|Year : 2019 | Volume
| Issue : 10 | Page : 1448-1456
CBCT analysis of schneiderian membrane thickness and its relationship with gingival biotype and arch form
S Chaturvedi, SB Haralur, MK Addas, MA Alfarsi
Department of Prosthetic Dentistry, College of Dentistry, King Khalid University, Abha, Saudi Arabia
|Date of Acceptance||03-Jun-2019|
|Date of Web Publication||14-Oct-2019|
Dr. S Chaturvedi
Department of Prosthetic Dentistry, College of Dentistry, King Khalid University
Source of Support: None, Conflict of Interest: None
| Abstract|| |
Objective: The purpose of this study was to investigate a relationship between gingival tissue biotypes and arch form with Schneiderian membrane thickness, using limited cone beam computed tomography. Materials and Methods: A total of 90 subjects were selected. For each subject three parameters were assessed – gingival biotype - clinically by Probe transparency method as thin or thick and coded as 0 and 1, respectively, gingival thickness and Schneiderian membrane thickness in mm, arch form as square, oval, or tapered (radiographically by cone beam computed tomography images). Central incisors and first molars were assessed for gingival biotype and gingival thickness and Schneiderian membrane thickness was determined at 16. Numerical data were estimated for normal distribution. Analysis of Variance test was followed by Tukey honestly significant difference test and Pearson's correlation coefficient test for analysis. Results: Thin gingival biotype was found associated with the central incisors and thick gingival biotype with molars. Limited cone beam computed tomography scans evaluation revealed highest prevalence of square arch form followed by oval, and tapered. The average thickness of the Schneiderian membrane was 1.18 ± 0.43 mm on left side and 1.09 ± 0.41 mm on right side with a range of 0.50 – 2.00 mm. Mean Schneiderian membrane thickness was more in case of thick gingival biotype and with square arc form both on right and left sides. Conclusions: The Schneiderian membrane thickness was positively and highly associated with gingival biotype. The gingival biotype and arch form had significant effect on Schneiderian membrane thickness and can provide valuable clinical information on Schneiderian membrane thickness preoperatively for implant placement and sinus lift procedures.
Keywords: Cone beam computed tomography, dental implant, gingival biotype, sinus lift
|How to cite this article:|
Chaturvedi S, Haralur S B, Addas M K, Alfarsi M A. CBCT analysis of schneiderian membrane thickness and its relationship with gingival biotype and arch form. Niger J Clin Pract 2019;22:1448-56
|How to cite this URL:|
Chaturvedi S, Haralur S B, Addas M K, Alfarsi M A. CBCT analysis of schneiderian membrane thickness and its relationship with gingival biotype and arch form. Niger J Clin Pract [serial online] 2019 [cited 2020 Sep 28];22:1448-56. Available from: http://www.njcponline.com/text.asp?2019/22/10/1448/269010
| Introduction|| |
Digitalization of dental technologies has opened a wide range of methods to evaluate and relate the various anatomical structures in and around the stomatognathic system. Various features which cannot be distinguished with normal examination can be easily studied with advancement in radiology. Especially with the introduction of limited cone beam computed tomography (CBCT) scanning, there was a major shift in dento-maxillofacial radiology from two- to three-dimensional (2D to 3D), image reconstruction, visualization, and data acquisition. In comparison to computed tomography (CT) scanning, CBCT scanning has several advantages, the most important being less radiation for the patient. In particular, for the research, diagnosis and treatment planning for implants, CBCT scanning has exhibited imperative returns over conventional intraoral radiographs.,,
In radiographic studies of CT and magnetic resonance imaging, coronal slices were well established for evaluating the mucosal thickness in the maxillary sinus, and the measurements were always performed perpendicularly to the underlying bone.,,,, Previous studies described the average thickness of normal mucosa as 1 mm with an appreciable variation in individuals., A study on unfixed, fresh cadavers without sinusitis mentioned membrane's thickness as 0.3-0.8 mm. At single-implant sites, it is particularly important to correlate the extension of the sinus lifting with sinus membrane deformation capacity as well as thickness. Clinical studies reported a high correlation between the sinus membrane thickness and the risk of perforations.,
Various factors, which may influences Schneiderian membrane thickness (SMT), are illustrated in the literature. Vallo et al. found higher SMT values in maxillary sinuses adjacent to periodontal and endodontic lesions. In contrast, recently Gingival thickness and sex are identified as an influencing factor for maxillary sinus mucosa thickness in a multivariate regression analysis: the membrane is thicker in patients with thick gingival biotype and thinner in female subjects.,, Endodontic, periodontal, and periapical status of the dentition in the region of interest had not shown any statistically significant influence.
