in vivo 29: 467-486 (2015)

The Nasopalatine in Adults on Cone Beam Computed Tomograms–A Clinical Study and Review of the Literature

REINHARD E. FRIEDRICH, FRANK LAUMANN, TOMISLAV ZRNC and ALEXANDRE T. ASSAF

Department of Oral and Craniomaxillofacial Surgery, Eppendorf University Hospital, University of Hamburg, Hamburg, Germany

Abstract. Aim: The aims of this study were to assess the sagittal plane only, but the technique allowed demonstration location, morphology and anatomical dimensions of the of all aspects using the combined 2D/3D interpretation. nasopalatine canal (NPC) on cone beam computed Conclusion: The NPC may exhibit important anatomical tomographic (CBCT) images and to compare our findings variations, both with regard to morphology and its with recent reports on this matter. A detailed knowledge of dimensions. To avoid any potential complications during anatomical variations is mandatory in skeletal surgery of the dentoalveolar surgery, careful preoperative evaluation is anterior . Patients and Methods: Two hundred CBCT required. 3D imaging is recommended to determine canal scans of the mid-facial region were analyzed from adult topography and dimensions, and to assess the individual patients at the Outpatient Clinic of the Department of Oral anterior maxilla’s dimensions prior to surgical procedures, and Craniomaxillofacial Surgery, University of Hamburg, such as dental implant insertion or augmentation. Germany. Patients were scanned using standard exposure time at normal patient positioning inside the CBCT device. The nasopalatine canal (NPC) is part of the anterior maxilla. Three-dimensional (3D) CBCT images were carefully Diseases of this bone can affect the NPC. In addition, the analyzed regarding NPC location, morphology and planning surgical procedures of the anterior maxilla is based anatomical dimensions, and variations of radiological on a detailed knowledge about this region. This study morphology, with respect to age and gender. Results: In the provides new information on the topography of the NPC sagittal plane, the NPC typically appeared as a canal with with special reference to a radiological and surgical a mean length±standard deviation (SD) of 11.15±2.87 mm. perspective. The oral cavity opening of the canal is the , with a mean diameter of 4.49±1.71 mm. At the entrance to Anatomy of the NPC. The paired NPC is localized in the the nasal floor, in most cases, two apertures were found (Y- anterior maxilla, close behind the central (1). The canal morphology), but also three or four openings were NPC forms a tube connecting soft tissues of the nasal and observed. In particular cases, the canal presented a oral cavities (2, 3). The oral aperture of the NPC lies in the cylindrical aperture with only one exit to the nasal floor. The anterior , just dorsal to the roots of the upper average width of the NPC at the level of the nasal floor was central incisors (3). The funnel-shaped opening to the oral 3.43±1.54 mm. The labiopalatal width of the NPC measured cavity is defined as the incisive foramen or fossa (1). Inside perpendicular to the long axis of the canal on sagittal plane the bone, the NPC divides in the cranial course into two was 2.48±1.33 mm. Interpretation of NPC morphology was tubes that run separately to the nasal aperture, termed nasal significantly different when analyzing the images in the foramina (4-7). The NPC contains fibrillary connective and adipose tissues (6), minor salivary glands (8, 9), and the and artery (10, 11). During its osseous passage, the artery maintains anastomoses with the major Correspondence to: Professor Reinhard E. Friedrich, MD, DMD, palatine artery (12). Occasionally, two additional small Ph.D., Department of Oral and Craniomaxillofacial Surgery, channels are found in the medial to the NPC Eppendorf University Hospital, University of Hamburg, Martinistr. (canals of Scarpa). These channels carry further nerve 52, D-20246 Hamburg, Germany. Tel: +49 40741053259, e-mail: filaments of the nasopalatine nerve, terminating in the [email protected] incisive foramen as Scarpa’s foramina. In the oral cavity, the Key Words: Nasopalatine canal, incisive canal, cone beam computed left supplementary channel opens anteriorly and the right tomography, maxilla, primary palate, radiological anatomy, implant posteriorly to the oral opening of the NPC (3, 13). The NPC dentistry, local anesthesia, dentoalveolar surgery. should not be confused with the paired nasopalatine or

0258-851X/2015 $2.00+.40 467 in vivo 29: 467-486 (2015)

Figure 1. Schematic representation of nasopalatine canal development according to Radlanski et al. (16), modifying illustrations of Bornstein et al. (13), axial aspect from caudal direction. The nasopalatine canal (sive incisive canal) is part of the developing primary palate and therefore the canal is located anterior to the sutura incisiva in the incisive bone (shown in B). A: Schematic drawing of the developing palate: The primary palate [1], contains the nasopalatine duct (dots). The palatine processes of the maxilla [2] have not yet conjoined in the medio-sagittal plane, leaving the gap open to the visible nasal septum [3]. B: Fused palate with two maxillary processes and incisive bone. The suture between the incisive bone and the fused palatine processes (incisive suture) is indicated as a v-shaped dotted line. The inset indicates the region presented in detail in C. C: Detail of inset shown in B: The nasopalatine canal at the 12th week of fetal development: 1: nasopalatine duct, 2: nasopalatine nerve, 3: nasopalatine artery. The nasopalatine duct is obliterated during further stages of physical development. However, remnants of the duct may persist up to post-natal life (14). The dotted line indicates the border with the fused palatine processes of the maxilla and the vertical line indicates the anterior end of the median palatine suture.

incisive duct (2, 14). This duct develops prenatally in the 6th (34, 35), topography (36), volumetry of the maxilla for to 12th fetal weeks from epithelia within the NPC and forms estimation of donor sites for bone grafts (37), computer- a temporary connection between the nasal and oral cavities aided manufacturing (38), and basic science in dentistry (39). during the 13th and 14th fetal weeks (15-17) (Figure 1). Some studies were recently published on the radiological morphology of NPC on CBCT images, revealing substantial Surgery of the anterior maxilla. Knowledge of precise variation in the radiological morphology of the canal (13, 40- anatomical descriptions, dimensions, and the location of the 48). The purpose of this study was to generate our own NPC is crucial in the fields of dentistry and oral and relevant data on the morphological characteristics of NPC maxillofacial surgery, e.g. for local anesthesia of the anterior derived from CBCT and to compare our findings with recent maxilla, and the planning of surgical procedures concerning radiological and morphological data on NPC anatomy this region, such as dental implant placement or apical root generated with different morphometric and imaging resection. Surgery in the anterior maxilla can give rise to techniques. Finally, we compared the measurements of contact of surgical instruments and implants with the current CBCT studies and findings derived from anatomical structures running through or close to the NPC (18-22). This dissections (49). situation may cause surgical problems (23, 24), and lead to sensory dysfunction (20, 25) or poor osseointegration of Patients and Methods implants. Patients. The NPC was analyzed on CBCTs of 200 adult patients (female: 94, male: 106; mean age=44.96 years, range=20-98 years) Radiology of the anterior maxilla. Computed tomographic undertaken at the Department of Oral and Craniomaxillofacial (CT) studies are performed to better visualize this anatomical Surgery, Hamburg University, Germany, between 2011 and 2013 region as a prerequisite to more precise surgery of the (Table I). The radiographs were made for diagnosis of dental or anterior maxilla (26-29). Within the past decade, limited diseases unrelated to the present analysis. We excluded cone beam computed tomography (CBCT) has become a patients from the evaluation who were subjected to radiography of useful tool for investigating the facial in detail (30). the anterior maxilla for cysts of the nasopalatine duct or had apical CBCT allows imaging of osseous structures with less jaw lesions in proximity to the upper incisors; likewise radiographs of patients with known craniofacial deformities or radiation exposure than conventional multi-slice CT (31). dental implants in the frontal maxilla were also excluded. This CBCT has already been widely applied for several study was approved by the Institutional Review Board of indications in the fields of oral and maxillofacial disciplines, Eppendorf University Hospital to fulfill the requirements for a such as trauma (32), periodontal disease (33), morphometry medical thesis in dentistry (FL).

