Simone F. M. Janner Characteristics and dimensions of the Marco D. Caversaccio Patrick Dubach Schneiderian membrane: a radiographic Pedram Sendi analysis using cone beam computed Daniel Buser Michael M. Bornstein tomography in patients referred for surgery in the posterior maxilla

Authors’ affiliations: Key words: cone beam computed tomography, dental implants, mucosal thickness, posterior Simone F. M. Janner, Daniel Buser, Michael M. maxilla, Schneiderian membrane, sinus floor elevation, volume tomography Bornstein, Department of Oral Surgery and Stomatology, School of Dental Medicine, University of Bern, Bern, Switzerland Abstract Marco D. Caversaccio, Patrick Dubach,ClinicforEar, Objectives: To determine the dimensions of the Schneiderian membrane using limited cone beam Nose and Throat Diseases, Head and Neck Surgery, Bern University Hospital, University of Bern, Bern, computed tomography (CBCT) in individuals referred for dental implant surgery, and to determine Switzerland factors influencing the mucosal thickness. Pedram Sendi, Institute for Clinical Epidemiology & Material and methods: The study included 143 consecutive patients referred for dental implant Biostatistics, Basel University Hospital, Basel, Switzerland placement in the posterior maxilla. A total of 168 CBCT images were taken using a limited field of view of 4 4cm,6 6 cm, or 8 8 cm. Reformatted coronal CBCT slices were analyzed with regard to the Corresponding author: thickness and characteristics of the Schneiderian membrane in nine standardized points of reference. PD Dr Michael M. Bornstein Department of Oral Surgery and Stomatology Factors such as age, gender, or status of the remaining dentition that could influence the dimensions School of Dental Medicine of the Schneiderian membrane were evaluated using univariate and multivariate linear regression University of Bern Freiburgstrasse 7 models. 3010 Bern Results: The thickness of the Schneiderian membrane exhibited a wide range, with a minimum value Switzerland of 0.16 mm and a maximum value of 34.61 mm. The highest mean values, ranging from 2.16 to Tel.: þ 41 31 632 25 45/66 Fax: þ 41 31 632 09 14 3.11 mm, were found for the mucosa located in the mid-sagittal regions of the maxillary sinus. The e-mail: [email protected] most frequent mucosal findings diagnosed were flat thickenings of the Schneiderian membrane (62 positive findings, 37%). For the multivariate linear regression model, only gender had a statistically significant influence on the mean overall and mid-sagittal thickness of the sinus mucosa. Conclusion: There is great interindividual variability in the thickness of the Schneiderian membrane. Gender seems to be the most important parameter influencing mucosal thickness in asymptomatic patients. Future studies are needed to assess the therapeutic and prognostic consequences of mucosal alterations in the maxillary sinus.

Since the first description in 1998 (Mozzo et al. pekar et al. 2008), CBCT imaging is becoming 1998), cone beam computed tomography (CBCT) more popular (Ziegler et al. 2002; Bremke et al. has become a popular and important technique 2008). for diagnosis and treatment planning in dental The placement of endosseous dental implants medicine (Ziegler et al. 2002; Bremke et al. has become an established and very common 2008). It has already become an established surgical procedure in dentistry over the past three diagnostic tool for some indications, such as decades. In the posterior maxilla, reduced endodontics (Lofthag-Hansen et al. 2007; Patel height and low bone density are the most com- 2009), dental traumatology (Bornstein et al. mon limitations for implant placement (Jemt & 2009), apical surgery (Rigolone et al. 2003; Low Lekholm 1995). Sinus floor elevation (SFE) pro- et al. 2008; Bornstein et al. 2010), challenging cedures have been documented as predictable Date: Accepted 7 December 2010 periodontal bone defects (Misch et al. 2006; Kasaj surgical options to overcome this obstacle (Born- & Willershausen 2007), preoperative planning of stein et al. 2008). Radiographic findings that To cite this article: Janner SFM, Caversaccio MD, Dubach P, Sendi P, Buser D, furcation surgery (Walter et al. 2009), and dental sometimes may pose problems for the surgeon Bornstein MM. Characteristics and dimensions of the implant surgery (Guerrero et al. 2006). Even for planning an SFE procedure with or without Schneiderian membrane: a radiographic analysis using cone beam computed tomography in patients referred for dental visualization of the paranasal sinuses, for which simultaneous dental implant placement are the implant surgery in the posterior maxilla. conventional computed tomography (CT) is con- presence of bony septa (Naitoh et al. 2009), Clin. Oral Impl. Res. xx, 2011; 000–000. doi: 10.1111/j.1600-0501.2010.02140.x sidered the diagnostic method of choice (Fatter- thickening of the Schneiderian membrane, prior