For successful dental implant rehabilitation, along with systemic condition accurate assessment of gingival architecture, alveolar bone, arch form (AF) are important. In posterior maxilla, preoperative prediction of the antral membrane thickness may provide additional information for surgical planning.
Also, it has long been suggested that the thickness of the marginal periodontium  and AF  are genetically determined but no knowledge is still available concerning their relation with the sinus mucosa. The term gingival biotype (GB),,, had been used to describe the thickness of the gingiva in the facio-palatal dimension , with two variants as (i) Thick biotype (prevalence: 85%) and (ii) Thin biotype (prevalence: 15%). The teeth bearing areas of the jaw are arranged in the form of arches and are classified as tapered, oval, or square.,, AF basically refers to the overall configuration of the dental arch, and this takes into account the symmetry, roundness, elongation, and convexity. Various method have been described in literature for proper assessment of these two factors which can help in easy predilection of SMT clinically.
Thus, a hypothesis was formulated for the present study that GB and AF may assist the clinician in determining the features of the Schneiderian membrane. Therefore, this study was conducted with the aim to investigate whether a relationship exists between gingival tissue biotypes and AF with SMT, using limited CBCT.
| Method and Materials|| |
This study was conducted in full accordance with the World Medical Association Declaration of Helsinki, in King Khalid University College of Dentistry (KKUCOD), Abha, Aseer Province, Saudi Arabia. The ethical approval (SRC/ETH/2017-2018/38) was taken from the ethical committee of the KKKUCOD and written informed consent was obtained from all subjects.
The samples were collected from the KKUCOD, outpatient department (OPD), in a period of 8 months (March to October 2018). In this cross-sectional study, single examiner selected all samples on the basis of inclusion and exclusion criteria from OPD with the age range of 25-45 years. A total of 90 samples were collected with following inclusion criteria: clinically healthy gingiva, no bleeding of probing, no periodontal probing depth in excess of 3 mm, presence of all maxillary teeth without any prosthesis (Fixed partial denture [FPD], Removable partial denture [RPD]), clear and continuous lamina dura at the apical third of maxillary teeth roots. The exclusion criteria were as follows:  maxillary sinus pathologies (sinusitis, cysts, neoplasms, and allergies); any medication and systemic disease that could affect the thickness of the periodontal soft tissues (cyclosporin A, calcium channel blockers, phenytoin, diabetes, and immunologic diseases); extensive restorations or previous mucogingival or periodontal surgery in the maxillary anterior and/or posterior region; periapical pathology on maxillary teeth; previous orthodontic treatment that could affect the thickness of the labial gingival or AF (such as arch expansion); smoking habits; and pregnancy or lactation.
Following this, for all subjects CBCT scan were obtained by Veraviewepocs 3D CBCT scanner (Veraviewepocs 3DF40 J. Morita MFG CORP. Kyoto, Japan) with the following settings: 90 kVp at 3 mA for a total scan time of 15 s, with a voxel size 0.3 mm (all protection protocol were followed while making scans according to ethical standards). For all CBCT images, a limited field of view (FOV) of 4-4 cm, or 6-6 cm was selected. The 3D image was reconstructed by Veraviewepocs 3D software and saved in digital imaging and communications in medicine (DICOM) format with slices at an interval of 0.5 mm.