468 Friedrich et al: Nasopalatine Canal Morphometry by CBCT

Table I. Age and gender of patients studied for radiological morphology of the nasopalatine canal.

Age (years) Female, n Male, n Total, n

20-29 33 29 62 30-39 11 14 25 40-49 14 20 34 50-59 13 16 29 60-69 13 18 31 70-79 7 4 11 80-89 2 5 7 90-100 1 0 1 Total 94 106 200

Cone beam computed tomography. All CBCTs were performed with the same equipment (3D Accuitomo 170, Model MCT-1 EX-1 F17; Morita MFG Corp., Kyoto, Japan). All images were made using ‘slow mode’ with 100 single projections over 2 min with a required exposure time of 18 seconds (360˚). Thickness of the performed slices was 1.00 mm, voxel size was 80-250 μm, and exposure volume 170 mm ×120 mm. Evaluation of all dental images performed pre- and postoperatively was carried out using iDixel™ 2.0 3D Imaging Software (J. Morita Europa GmbH, Dietzenbach, Germany). All images were evaluated by two maxillofacial surgeons (REF, TZ). To display the raw dataset, a 2.66 GHz Intel Xeon PC with 3.25 Gb RAM, Windows XP™ Professional operating system and a 27" Dell U2711H™ monitor with an image resolution of 2,560×1,600 pixels was used. All raw data were converted into three-dimensional data for single layer and three-dimensional evaluation in 1-mm layers. All measurements analyzed in this study were determined in three different imaging planes (sagittal, axial, coronal).

Sagittal plane measurements. As a first step, we inspected the sagittal planes of the anterior maxilla in order to determine the reference for the middle of the canal (Figure 2A). The selection of the sagittal reference plane as the plane imaging the center of the canal was verified using a 3D navigation tool that simultaneously displayed the current position in the axial plane (Figure 3). Anterior and dorsal reference points were the anterior and posterior nasal spines. Within the sagittal plane, we evaluated seven different measurement points to describe all anatomical relations of the NPC, such as the angle between the nasal floor and the longitudinal axis of NPC (Figure 4), the distance between the top of the and the buccal border of the NPC (Table II). A total of seven Figure 2. Measurement of the anterior maxilla, sagittal plane. A: Illustration of the measurement points (see Table III): 1: The nasal defined measurements were taken (Figure 2A and 4). Linear opening of the nasopalatine canal (NPC); 2: width of canal at its center; measurements of points 5 to 7 were performed perpendicular to the 3: diameter of oral opening of the incisive foramen; 4: length of the NPC centerline of the NPC depicted on the sagittal plane (Figure 3). measured along the center of the canal's long axis; 5: bone thickness from During a second step, grading and classification of the different the incisive foramen to the buccal cortical layer; 6: distance between the variations of the NPC course was performed within the sagittal buccal definition of the NPC and buccal cortical layer of the alveolar plane, using a classification proposed by Bornstein et al. (13). The process, the dorsal extension of this line is a tangent to the most caudal NPC was divided into five different types, consecutively numbered and dorsal bony definition of NPC and runs perpendicular to the long 1 to 5 (Figure 5A). Type 1 is NPC with a straight, predominantly axis line of the canal; 7: a line from the buccal cortical layer to the thin channel with parallel walls. Type 2 exhibits an increasing anterior definition of the NPC passing the canal at a point half its length. divergence of the walls towards the oral opening, whereas type 3 B: Graph of measurements made in the sagittal plane. C: Graph showing NPC exhibits a diametrically opposed divergence, towards the nasal the impact of gender on measurements made in the sagittal plane. opening. Type 4 NPC was applied in cases with a kinking of the *α<0.05, **α<0.01, ***α<0.001 comparing females with males.

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Table II. Measurement points of nasopalatine canal (NPC) in the sagittal plane. Measurements 5, 6 and 7 were performed perpendicular to the constructed longitudinal axis of the NPC in the sagittal plane.

Measurement point Anatomical structure

1 Diameter of nasal foramen 2 Diameter of the canal measured at the midpoint of longitudinal extension 3 Diameter of the incisive foramen 4 Length of the NPC from nasal to oral aperture 5 Distance between the anterior border of the incisive foramen and anterior cortical layer of the alveolar bone Reference point: Most caudal point of the anterior NPC wall at the incisive foramen, line is perpendicular to the long axis line of the NPC 6 Distance between the anterior border of the incisive foramen and the anterior cortical layer of the alveolar bone Reference point: Most anterior point of the anterior NPC wall at the incisive foramen 7 Distance between the anterior definition of the center of the NPC and the buccal side of the alveolar bone 8 Distance from the anterior nasal spine to the anterior wall of the nasal foramen (see Figure 4)

Table III. Definition of measurements made in the axial plane.

Measurement point Anatomical structure Measurement type, description

1 Diameter of nasal foramina (aggregated) Ø (mm) 2 Number of nasal foramina n, 1-4 3 Shape of nasal foramina Round/oval 4 Number of septa inside the NPC n, 0-4 5 Number of supplementary canals n, 0-2 6 Minimum distance between root of central and anterior definition of NPC Ø (mm)

tube. This kinking was observed in the cranial third of the channel Table IV. Dimensions of the nasopalatine canal and adjacent osseous and the redirection was posteriorly. Type 5 represents NPC with structures in the sagittal plane of cone beam computed tomograms of curved walls. This type is complementary to a deep intraosseous the anterior maxilla. Please refer to Table II for description of beginning of the foramina of both sides. The distribution of canal measurement points. types is shown in Table VII (No. 1 to 5 are applied for types identified in the sagittal plane). Measurement point

Axial plane measurements. In the axial plane, six parameters were Value (mm) 1 2 3 4 5 6 7 determined to characterize the NPC (Figures 6-9): measurement of the maximum diameter(s) at the nasal foramen (and their addition to Mean 3.43 2.48 4.49 11.15 6.74 6.73 7.48 the whole diameter), evaluation of the number of foramina at the Minimum 0.67 0.34 0.70 2.10 0.57 0.60 0.50 nasal opening (Figure 6), and description of the shape and course Maximum 7.72 9.16 11.41 19.80 10.00 9.80 12.97 of the canal (round vs. oval). Furthermore, the number of bone septa Standard deviation 1.54 1.33 1.71 2.87 1.60 1.50 1.61 within the NPC (Figure 7, and 8A and B) and the number of external canals was registered, the latter item being verified on sagittal sections (Figure 9). Finally, the minimum distance was measured between the dorsal surfaces of the central incisor roots to the anterior wall of the NPC, as illustrated in Figure 8A. In order to achieve reproducible results of nasal foramina measurements in Coronal plane measurements. In the coronal plane, we performed the axial plane, the maximum cranial layer was chosen that gave a two types of measurements. Firstly, the diameter was calculated at circular, i.e. complete, osseous boundary. Simultaneous depiction of the level of the NPC midline (Figure 10). Furthermore, a second the NPC in the sagittal plane revealed a measurement position at the typing of the NPC was applied as proposed by Bornstein et al. (13). cranio-dorsal definition of the nasal foramen (Figure 6). The number This classification is based on the number of nasal openings visible and size of the openings (Figure 7) and also septa of the lumen on CBCT and essentially differentiates three types of openings. (Figure 8A and B) were recorded with the help of simultaneous These authors classified three main NPC types (type a, b and c, depiction of the structure in perpendicular planes. In rare cases, a Figure 11A). Originally, group ‘c’ was subsequently divided into supplementary canal was noted (Figure 9). The definition of two sub-groups. However, Bornstein et al. mentioned these measurements are summarized in Table III. subgroups only briefly in their publication but did not evaluate

