of 618 teeth. In our results, G2 (n = 139/203-52%) had a higher prevalence of impacted teeth than G1 (64/203-18.2%), and the most common impacted permanent teeth were mandibular cen-tral incisors, maxillary canines, and maxillary lateral incisors. Oddly, delayed/unerupted teeth were most prevalent in G1 (n = 106/135-30%) compared to G2 (n = 29/135-11%), and the most common delayed/unerupted permanent teeth were maxillary lateral incisors, maxillary canines, and mandibular 1st molars. Furthermore, the only tooth which was statistically significant was the mandibular 2nd premolar [29][30][31]. This study had a few limitations that should be considered, including the small sample numbers from a crosssectional analysis from a single institution, the fact that GC shape disturbances during teeth eruption or impaction could not be evaluated, and lastly, only individuals living in Pará State, northern Brazil, were included.

Conclusions
Based on the findings of our study, we concluded that GC was more common among nonsyndromic individuals than Ds individuals, the prevalence rates between the two groups presented a possible influence of Ds and its oral manifestations or craniofacial characteristics, which might increase the delay or impaction of teeth or dental eruption state, which will also prejudice GC formation, as demonstrated in our results. Therefore, the higher GC absence among Ds individuals may be a new disturbance eruption or impaction for these patients, so Ds might be a prevalence parameter for GC.