Three parameters were assessed in selected subjects - GB (clinically by Probe transparency (TRAN method) and Gingival thickness (GT), SMT, AF (radiographically by CBCT images).
Probe transparency  method is the least invasive method documented in literature to evaluate the GB. The sulcus probing was done at the midfacial and mid buccal aspect of the maxillary central incisors , and first molars , respectively. Based on visibility of the underlying periodontal probe through the gingival tissue, the GB was categorized as either thin or thick and coded as 0 and 1, respectively (visible = thin, not visible = thick) [Figure 1].
Evaluation of the CBCT images were done by chief researcher and calibrated before by otolaryngologist for better knowledge and understanding of anatomy and maxillary sinus pathologies.
To determine the thickness of the Schneiderian membrane, the CBCT slices were first reorganized to place the posterior maxillary segment ( first premolar to the second molar) of the alveolar bone crest in a vertical position in the axial slices, and the palate/floor of the nose in a horizontal position in the coronal slices. Then in the sagittal slices measurements were calculated by a built-in digital calliper in millimeters perpendicularly from the underlying bone plate of the sinus to the mucosal surface [Figure 2]. Through drawing lots, 32 mesiobuccal, 34 distobuccal, and 24 palatal roots were selected for teeth 16 and 26 each in 90 selected subjects.
|Figure 2: Determination of thickness of the Schneiderian membrane in CBCT slices. (a)-Axial slice,(b)-Sagital slice, – measurement of schinederian membrane thickness. (c)-Coronal slice, (d)-Orientation of arch|
Click here to view
The gingival thickness was measured at 2 mm apically the alveolar crest and perpendicular to the external cortical plate of the tooth socket by using the cross-sectional images taken at the midline of the selected teeth [Figure 3].
|Figure 3: Determination of Gingival thickness in CBCT slices. (a)-Axial slice, (b)- Coronal slice, (c)-Sagital slice, – measurement of gingival thickness. (d)-Orientation of Arch|
Click here to view
The maxillary AF was determined by using the same software of CBCT. With the help of horizontal sections of CBCT, the occlusal view of the arch was located. The measuring tools of the software were used to join the following reference points: incisal edges of the incisors, cuspids tips of the canines, and the buccal cuspids tips of the premolars and molars, to obtain the dental AF [Figure 4]. These images of the dental arches were used to classify the arches as square, oval, or tapered.
|Figure 4: Various arch forms in horizontal section of CBCT (Points joined are-incisal edges of the incisors, cuspids tips of the canines, and the buccal cuspids tips of the premolars and molars, to obtain the dental AF), (a) Square Arch Form, (b) Tapered Arch Form (c) Oval Arch Form|
Click here to view
To reduce variations in measurement, in this study, the chief researcher made all measurements. The intra-examiner reliability in measuring SMT and GT was assessed by measuring, eight randomly selected cases, twice at an interval of 2 days, resulting in a mean difference of 0.16 mm per image (range of 0–0.35 mm). For the further study, each measurement was repeated, and the mean value was calculated. When the difference between two values was 0.2 mm, a third measurement was performed. Also, the inter-operator error measurements were done by asking a trained prosthodontist to take measurements on the same eight selected subjects. The intra-operator and inter-operator error was assessed using the intra-class correlation coefficient. High correlation was found for both intra-operator (r = 0.84) and inter-operator (r = 0.86) error. Correlation between examiners in classifying the morphology of the dental arch was evaluated by applying the modified Kappa test.