470 Friedrich et al: Nasopalatine Canal Morphometry by CBCT

Table V. Impact of gender on dimensions of the nasopalatine canal Table VI. Impact of age on dimensions of the nasopalatine canal (NPC) (sagittal plane). The comparisons of measurements reveal males (sagittal plane). The comparisons of measurements show statistically to have statistically significantly greater dimensions of the NPC at significant differences in values with respect to increasing age. Data are different measurement points. Data are the mean values±standard the mean values±standard deviation; level of acceptable significance deviation; level of acceptable significance was set at α=0.05. Please was set at α=0.05. Please refer to Table II for description of refer to Table II for description of measurement points. measurement points.

Measurement Female Male 95% CI p-Value Measurement Mean value 95% CI p-Value point (mm) (mm) (mm) point (mm) (mm)

1 3.27±1.49 3.57±1.56 −0.74 to 0.12 0.162 1 3.43 −0.014 to 0.009 0.703 2 2.28±1.24 2.67±1.39 −0.74 to −0.01 0.045 2 2.48 −0.004 to 0.015 0.273 3 3.96±1.29 4.96±1.90 −1.41 to −0.52 0.00002 3 4.49 0.015 to 0.039 0.00001 4 10.18±2.37 12.02±3.01 −2.60 to −1.08 0.000004 4 11.15 −0.220 to 0.190 0.900 5 6.36±1.54 7.10±1.58 −1.17 to −0.32 0.0012 5 6.74 −0.030 to −0.007 0.002 6 6.37±1.48 7.05±1.46 −1.11 to −0.29 0.0008 6 6.73 −0.024 to −0.002 0.018 7 7.24±1.56 7.69±1.64 −0.91 to −0.01 0.047 7 7.48 −0.015 to 0.009 0.924

CI = Confidence interval. CI: Confidence interval.

these types separately (13). In the present study, we examined the Table VII. Morphological variants of nasopalatine canal type with classification of NPC with cranial distributions more thoroughly. reference to gender by imaging in the sagittal plane (Types in the However, this analysis was not practicable before checking the sagittal plane are identified by numbers). simultaneous visualization of the NPC in the axial plane for reference in order to distinguish overlays. The typing of the NPC in Canal type Female (N=94), Male (N=106), Total this plane resulted in five main types identified by capital letters n (%) n (%) number (%) A-E (Figure 11A). Type 1 22 (23.4%) 15 (14.2%) 37 (18.5%) Statistics. IBM™ software SPSS™, version 21 (International Type 2 32 (34%) 27 (25.5%) 59 (29.5%) Business Machines, Armonk, NY, USA), was used for descriptive Type 3 8 (8.5%) 7 (6.6%) 15 (7.5%) statistics. The data were analyzed for significant differences as a Type 4 10 (10.6%) 21 (19.8%) 31 (15.5%) function of gender and age. Analysis of variance was applied for Type 5 22 (23.4%) 36 (33.9%) 58 (27%) values for measurement points 1 to 7 and the nasal floor/NPC angle in the sagittal plane, for values for measurement points 1 to 5 in the axial plane and values for measurement point 1 in the coronal plane. We used crosstab analysis for nominal variables, such as type of canal, septa and number of nasal foramina (Chi- Table VIII. Impact of gender on the distance between the anterior nasal square test). The significance level of calculated differences was spine and anterior (labial) wall of the nasal foramen (measurement set at α<0.05. point 8; see Table II) in the sagittal plane. Level of acceptable significance was set at α=0.05. Comparison of data. We compared the data to selected published results for NPC morphology: Bornstein et al. used CBCT for Gender Mean SD 95% CI p-Value descriptive morphology of the NPC (13). Measurement points 1-7 (mm) (mm) (mm) (sagittal plane) and canal typing in the coronal plane refer to the analysis tools published by this group and thus allow direct Female 13.11 2.12 −1.00 to −0.156 0.0075 comparison of results. Furthermore, the studies of Song et al. (29), Male 14.04 2.58 Mraiwa et al. (28), Jacobs et al. (3) and Liang et al. (27) were Total 13.61 2.41 selected to compare our data with corresponding data on NPC morphology derived from other imaging sources, i.e. spiral CI: Confidence interval for the mean difference between genders; SD: computed tomography (CT) (27, 28), high-resolution magnetic standard deviation. resonance imaging (MRI) (3), and micro-CT (29). Furthermore, we compared our data to recent studies on this subject also applying CBCT (40-48). If the definition of measurement points in these studies were the same as in the present study, the values were NPC. Therefore, we wanted to compare our results with findings compared in order to clarify possible effects of ethnicity, age or derived from volumetric experiments of the NPC of prepared gender on the radiological morphology of this distinct anatomical by Hassmann (49). In those experiments, the NPC was filled with unit. In addition, we compared our data with results derived from Xantopren™-blue (Heraeus-Kulzer, Weinheim, Germany). After conventional analyses prior to the implementation of removal of the bony shell, the hardened plastic was removed from computer-supported sectional imaging techniques for studying the the cavity and measured (49).

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Table IX. Frequency of variant numbers of nasal foramina in the axial Table XII. Distance between the upper central incisor roots to the lumen plane (measurement point 2; see Table III). of nasopalatine canal (minimum distance) with reference to gender (see Figure 8A). Gender had no impact on the distances measured in the Number of nasal foramina axial plane (p>0.05).

1234Gender N Mean±SD (mm)

Total (%) 36 (18%) 114 (57%) 38 (19%) 12 (6% Female 72 2.82±1.45 Female (n) 14 65 11 4 Male 87 3.02±1.23 Male (n) 22 49 27 8 Total 159 2.93±1.33

Table X. Frequency distribution of oval and round canal shapes with Table XIII. Impact of age on the distance between the dorsal interface respect to gender in the axial plane (measurement point 3; see Table III). of central incisor root to the nasopalatine canal lumen with respect to age as determined in the axial plane. The number of patients in this Canal shape analysis is lower than the total number of patients due to loss of upper central incisors in some individuals, predominantly in older patients. Round Oval Age (years) Mean (mm) Number of patients Total (%) 144 (72%) 56 (28%) Female (n) 60 34 20-29 2.27 59 Male (n) 84 22 30-39 2.72 21 40-49 3.11 26 50-59 3.59 24 60-69 3.96 21 70-79 4.00 7 80-89 − 0 Table XI. Gender- and age-specific distribution of the frequency of septa 90-100 − 0 inside the nasopalatine canal (axial plane) (measurement point 4; see Table III).