c 2011 John Wiley & Sons A/S 1 Janner et al Characteristics and dimensions of the Schneiderian membrane destructive maxillary sinus surgery (e.g., Cald- well-Luc operation), and manifest pathology such as acute rhinosinusitis or neoplastic processes (van den Bergh et al. 2000). There is only limited knowledge of the mean thickness and the dimen- sion of the Schneiderian membrane, and there are no guidelines for assessment and classifica- tion of mucosal findings in the maxillary sinus before SFE. The objective of the present study was to analyze the thickness and the anatomic charac- teristics of the Schneiderian membrane using limited CBCT in patients referred for dental implant placement in the posterior maxilla. Ad- ditionally, the influence of age, gender, smoking habits, periodontal and endodontic findings, and thetimeperiodelapsedsincethelasttooth Fig. 1. Location of the measurement regions in the sagittal cone beam computed tomography slices: anterior region (a; PM1, removal in the region of interest on the dimen- first premolar; PM2, second premolar), middle region (m; M1, first molar), and posterior region (p; M2, second molar; M3, third molar). Patient with a distal extension situation in the left posterior maxilla (a); patient with a single tooth gap in the left sions and morphology of the maxillary sinus posterior maxilla (b). mucosa were evaluated.

Evaluation of the images selected anterior slice of the maxillary sinus The CBCT images were evaluated by an experi- floor corresponds to the region between the root Material and methods enced graduate student not directly involved in tips of the maxillary premolars in a dentate the treatment and follow-up of the patients (S. J.). Patient selection patient (Fig. 1). The following anatomic land- For knowledge and diagnostic skills of maxillary For the present study, all partially edentulous marks in the coronal CBCT slices were selected sinus pathologies, the graduate student was in- patients scheduled for limited CBCT imaging for for standardized measurements at each position structed by two ENT specialists. For calibration further radiographic evaluation of a future im- (Fig. 2a–c): and evaluation of intraexaminer reliability, 10 plant insertion site in the posterior maxilla (first randomly selected cases were measured twice (1) The onset of the zygomatic process for the premolar to second molar) were consecutively on two different days, resulting in a mean differ- lateral measurement ( ¼ alat). enrolled. All patients had been referred by their ence of 0.18 mm per image (range of 0–0.33 mm). (2) The deepest point of the sinus floor in the private dentist to the Department of Oral Surgery For the further study, each measurement was coronal CBCT slice for the mid-sagittal and Stomatology at the University of Bern for repeated, and the mean value was calculated. measurement ( ¼ amid). implant therapy. The CBCT image taking oc- When the difference between two values was (3) The ipsilateral bony floor of the nose for the curred in the period between January 1, 2008 and 0.2 mm, a third measurement was performed medial measurement ( ¼ amed). December 31, 2008. Patients with a history of (Bornstein et al. 2010). CBCT images were ana- previous dental implant placement or bone graft- lyzed using a Dell 380 Precision workstation ing in the posterior maxilla, reduced sinus visi- In cases where the sinus floor was located more (Dell SA, Geneva, Switzerland) and a 19 in. bility in the CBCT scan volume (less than the cranial than the onset of the zygomatic process, Eizo Flexscan monitor with a resolution of region of the anterior maxillary sinus border to or than the bony floor of the nose, the lateral (lat) 1280 1024 pixels (Eizo Nanao AG, Wa¨dens- the second molar in the sagittal slices; floor of the – respectively, the medial (med) – measurements wil, Switzerland). The analyses and measure- nose and/or onset of the zygomatic process not were performed at the height of the onset of the ments described below were performed using a visible in the coronal slices), or with evident ipsilateral inferior nasal choncha. These three specialized computer software (i-Dixel Version artifacts due to movement during image taking measurements were repeated in 1.8, Morita). were excluded from the present study. the middle region (Fig. 1, see marking m), corre- Atthetimeoftheretrospectivedataanalysis, sponding to the apex of the first maxillary molar (mlat, mmid, mmed), and in the posterior region the implant therapy planning, and in most cases, Measurements to determine the thickness of the the implant surgery had already been performed. Schneiderian membrane (Fig. 1, see marking p), corresponding to the The CBCT slices were first reformatted to region between the apex of the second and the place the posterior maxillary segment (first third maxillary molars in dentate patients (plat, Imaging procedure premolar to second molar) of the alveolar pmid, pmed). In edentulous posterior sites, dis- The CBCT images were obtained with a 3D bone crest in a vertical position in the axial tances between premolar roots were set at 7 mm, Accuitomo XYZ Slice View Tomograph (Morita, slices, and the palate/floor of the nose in a and distances between molar roots at 8 mm. Kyoto, Japan) with a voxel size of 0.08 mm. horizontal position in the coronal slices. Subse- Therefore, the radiographic evaluation included Operating parameters were set at 5.0 to 7.0 mA quently, three standardized measurements of the nine separate measurements for each maxillary and 80 kV and exposure time was 17.5 s. For all dimensions of the Schneiderian membrane in sinus analyzed (Fig. 3). All measurements of the CBCT images, a limited field of view (FOV) of millimeters were performed using the coronal mucosal thickness were performed perpendicu- 4 4 cm, 6 6 cm, or 8 8 cm was selected. CBCT slice in the anterior region of the maxillary larly to the underlying bone, starting at the The data were reconstructed with slices at an sinus in the lateral (alat), in the mid-sagittal underlying bony plate and ending at the mucosal interval of 0.5 mm. (amid), and in the medial (amed) aspect. The surface.