Numerical data so obtained after recording were estimated for normal distribution. It was analysed using descriptive statistics and comparisons were made between GB, GT, AF and SMT. For multiple comparisons, two-way ANOVA (Analysis of Variance) was used to detect effects of various GB and AFs and their interactions with SMT. ANOVA was followed by Tukey HSD test (Tukey honestly significant difference test) for paired comparisons of the means. Pearson's correlation coefficient was calculated to examine the relationship between gingival biotypes and sinus membrane thickness. All tests were calculated with a statistical significance level of 5% and confidence interval of 95%. Statistical analysis was performed with IBM SPSS Statistics Version 20 for Windows (IBM Corporation, NY, USA. SPSS, Inc., an IBM Company).
| Results|| |
GB was determined as thin in 57.8% cases at 11, 61.1% at 21 and thick in 53.3% at 16 and 57.8% at 26 overall thin GB was associated with the central incisors and thick GB with molars [Figure 5]. The gingival thickness varies from 0.50 to 2.00 mm. At the right side the average GT at CI was 1.13 ± 0.41 mm and 1.23 ± 0.41 mm at Molar and 1.14 ± 0.42 mm and 1.30 ± 0.40 mm at CI and molar, respectively, on left side [Figure 6]. On segregating GT under thin and thick GB, the average thickness at CI and Molars were determined and presented in [Table 1].
|Table 1: Gingival biotype thickness summaries individually in thick and thin categories|
Click here to view
Limited CBCT scan evaluation revealed highest prevalence of square AF followed by oval, and tapered [Figure 7].
Maxillary sinus examination showed the average thickness of the Schneiderian membrane was 1.18 ± 0.43 mm on left side and 1.09 ± 0.41 mm on right side with a range 0.50 – 2.00 mm [Figure 6]. A wide inter- and intra-individual variability was observed in SMT. On comparing the SMT between the two sides it was found that the SMT on left side was 1.18 ± 0.43 mm which was significantly greater (P < 0.001) than the thickness at right side where the mean value was only 1.09 ± 0.41 mm [Table 2].
On comparing SMT with various GB, it was determined that the mean SMT was more in case of thick GB both at CI and M both on right and left sides [Figure 8]. The sinus mucosal thickness was positively associated with GB and showed high correlation with GT (AT 11 [r = 0.892, P < 0.001], 16 [r = 0.982, P < 0.001], 21 [r = 0.810, P < 0.001] and 26 [r = 0.975, P < 0.001]) [Figure 9].
The assessment of the data on AF and SMT, the prevalence of square AF was maximum in the studied population [Table 3]. Among various AFs it was found that the maximum thickness of SMT was seen with square arc form both on right and left sides. However, no significant difference was observed in mean SMT among the various AFs (P = 0.069) [Figure 9].
| Discussion|| |
The clinical data and radio-morphometric data obtained by limited CBCT, indicate a positive correlation between SMT, GB, and AF; thus validating our hypothesis. The study was conducted in meticulously selected young age group individuals to avoid the effect of confounding factors thus results of this study provided reference data of normal ranges of SMT for subjects with different GB and AFs. This will be useful for clinicians involved in the rehabilitation of patients with a conventional or implant supported prosthesis and performing complex maxillary sinus augmentation implant surgeries.
All participants in the study were free from any sinus pathologies or periapical infections of the maxillary teeth, as this could influence the SMT. Also, clear and continuous lamina dura at the apical third of maxillary teeth roots was assessed during enrolment.
During rehabilitation with implants, especially for vertical ridge defect in the posterior maxilla, sinus augmentation has become a widely used and predictable procedure ,,, However, membrane perforation still occurs, may be due to inadequate surgical planning and/or operator's skill. It is always difficult to properly assess SMT preoperatively due to a lack of rationality and reliability of measurement methods. Which types of mucosal thickening require therapy is still unknown, but historically more than 2 mm is considered a reliable threshold for pathological mucosal swelling. In our study, also similar readings of SMT were obtained with 2.00 mm maximum thickness in subjects without any pathologies.