Number of nasal septa Table XIV. Mean values of the diameter of the nasopalatine canal in 01 2 4 the coronal plane with respect to gender. Total (%) 116 (58%) 15 (7.5%) 61 (30.5 %) 8 (4%) Gender Mean±SD (mm) N Female (N=94), n 56 5 30 4 Male (N=106), n 60 10 31 4 Female 3.19±1.09 94 Age (years), n (%) Male 3.18±1.19 106 20-29 32 (52%) 6 (10%) 21 (33%) 3 (5%) Total 3.18±1.14 200 30-39 12 (48%) 1 (4%) 11 (44%) 1 (4%) 40-49 12 (35%) 8 (24%) 12 (35%) 2 (6%) SD: Standard deviation. 50-59 22 (76%) 0 6 (21%) 1 (3%) 60-69 26 (84%) 0 5 (16%) 0 70-100 12 (63%) 0 6 (32%) 1 (5%)

crestal (measurement point 5)=6.74 mm, halfway down (point 6)=6.73 mm; apical (point 7)=7.48 mm]. The results are summarized in Table IV and illustrated in Figure 2B. Results The factors gender and age had an impact on the measurements: the thickness of the buccal lamella was Sagittal plane. The mean diameter of the nasal and oral dependent on gender (measurement points 5-7, Table V). The opening was 3.43 mm and 4.49 mm, respectively. The mean extension of the NPC was also dependent on gender, except diameter of the NPC in the middle of the longitudinal for measurement point 1: females had significantly lower extension was 2.48 mm, the narrowest site of the tube. The values than males (Figure 2C). In this study group, the mean NPC length was 11.15 mm. angulation of the NPC in relation to the nasal floor showed The investigation of the buccal lamella showed an increase no significant differences concerning gender. The impact of of bone diameter in the crestal to apical direction [mean values: age was less pronounced compared to gender; measurement

472 Friedrich et al: Nasopalatine Canal Morphometry by CBCT

Table XV. Frequency of nasopalatine canal types by imaging in the coronal plane.

Canal type, N (%)

A B C D E Total

Female 20 (21.3%) 17 (18.1%) 38 (40.4%) 14 (14.9%) 5 (5.3%) 94 (100.0%) Male 29 (27.4%) 15 (14.2%) 33 (31.1%) 20 (18.9%) 9 (8.5%) 106 (100.0%) Total 49 (24.5%) 32 (16.0%) 71 (35.5%) 34 (17.0%) 14 (7.0%) 200 (100.0%) Sum of C, D and E: 119 (59.5%)

Table XVI. Comparison between measurements reported in other studies and the current study. Please refer to Table III for description of measurement points. Data are mean values (mm).

Measurement point

Authors (Ref.) Imaging technique 1 3 4 5 6 7

Bornstein et al. (13) CBCT (N=100) 3.49 4.45 10.99 6.50 6.59 7.60 Mraiwa et al. (28) Spiral CT (N=34) 4.9 4.6 8.1 - - - Liang et al. (27) CT/MRI (N=120) - - 9.9 - - - Song et al. (29) Micro-CT (N=56) - - 11.5 - - - Present study CBCT (N=200 ) 3.43 4.49 11.15 6.38 6.39 7.66

CBCT: Cone beam computed tomography; MRI: magnetic resonance imaging.

points 2 and 3 decreased in value with increasing age, but all statistically significantly impacted by gender. However, the other values decreased in relation to age (Table VI). nasal opening was slightly smaller in females compared to The classification of NPC in the sagittal plane showed an males. A discrete age-dependent decrease in size of the nasal imbalance in the distribution of the findings with the five opening was found (0.002 mm/a, p=0.82). types of NPC shape (Table VII). Types 4 and 5 were more The number of nasal openings differed markedly (Table IX). frequently present in males, whereas types 1 and 2 were In this study, only 57% of NPCs had two nasal foramina. more frequently diagnosed in females. Type 3 NPC was by The shape of the NPC at the nasal opening was far the rarest finding in both sexes. There was no significant determined as round or oval; however, the caudal parts of the impact of age or gender on the type of NPC (Table VII and canal close to the nasal foramen were all round. A round Figure 5B). nasal opening was the prominent finding (Table X). The distance from the anterior tip of the nasal spine to the The number of septa inside the main canal also markedly anterior margin of the nasal foramen differed by gender and was differed (Table XI). The majority of NPC had no septa extended in males (female=13.11±2.12 mm; male=14.04±2.58), (n=114). Interestingly, we found 61 cases with a septum 95% confidence interval for mean difference: −1.00 to −0.156, separating the canal into two tubes. Higher numbers of septa p=0.0075) (Table VIII). This distance was about 0.579 mm were also noted (Table XI). The number of septa showed no shorter in females compared to males (Figure 4). However, this dependency on age and gender. However, in cases aged 50 distance varied substantially: the shortest distance was 6.32 mm, years or more, the number of septa decreased. Supplementary the largest 21.63 mm. There was no impact of age relevant for lateral canals were noticed in five cases only (Figure 9). The this item (p=0.398). The mean angle between the nasal floor supplementary canals were located anteriorly or laterally to (line from anterior to ) and the long axis of the main canal. The probability of diagnosing supplementary the NPC was 104.39˚. canals is about one in 40 and not a very rare finding. The narrowest distance between the apices of central Axial plane. Five measurement points were recorded in the incisors and the anterior border of the canal was determined axial plane. As a first step, we counted all nasal foramina and in 158 cases [42 cases were excluded due to loss of frontal measured the (summarized) maximum diameter(s). The teeth (n=30), and positioning of the dental roots caudal to the mean diameter of the nasal opening was 4.6±1.77 mm; incisive foramen (n=12)]. The mean distance was 2.92±1.333 females=4.42 mm, male=4.76 mm). This value was not mm) and not dependent on gender (p=0.524). However, age

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Figure 3. Illustration of the procedure to identify the layer for measurement with the assistance of simultaneous orientation by navigation lines in a second plane.

did influence the value significantly (p<0.0001). An increase in age increased the distance on average by 0.0036 mm per year (Tables XII and XIII) (Figures 8A and B).

Coronal plane. The coronal plane served for two analyses (Figures 10 and 11). The mean diameter of the NPC, as determined in the center of the longitudinal axis, was 3.18±1.4 mm (females=3.19±1.09 mm, n=94; males= 3.18±1.19 mm, n=106). The diameter of the NPC in the coronal plane showed no dependency on gender (Table XIV). Secondly, the classification of NPC types as proposed by Bornstein et al. (13) was applied (Table XV). The NPC types showed no gender-related frequency. The addition of NPC Figure 4. Anterior maxilla and nasopalatine canal (NPC), sagittal types C, D and E to one class of canal type accounted for plane. The short line is the line extending from the anterior nasal spine 119 (59%) cases (6). to the buccal (anterior) and most cranial border of the NPC. This posterior definition of the line is identical to the anterior and cranial Comparison of study data to those of other studies. The boundary of the nasal opening in the sagittal plane (measurement point no. 8, see Table II). The angled line on the right illustrates the comparison of the values of sagittal plane measurement points measurement of the angle of the nasal floor (horizontal line) to the line 1-7 (Table II) between the present study and that of Bornstein et passing through the center of the canal. al. (13) showed they matched strongly (Table XVI, Figure 12). The analysis of the selected references of the literature revealed that measurement point 4 was the only one applied in all studies (13, 27, 28, 29). The value of measurements age, but these correlations were not confirmed in every item. differed markedly between spiral CT and CBCT. Only The results of these studies are summarized in Table XVII. micro-CT values (29) exhibited minor discrepancies from our measurements. The results are summarized in Table XVI. Discussion Numerous studies investigated the NPC by CBCT (41-48). The definition of measurement points differed between This study provides relevant data on the NPC and studies. However, the studies reveal a wide spectrum of surrounding structures derived from CBCT images. The NPC forms of the channel, topographical relationships to adjacent shows age-dependent alterations of spatial relationship to structures, and some values are dependent on gender and incisors relevant for oral surgical procedures. Individual