In this study, both inter- and intra-individual variability of SMT was noted, with values ranging from 0.5 mm (minimum) to 2.00 mm (maximum). In a previous post mortem study, the SMT was evaluated with a range of 0.30-0.80 mm., In a similar study using 20 fresh cadavers, Pommer et al. found a mean thickness value of 0.09 ± 0.05 mm (range, 0.02–0.35 mm). Also, in a histological study of Schneiderian membrane of healthy subject, Aimetti et al. measured a mean thickness of 0.97 ± 0.36 mm, sinus biopsies specimens. All three mentioned groups describe great inter-individual variability in the thickness of the Schneiderian membrane. In the present study, limited CBCT scanning was used to visualize Schneiderian membrane. CBCT is a volumetric acquisition technique providing accurate and reliable submillimetre resolution images in all spatial dimensions, which shows promise in the detection of maxillary sinus anatomy.,,, Smaller FOV was used, thus adhering to the ALARA (as low as reasonably achievable) principle in radiology. FOV is the term used to refer to the scan volume of a particular CBCT unit. Since, larger FOVs result in higher effective radiation doses, as a rule, smaller FOVs are recommended for imaging a quadrant or single tooth. The CBCT scan used in the present study helped as it can improve the spatial resolution of high-contrast structures in any chosen viewing plane. This superior spatial resolution, that is, the ability to discriminate objects of different attenuation separated by very small distances, is one of the most attractive qualities of CBCT imaging.,
There are different views regarding Schneiderian membrane perforation, some authors , observed no difference in vital bone formation and implant survival while others have shown more postoperative complications such as sinusitis, graft failure  and less implant survival rate. Barone et al. described that membrane perforation might lead to graft migration and sinus infection and proved that an intact Schneiderian membrane is essential for better vascularity, graft stability and maturation of the inserted bone graft materials., Apart from this, the presence of osteoprogenitor cells in Schneiderian membrane speed up bone formation. Thus, in the light of present literature it is commonly accepted that membrane integration is often associated with a better clinical outcome.
But till now, we did not find any firm justifications in indexed data search engines which directly relate altogether GB and AF with SMT. Individual studies had been performed but direct correlation have not been assessed, despite of the fact, it has a very important role during diagnosis and treatment planning in implantology. Keeping this in mind, the present study was conducted to relate GB and AF with SMT, which are the common clinical assessment in any oral rehabilitation.
In our study, the characteristics of GBs were defined by the conditions observed in the maxillary anterior and posterior region. In literature, one of the studies described, gingival thickness of ≥2 mm (measurements of 1.6–1.9 mm were not accounted for) was considered as thick tissue biotype and a gingival thickness of <1.5 mm was referred as thin tissue biotype, another study mentioned if thickness is >1.5 mm, it was categorized as thick biotype and if less than 1.5 mm, it was considered as thin, Müller et al. described a thin gingival phenotype characterized by gingival thickness <1 mm and a flat-thick gingival morphotype with gingival tissues >1 mm. Various invasive and non-invasive methods were proposed to determine GB based on measured tissue thickness. These include direct measurement, probe transparency method, ultrasonic devices, and cone-beam computed tomography scan. Placing a periodontal probe in the gingival sulcus and observing the transparency is a simple method to determine tissue thickness and the same was used in this study to categorize the GB and GT was evaluated using the limited CBCT scans with smaller FOV. Like, previous comparable studies in our study also thick GB was associated with minimum GT of 1.34 ± 0.39 (range 0.50-2.00) and thin GB with minimum GT of 0.87 ± 0.20 (range 0.50 -1.40). The prevalence of thin and thick GB was close to 57% and 43% in anterior region (11 and 21) and 40% and 60% in posterior region (16 and 26) in the concerned population.
The thickness of the Schneiderian membrane was found to be higher in individuals with thick GB on both side (at the right side the mean SMT thickness in case of thick biotype was 1.43 ± 0.39 mm and 1.39 ± 0.33 mm which was greater than the thin biotype with mean SMT 0.85 ± 0.21 mm and 0.75 ± 0.13 mm at 11 and 16, respectively. Similarly on the left side the mean SMT in case of thick biotype was 1.55 ± 0.38 mm and 1.48 ± 0.32 mm which was greater than the thin biotype with mean SMT 0.94 ± 0.26 mm and 0.77 ± 0.11 mm at 21 and 26, respectively. The difference in SMT thickness between the two biotypes was highly significant (P < 0.001). The correlation between the two parameters was high and statistically significant.