474 Friedrich et al: Nasopalatine Canal Morphometry by CBCT

Figure 5. A: Types 1 to 5 of nasopalatine canal (NPC) determined in sagittal plane as proposed by Bornstein et al. (13). B: Frequency of NPC types determined on sagittal planes of cone beam computed tomography according to gender. Typing was performed according to (13).

variation of spatial parameters is high in this region, e.g. studies on this subject using CBCT imaging for visualization bone thickness, volume of NPC, and topography of the of the NPC point to ethnic differences in this anatomical channel to tooth roots (47). This study confirms the effect of region (43, 48). This effect was denied by others (47). gender on several morphological parameters of NPC (47). The present studied used the same evaluation protocol as CBCT allowed clear and artifact-free imaging of the relevant that of Bornstein et al. (13), with few modifications, and the structures. same radiological device. The distribution of age and gender The NPC is a paired canal forming two nasal apertures that is similar in both studies, allowing direct comparison of data. merge to a single channel towards the oral opening (1, 5, 6, In general, the differences between the measurements of both 11, 12, 50). However, this anatomical description applies only studies are small. Our measurements at points 1, 3, 4, 5, 6, to a subgroup of NPCs. The number of canals and nasal and 7 obtained from sagittal planes are practically identical foramina and the osseous septation inside the canal diagnosed to those of this reference study. This selection of points on CBCT illustrate the variability of the osseous anatomy in allows the quantification of maxillary bone anterior to the this region with respect to the floor plan of palate formation NPC as a prerequisite for dental implant positioning. by fusion of three bones (16), (Figure 1). Our data support Furthermore, these points allow the measurement of previous results indicating the close relationship of some characteristic data of the lumen of the NPC. The comparison anthropometric findings to age and gender (13, 46). Other to the results presented by Bornstein et al. (13) show minor

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Figure 6. Different numbers of nasal foramina according to measurement point 2 in axial plane analysis. A: 1; B: 2; C: 3; D:3.

discrepancies only with respect to findings obtained in the sagittal plane. These differences (measurement points 1-7) range between −0.12 mm and +0.16 mm and appear not to be of clinical significance. Our data confirm the dependency on gender of several measurements in this plane. The dependency of the measurements on age was restricted to Figure 7. Schematic drawing of septa inside the lumen of the three measurement points. The five types of the NPC course nasopalatine canal as visible on axial sections of cone beam computed in the sagittal plane demonstrate the high variability of this tomograms. The canal can have a clear lumen, be separated into halves, structure in humans and the frequency distribution of this divided into three parts or may even be quartered (from left to right). item even varies between studies using the same classification of NPC (13, 46) (Table XVII). On the other hand, the typing of the NPC in the coronal plane revealed results different from those of the reference The typing of the NPC in the coronal plane also reflects study. In order to allow direct comparison of data, types C, D the high variability of the NPC shape, as already reported by and E of our study are equivalent to the type C category of others (7, 13, 19, 27, 28). Furthermore, we typed the NPC the previous study (13). Applying these criteria, the number into five classes in the coronal plane with respect to the of NPCs with one canal and two, three or four nasal openings variation of nasal openings. Up to four nasal openings were constitutes the largest group (about 60%) compared to 40% recorded on CBCT images. In order to determine these (13). One reason for the difference between these studies variations of NPC morphology, the complementary imaging could be the assistance of image interpretation using the axial in the axial planes was mandatory (28). The most prominent plane for comparison in our investigation. Overlays of type of NPC is a canal with two nasal openings. However, openings and side channels were more easily detectable using this configuration accounted only for 35.5%. The number of planes perpendicular to each other rather than single-plane nasal floor foramina is highly variable, e.g. Liang et al. found analyses. up to four foramina in only 1% of their sample (27); on the

476 Friedrich et al: Nasopalatine Canal Morphometry by CBCT

Figure 8. Septa of the nasopalatine canal, axial plane. Canal with one (A), three (B) and four (C) septa. The line in A illustrates the measurement of the minimum distance between the central incisor root and the canal wall. D: Narrowest distances between the incisor root and the nasopalatine canal according to age and gender (axial plane).

Figure 9. Separate additional canal anterior to the nasopalatine canal Figure 10. Measurement of the diameter at the height of the middle of (sagittal plane). length of the nasopalatine canal, C-type of nasopalatine canal, coronal plane. Section was verified by simultaneous imaging of the canal in a second plane.

other hand, Thakur et al. found a considerably higher number attributable to different imaging techniques (29), definition of of nasal openings on CBCT images (40). At present, it is not terms (29, 43), or combinations thereof. clear whether the high number of anatomical variations of Our data show the narrow position of the central incisor nasal openings of NPC represents ethnic differences or are roots to the NPC that is 2.9 mm on average (Table XII) and

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Figure 11. Types of morphology of the nasopalatine canal (NPC). A: Comparison of schematic representations of NPC types according to Bornstein et al. (13). The lower images (a-c) show the original classification, but only three were further analyzed (13), compared to the classification used in the current study (types A-E) with representative radiographs (top). The classification reflects the visualization of the branches of the radiolucent tube connecting the nasal floor and oral cavity in the coronal plane. However, the distinction of nasal openings of the NPC required additional imaging in the axial plane, in particular in order to identify types D and E (see radiographs above). B: Comparison of the frequencies of NPC types between the reference study (13) and the current investigation revealed major differences (coronal plane).

similar to the findings reported by Chatriyanuyoke et al. Nevertheless, digital measurement of skull anthropometric (36). On the other hand, the mean distance between the relationships proved to be highly precise (52, 53) and the central incisor root apices and NPC was calculated as distances between the roots of upper jaw incisors and NPC 7.4±0.1 mm, based on saw cuts of human skulls (51). differ with respect to root angulation and course of the canal.

478 Friedrich et al: Nasopalatine Canal Morphometry by CBCT

Figure 13. Terminology of the nasopalatine canal (or incisive canal) as proposed by Jacobs et al. (3).

Figure 12. Comparison of measurements (mean values) between the reference study (13) and the current investigation revealed only minor differences (sagittal plane). range from 8 to 13 mm (54). Recently, Al-Amery et al. reported a mean NPC length of 16.33±4.43 mm and a slight but significant difference between males and females (47). Other authors described sexual dimorphism for canal length In the axial plane, the shortest distance was measured on sectional images (43, 44). However, the individual between the incisor root and the lumen of the NPC. An variability of NPC length was considerably high in both important result of our investigation is that the mean values sexes (44, 47). Age had no impact on NPC length according of this distance differed between the group of individuals to some authors (47), but others revealed an impact of age aged 20 to 29 years and the group aged more than 70 years on this dimension: some revealed an age-dependent decrease by 1.73 mm on average, revealing an increase of this (13) and others an increase (27). distance with increasing age (Table XIII). However, males Some studies revealed the close association of edentulism had higher buccal bone thickness than females, both of the anterior maxilla with decreased NPC length and concerning length and width of the bone anterior to the NPC buccal bone dimensions (27, 44, 48). On the other hand, (10, 44, 48). This findings was confirmed in other studies, neither the length (13) nor the diameter of NPC were altered but without statistically significant difference (46). with respect to presence or absence of upper jaw frontal teeth Interestingly, distinct bony septa were noted inside the canal (48). However, Mardinger et al. demonstrated the expansion evaluated on axial views of the skull. With reference to the of the canal width consequent to tooth extraction (54), but number of septa, four types of NPC were registered: canals this findings was not supported by recent studies (27, 48). without septa, and those with one, three or even four septa. A Further studies emphasized that age had no effect on NPC total of 43% of NPCs exhibited this variation. Within this length and diameter (28, 43, 44). subgroup, NPC with three septa dominated (n=63). On the Measurement of the canal width is important to define other hand, NPC with four septa were noted eight times and intraluminal pathologies (28). A diameter of up to 6 mm is NPC with one septum in 16 cases. This finding was not suggested to be within the normal range; diameters larger associated with age or gender. Nevertheless, the number of than 10 mm are suspected to indicate a pathological process, septa decreased with age, particular in individuals older than in particular nasopalatine duct cyst (28). On the other hand, 50 years (p>0.05). The detection of septa is strongly the mean diameter of cysts of the NPC is about 17.1 mm dependent on the resolving power of the imaging system (29). (55). The present study and others reveal a high range of NPC diameters diagnosed in individuals without associated Length and width. The mean length of NPC was 11.15 mm pathological findings of the anterior maxilla (excepting tooth in the present study. According to current radiological reports loss). These sectional imaging studies on NPC bring into on NPC morphology, the length of the canal is expected to question the definition of osteolytic bone processes arising

479 in vivo 29: 467-486 (2015) Continued in lower in lower parameters. were obliterated. and dental status (incisors) on several (incisors) on several Table XVII. Table ‡ (28.8%) gender. but n=2.08-2.14 specific n=2.08-2.14 specific (age-dependent) differences. (n.s.) in (Bone thicker (sagittal) dentate patients) † 4: 13 (2.7%) 4.85±1.41/ 19 (3.9%) presence and not vs. round: 50%, 2: 10.4%, fused to one ovoid: 34.2%,ovoid: 3: 2.6% lobulated: 15.8%lobulated: parts of NPC plane) and shape foramina/canals (mm) n (%) tree branch 3.25±5** 5.26±1.51 NPC Ten on age. NPC Nasal opening palatal: 3.15) third of NPC, gender . (nasal fossa: 42, vertical: lateral 3: 13%, (range predo- canal division vs (sagittal) 2.32, level: 1 curved: F/M: n.s. in upper plane showed 10.96*** 2.86, mid- 4, vertical diameter) 4: 2% 1.40-5.90), minantly in coronal 11.26±2.86*** tree-branch 2.63±1.15** 4.33±1.38 C: 106 values, F/M: 10.24±2.19/. > cylindrical 2.39±1.04/ 3.85±1.41/ (9.8%), measurement (N=319) sagittal) (N=133), edentate) banana-like for impact of age, F/M=413/312 Northern Cyprus (probably (axial) ethnicity gender, 38, n.d. Korea 15.87±2.92 − n.d. 3.89±1.06, 1: 87%, 3.49±0.76 n.d. †All canals 490 46.1 Turkey Mean: 12.59±2.89, n.d. > Hourglass 3.09±1.25, 1: 217 (44.3%), Mean: 1 Canal: Length of NPC 50/5047/33 (range 18-42) (range 4.60-15.70), 2.78±0.85 slanted curved: (medio- 12.80±2.17 2: 81%, 3.62±0.94 typing, of and level 3.06±1.16 6.10±1.47 bone thickness. 12/26 F/M= 13.50±3.01*** banana > cone 2.93±1.19 3: 72 (14.7%) F/M: 2 Canals: central incisor 516:417 M: 41.37± Spain (N=310), 11.96±2.73*/*** 2.43±0.85/ funnel-like> CBCT and spiral 176/192 (range 6-15) 10.83±2.56 banana > cone 2.53±1.09; 2: 60, 4.13±1.40, (61.4%), group: age had 240/250 > cylindrical . Literature review of radiological findings of the nasopalatine canal (NPC) based on cone beam computed tomographic studies. of the nasopalatine canal (NPC) based on cone beam computed tomographic findings of radiological review . Literature (2011) F/M= 10.99±0.27, F/M: 3.37/3.65 F/M: B: 15, status on buccal et al. et al. Güncü et al. 933,F/M= (2012) (48) F: 40.14±15.58, (N=171), Turkey F/M=10.39±2.47/ F/M= Cylindrical > 15.80; n.d. Arabia Saudi (dentate/ n.d. 2.79±0.94* > hourglass-like n.d. n.d. Based on both CT images. Data Bornstein et al. 100,(13) 43.09±19.88 Switzerland 56/44 Mean: n.d. n.d. F/M=10.41/11.73 Mean: 3.49 n.d. Mean: 4.45, A: 45, Impact of dental (n.s.) (sagittal) 4.38/4.55 C: 40 bone thickness Etoz (2014) (43) (500), (range: 17-77) F/M: 11.64±2.43/ funnel > F/M: 2: 188 (38.4%), 5.06±1.48, 471 (96.1%), depends on Thakur et al. 100, F/M=(2013) (40) Range 20-86 India Mean: 10.08±2.25 Zhou et al. Mean: (2013) (41) 80, F/M= Slanted: 49, 23.08±6.30 Sekerci 1.75±0.77 et al. 368, F/M= China(2014) (42) 11.23 1: 4%, Mean (axial): Mean: F/M: 9.20 Turkey No Only NPC length n.d. Mean: n.d. n.d. Mean: Funnel > (range 2.40-16.06), Mean: n.d. > hourglass 1: 290, Mean: F/M: Mean: n.d. A: 226 3: 18 thin labial Very Pediatric age F/M: B: 36 no impact on Table XVII Table Authors (Ref.) N, genderKim (2004) (67) Age F/M= (years) Country Length Diameter (mm) Shape (mm) Diameter (sagittal No. or (mm) Oral of Frequency percent of Remarks opening canal types,