The AF described in the glossary of prosthodontic terms as “the geometric shape of the dental arch when viewed from the horizontal plane”. Failure to maintain the AF during treatment may results in loss of stable, functional, and aesthetic outcome. In the present study, the arch from was classified as square, tapered and oval by visual examination of the outline obtained in the horizontal slice of mandibular arch CBCT image. This method of classifying arches was considered above the mathematical functional methods., Some authors argue that anatomical structures could not be reduced to the mathematical precision of geometrical terms. Visual analysis method of classification of the dental arch was also used by other authors like FELTON  and NOJIMA. In present study, the same CBCT scan, which were used for SMT measurements, the arch form was determined, no separate procedure was carried out for this, compared to previous studies where separate cast, photocopying plaster models, occlusal view intra-oral photographs, 3D scanning of intraoral tissues or dental casts, digitizing natural, normal occlusion models and applying mathematic formulas to establish dental AF, were used.
In the present study, the AF was found to be associated with SMT. In the studied population, the prevalence of square AF was maximum 40% followed by oval and tapered. The maximum SMT was seen with square arc form with mean 1.16 ± 0.43 mm and 1.29 ± 0.44 mm while the minimum thickness was seen in tapered arc form with mean 0.93 ± 0.35 mm and 0.98 ± 0.40 mm on right and left sides, respectively. However, no significant difference was observed in mean SMT among the various AFs (P = 0.069) [Figure 10].
Based on the results of present study, the reference data of normal ranges of SMT could be provided to the clinicians who can use it even before any invasive or non-invasive investigations for implant treatment planning and sinus lift. This study is of valuable clinical importance as with routine determination of GB and AF the clinician can predict preoperatively the maxillary sinus mucosal thickness that may have practical implications for the related surgery. During preoperative planning it may impart a clear information on both technical intricacies of sinus surgery and resilience properties of the Schneiderian membrane. This may be more significant during maxillary sinus elevation procedures, if the sinus mucosa is thin, the operator's skill plays a vital role for clinical success. During membrane elevation, as well as condensing of the grafting material, every attempt should be made to adjust the pressure applied to the sinus mucosa to safeguard against membrane perforation. Further investigations are needed to confirm these distinguished results of the study related to GB and AF. A number of limitations of the study must be taken into consideration: difference between male and female participants were not determined, small sample size and cross-sectional design. However, in a study by AIMETTI, mentioned that sex differences has a definite correlation with the SMT, but due to less availability and social regulations of the area concerned, gender difference was not considered. Inherent limitations of CBCT imaging should also be considered, some studies reported that CBCT gives varied data of SMT but it is the most used method with clinical predictability for implant and sinus surgeries. Also, the edentulous areas were not considered since such regions did not have a proper reference point such as a maxillary first molar tooth.
| Conclusion|| |
Within the limitations of the study, it can be concluded that SMT is more in individuals with thick GB and with square AF. The thickness of Schneiderian membrane was positively correlated with GT. It can be suggested that preoperative evaluation of GB and AF will be helpful for diagnosis and treatment planning, as well as for minimizing complications during surgery, as it can give an insight to SMT. Also, limited CBCT imaging can be regarded as a valuable diagnostic method to evaluate anatomically demanding areas such as the posterior maxilla and maxillary sinus before apical surgery.
We authors are very thankful to Dentaly dental clinic and research center, Abha, KSA for CBCT scans.
Financial support and sponsorship
The authors extend their appreciation to the Deanship of Scientific Research at King Khalid University for funding this work through General Research Project under grant number (G.R.P.370/1439).
Conflicts of interest
There are no conflicts of interest.
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[Figure 1], [Figure 2], [Figure 3], [Figure 4], [Figure 5], [Figure 6], [Figure 7], [Figure 8], [Figure 9], [Figure 10]
[Table 1], [Table 2], [Table 3]