480 Friedrich et al: Nasopalatine Canal Morphometry by CBCT on gender, age on gender, <0.001 surfaces of NPC; surfaces and dental status. p some values depend some values ‡ B: 10 C: 64 measurements. Other: shape/axial 3 (1.2%) classification. (8.19%), <0.01 and *** (52.45%) p E: 1 (0.4%), and coronal D: 7 (3.1%), classification <0.05, ** p (elliptical) direction found. 2.80, mesio- canals excluded. § s.: not significant. * s.: not significant. diameter and volumes gender on and calculated no impact of measurements plane) and shape foramina/canals (mm) n (%) (66.07%) > 5: 1 C: 95 Association of vertical (33.93%)vertical (42.4%), sagittal NPC <0.015 65.2% > F/M: n.s. 2: 34.4%, palatal: foramina/ patients p NPC Nasal opening 13.16±2.72 banana. Slanted 4: 7, (10.3%), dimensions. 11.92±2.74 than in females *** straight (32.6%) distal: 3.49 No ‘vertical’ 56/66 11.02±2.4,44/46 (Malay and 4.51-30.24), F/M: 3.02±1.0some 3.29±1.0 (39.34%), on 116/108 (range 18-84) (range: 4.35-23.57), > hourglass 2: 131, (41.1%), impacted on 252, F/M= 48 (range Turkey F/M: n.d. n.d. Mean: F/M= n.d. Mean F/M= n.d. Data on the relation . Continued. et al. et al. et al. Coronal plane (13); §no correlation between number of channels and length or width; F/M: Female to male; n.d.: not detailed; n. Table XVII Table Authors (Ref.) N, genderAcar (2014) (44) 137/115 Age (years) 19-75) Country Length Diameter (mm) 9.04/10.20 Shape (mm) Diameter (sagittal No. or (mm) Oral of Frequency percent of 3.03/3.12, Remarks opening canal types, ‡ 3.72/4.14 between linear (2015) (47) Chinese groups) longer in males slanted- 3: 1% López Jornet 122, F/M= (2014) (45) >18 Fernández- 224 F/M= Alonso 47.28±15.41 Spain(2014) (46) Spain Mean: Mean: 12.34±2.79 n.d.Al-Amery n.d. Cylindrical > 90, F/M=et al. F/M: 10.20±2.53/ n.d. 15-75 n.d. Malaysia 1: 58, 16.33±4.43 (range: Mean: F/M: 11.58±2.64/ 3.85±1.32, Slanted-curve: 6.06±3.00, n.d. n.d. 1: 64.4%, A: 92 > funnel-like Labio- Mean: Dental status See no. of A: 48 Gender had impact Edentulous 3: 27, B: 23 bone plate buccal

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Table XVIII. Comparison of frequencies of different canal types of the nasopalatine canal as defined with different imaging techniques in the coronal plane.

Canal type, n (%)

Study A B C D+E C+D+E

Present (N=200) 49 (24.5%) 32 (16%) 71 (35%) 48 (24%) 119 (59.5%) Bornstein et al. (13) (N=100) 29 (45%) 15 (15%) − − 33 (40%) Mraiwa et al. (28) (N=34) 8 (23.5%) − 22 (64.7%) 4 (11.8%) 25 (76.5%) Liang et al. (27) (N=120) 53 (44%) − 47 (39%) 20 (17%) 67 (56%)

from the NPC based on skeletal normative values only. External canals. In recent studies on radiographic imaging Indeed, clinical symptoms have to be considered prior to of the anterior maxilla and NPC, some authors pointed to the diagnosis of a nasopalatine ductal cyst and histological fact that external canals are present on sectional images in investigation is mandatory (56) but will confirm respiratory close proximity to the NPC. These studies investigated both epithelia in a small subset of cases only (55). axial and sagittal planes of the region. In our study, only five individuals had structures fulfilling diagnostic criteria of Nasal foramen. The terminology of the nasal opening of the accessory canals (2.5%). In comparison to recent studies NPC (or incisive canal) is still controversial (29). Throughout reporting rates of 15.7% (20) and 27.8% (21), our findings this study, we adhere to describing the cranial termination of reveal a significantly lower rate of this variant. Both studies the canal as the nasal opening or foramen. We agree with the point to the fact of close associations between these canals proposal of Jacobs et al. (3) and others defining the nasal and the canalis sinuosus. The discrepancies between our opening alternatively as Stensen's (or Stenson's) foramen, findings and the literature are partly explained by the giving credit to a pioneer of human anatomy (Figure 13). evaluation criteria: we defined an accessory canal only if However, survey of the literature reveals that not all authors present adjacent to the NPC and with clear evidence for use the anatomical terms for the NPC in the same way (29). continuous intra-osseous tube formation with opening of the The width and number of nasal foramen showed no canal to the nasal floor. However, we agree with the dependency on age (43). The mean width of the incisive conclusion of these authors that recent findings of additional foramen exceeds the mean width of the nasal foramen, but canals could have some impact on treatment planning in this the range of the parameter width is high in both sexes (47), region and the evaluation of patients with sensory disorders despite several reports detailing sexual dimorphism of nasal of the anterior maxilla (57). The very careful search for foramen width in humans on CBCT (Table XVII). anatomical variations of the anterior maxilla enabled by CBCT provides insight into the variability of its Incisive foramen. Width of the incisive foramen of less than 6 neurovascular supply (20). mm is rated as representing anatomical variations of the ostium. Pathologies are expected in foramina with diameters of 10 mm Imaging of NPC by other techniques (Table XVIII). Further or more (28). The mean values of the incisive foramen are researchers have investigated the NPC by different within the expected width for normal anatomy of the ostium techniques (3, 28, 29, 49). These results are compared to our (Table XVII). For example, in one study, the mean incisive findings. Song et al. (29) performed a three-dimensional ex foramen width was calculated as 3.85 mm, but the range was vivo study on the maxilla of 55 human cadavers using micro- 1.50 to 7.20 mm (46). The mean incisive foramen width in CT. These authors also investigated histological sections of males exceeds that of females (46). Sexual dimorphism of the the same specimen in order to detail the soft-tissue incisive foramen with respect to width of the ostium becomes compartments of NPC. The only measuring point identical evident after comparison of data from several studies (Table to our protocol is the measurement of the NPC length. The XVII), but other authors did not reveal different diameters of mean value was 11.5 mm and the value closest to our the incisive foramen with respect to gender (13). The width of corresponding CBCT measurements of NPC. The axial plane the incisive foramen was purported to be correlated with the analysis was performed in the central section of the NPC presence of teeth of the upper jaw. Some authors argued that allowing for no classification of the nasal foramina (29). extraction of teeth associated with enlargement of the sinus According to our findings, the branching of the NPC into could also induce expansion of the incisive foramen (54), but three or four nasal openings takes place in much more this hypothesis did not stand the test of time (43, 48). cranial sections. In the central section of NPC, a distinction

482 Friedrich et al: Nasopalatine Canal Morphometry by CBCT of canal types is restricted to type A and B, probably to type Table XIX. Comparison of measurements of this study to the C in some cases. However, type D and E are not visible in morphological findings of Hassmann et al. (48). the central section of NPC. On the other hand, Song et al. Present study Hassmann et al. (48) Difference described up to four very small channels inside the central section of NPC (29). Their description of a measuring point Length (mm) N=200 N=76 to determine the number of nasal openings means that this Mean 11.15 14.6 3.34 classification probably does not refer to the number of nasal Maximum 19.80 21.5 1.70 openings but to the number of tiny channels inside the main Minimum 2.10 7.00 4.90 Width (mm) N=200 N=32 canal. On CBCT, respective structures showing probably Mean 3.18 4.18 1.00 these channels were only visible as radiopaque particles but Maximum 6.33 7.00 0.67 not as a constant structure. Indeed, the phenomenon has been Minimum 0.7 3.00 2.30 reported also by these authors comparing radiological and Shape N=200 N=34 histological findings (29). The distribution of these septa are Round 72% 70.59% 1.41 Oval 28% 29.41% 1.41 similar in both studies. The predominant findings is a NPC without septa, followed by NPC with three or two lumen. Four lumen are the most rarely reported finding (Table XI). The comparison of the image quality, the quality of 3D reconstruction and analytical tools between the CBCT of living individuals and a micro-CT study of cadaveric partial Hassmann used dried skulls of an anatomical collection to maxilla, including the NPC, for experimental imaging study the extension of the NPC (49). He filled the space with revealed a more detailed imaging for the micro-CT. Xantopren™-blue and measured the cured plastic material Nevertheless, the quality differences of imaging between representing the canal from the nasal to the oral opening by both techniques were probably beyond clinical needs. means of a caliper. Furthermore, he classified the shape of Mraiwa et al. studied NPC morphology with spiral CT in the NPC. Interestingly, both length and width measurements 2D and 3D (28). The study group was small (n=34) and the of the NPC differed by up to 3.34 mm from our results measurements showed the largest differences from our (Table XIX). However, the number of specimens is too low findings (Tables XVI and XVII). Differences were about to draw any far-reaching conclusions concerning the quality +1.47 to −3.05 mm. These authors categorized the NPC into of direct morphological study of skull specimens in four types. The Y-shaped canal, comparable to our type C, comparison to CBCT images. was present in 64.7% (28). Bucco-palatine bony thickness in Our results support current assessments of the the upper incisor region was measured by CT. The thickness questionable quality of the anterior maxilla for maxillary varied considerably and the mean value (6.81 mm) is similar surgery, in particular implant dentistry in edentulous patient. to the mean values of other studies. However, the number of Indeed, Bornstein et al. reported the effect of missing upper investigated NPCs is small and the authors presented no incisors on the reduction of the horizontal width of the further specifications, e.g. age-dependent reduction of the buccal lamella (13). Furthermore, in this region, surgeons anterior-posterior extension of the buccal lamella. have to consider the impact of sexual dimorphism on bone Jacobs et al. investigated four human maxilla specimen for volume and topographical relationships. neurovascular structures inside NPC using high-resolution MRI (9.4 Tesla) (3). This procedure precisely visualized the Surgery. Artzi et al. have shown a technique to circumvent vessels and nerves inside the NPC, which is not possible on the scarce volume or low quality bone bed in this region by CBCT images. They compared the images with consecutive simultaneous insertion of dental implant and cortico- histological slices of the region of interest (n=4). They spongious bone graft in a perforated NPC (18). Furthermore, presented results of an ex vivo micro-anatomical study but Verardi and Pastagia described a procedure to apply provide no metric data for NPC based on MRI. They alloplastic bone transplant to the anterior maxilla in cases described the incisive foramen and branches sprouting out to with poor bone volume and enlarged NPC (59). This both sides containing connective tissues and blood vessels, but technique allowed implant placement in the central incisor also noted poor definition of bony walls. These authors region (59). Furthermore, CBCT was introduced as a concluded high-resolution MRI to be suitable for planning tool even to harvest bone in this region in the case distinguishing neurovascular structures inside the NPC but of insufficient bone volume at the implant site: a 2 mm emphasized the important limitations of this technique for safety margin around the nasopalatine canal was proposed to routine application (limited scanning volume, long acquisition preserve enough space for neurosensory function (37). On time, and high costs) (3). Probably MRI is useful to investigate the other hand, some reports point to difficulties arising from patients suffering from post-surgical neuralgia (58). the close relationship of dental implants and periodontal

483 in vivo 29: 467-486 (2015) pathologies to the NPC (60-63). These reports should alert cone-beam computed tomography. Clin Oral Impl Res 22: 295- the clinician to carefully investigate the anterior maxilla prior 301, 2010. to surgical treatment. In contrast to these reports calling for 14 Jacob S, Zelano B, Gungor A, Abbott D, Naclerio R and McClintock MK: Location and gross morphology of the increased caution in surgical procedures adjacent to the nasopalatine duct in human adults. Arch Otolaryngol Head Neck canal, other authors even use the NPC as a buttress for Surg 126: 741-748, 2000. implant retention (23, 24, 64, 65), but long-term follow-up 15 Kitamura H: Embryology of the Mouth and Related Structures. of these procedures needs to be reported. Development of Nasopalatine Ducts. Maruzen, Tokyo, pp. 153- 155, 1976. Conclusion 16 Radlanski RJ, Emmerich S and Renz H: Prenatal morphogenesis of the human incisive canal. Anat Embryol 208: 265-271, 2004. The NPC is a highly variable anatomic unit of the anterior 17 Bellairs AD: Observations on the incisive canaliculi and maxilla. The dimensions and topography of the NPC are nasopalatine ducts. Br Dent J 91: 281-291, 1951. 18 Artzi Z, Nemcovsky CE, Bitlitum I and Segal P: Displacement precisely imaged with CBCT. Whereas there is growing of the incisive foramen in conjunction with implant placement evidence from several studies for sexual dimorphism of some in the anterior maxilla without jeopardizing vitality of parameters of the NPC, the individual variability of the canal nasopalatine nerve and vessels, a novel surgical approach. Clin and its relationship to anterior maxillary teeth may exceed by Oral Impl Res 11: 505-510, 2000. far expected mean gender-specific values. CBCT is an 19 Liang X, Lambrichts I, Corpas L, Politis C, Vrielinck L, Ma GW established diagnostic tool in oral and maxillofacial imaging and Jacobs R: Neurovascular disturbance associated with implant (66). CBCT enables determination of volume and topography placement in the anterior and its surgical implications. J Dent Res 11: 56-64, 2008. in implant dentistry of the anterior maxilla (36, 44, 67) and 20 Oliveira-Santos C, Rubrira-Bullen IRF and Monteiro SAC: allows individual adaptation of surgical procedures in this Neurovascular anatomical variations in the anterior plate complex region (57). observed on CBCT images. Clin Oral Implants Res 24: 1044- 1048, 2013. References 21 Von Arx T, Lozanoff S, Sendi P and Bornstein MM: Assessment of bone channels other than the nasopalatine canal in the anterior 1 von Lanz T and Wachsmuth W: Praktische Anatomie. Vol. 1. maxilla using limited cone beam computed tomography. Surg Springer, Berlin-Heidelberg-New York, pp. 186-188, 1985. 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62 McCrea SJ: Nasopalatine duct cyst, a delayed complication to 66 De Vos W, Casselman J and Swennen GR: Cone beam successful dental implant placement: diagnosis and surgical computerized tomography (CBCT) imaging of the oral and management. J Oral Implantol 40: 189-195, 2014. maxillofacial region: a systematic review of the literature. Int J 63 Mealey BI, Rasch MS, Braun JC and Fowler BC: Incisive canal Oral Maxillofac Surg 38: 609-625, 2009. cysts related to periodontal osseous defects. J Periodontol 64: 67 Kim GT, Hwang EH and Lee SR: A study of incisive canal using 571-574, 1993. cone beam computed tomography. Korean J Oral Maxillofac 64 Peñarrocha M, Carrillo C, Uribe R and García B: The Radiol 34: 7-12, 2004. nasopalatine canal as an anatomic buttress for implant placement in the severely atrophic maxilla: a pilot study. Int J Oral Maxillofac Implants 24: 936-942, 2009. 65 Waasdorp J: Enucleation of the incisive canal for implant Received March 27, 2015 placement: a comprehensive literature review and case report. J Revised May 8, 2015 Oral Implantol 2014 Dec 23. [Epub ahead of print] Accepted May 11, 2015

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