2|Clin. Oral Impl. Res. 10.1111/j.1600-0501.2010.02140.x c 2011 John Wiley & Sons A/S Janneretal Characteristics and dimensions of the Schneiderian membrane

of interest (yes/no in anterior, middle, and posterior maxillary sinus regions).

Additional clinical and radiographic parameters as- sessed The season in which the CBCT image was taken (winter, spring, summer, autumn) was recorded for further evaluation as a potential parameter influencing the thickness of the Schneiderian membrane. The following anamnestic parameters of the included patients were recorded:

(1) Age and gender. (2) Tobacco use, classified as current, former, or never smoker. (3) Known rhinologic disease. (4) Weeks since last tooth/teeth removal in the examined maxillary segment.

Statistical analysis All data were first analyzed using descriptive statistics and box plots. In addition, the 95% confidence intervals of the mean thickness mea- sures were calculated for the different patient subgroups. The impact of potential influencing parameters on the mean values for the overall thickness (nine measurements per maxillary si- nus) and mid-sagittal thickness (three values per maxillary sinus) of the Schneiderian membrane was evaluated using univariate and multivariate linear regression models. Each sinus was consid-

Fig. 2. Landmarks for the measurement of the mucosa thickness in coronal cone beam computed tomography slices in the ered as independent because asymmetrical anterior (a), middle (b), and posterior (c) regions: the onset of the zygomatic process for the lateral measurement (lat); the thickness of the Schneiderian membrane was deepest point of the sinus floor for the mid-sagittal measurement (mid); the ipsilateral bony floor of the nose for the medial suspected in patients. The response variable measurement (med). The red dotted line indicates the position of the bony floor of the nose; the continuous red line indicates (thickness of the Schneiderian membrane) was the inferior nasal choncha. log-transformed for further analysis to achieve normality because the original data were skewed. All parameters with a P-value of 0.2 or less in the Mucosal thickening of 42 mm was classified (1) Status of the dentition in the posterior max- univariate analysis were included for further as pathological, and was classified according illa: single tooth gap, multiple tooth gap, analysis in a multivariate linear regression model. to criteria adapted from Soikkonen & Ainamo distal extension situation, edentulous. The fit of the models was assessed by evaluating (1995): (2) Presence of endodontically treated teeth the residuals of the respective regression models. (yes/no in anterior, middle, and posterior In addition, a robust regression was performed on (1) Flat: shallow thickening without well-de- maxillary sinus regions). the log-transformed response variable to assess fined outlines. (3) Presence of apical lesions according to the whether the coefficients and standard errors would (2) Semi-aspherical: thickening with well-de- diagnostic criteria of Low et al. (2008) in 1 vary when more robust methods are used (Draper fined outlines rising in an angle of 430 the region of interest (yes/no in anterior, & Smith 1998). The significance level chosen for from the floor or the walls of the sinus. middle, and posterior maxillary sinus re- all statistical tests was P0.05. All analyses were (3) Mucocele-like: complete opacification of gions): a periapical radiolucency in connec- performed using a software package (Stata 11, the sinus. tion with the apical part of the root was Stata Corp., College Station, TX, USA). (4) Mixed flat and semi-aspherical thickenings. classified as a lesion when the width of the (5) Other mucosal thickening types or patholo- radiolucency exceeded at least twice the gical findings. width of the periodontal ligament space, Results and the lesion was visible in at least two The following findings of the teeth (canines, image planes. During the study period, a total of 199 patients premolars, and molars including the third molar) (4) Presence of periodontal lesions (positive for were included for potential analysis of their in the region of interest were evaluated by screen- radiographic marginal bone loss deeper than CBCT images with respect to the dimensions ing the corresponding CBCT sections in all three the midlevel of the respective root or invol- and anatomic characteristics of the basal Schnei- dimensions (sagittal, coronal, and axial): vement of furcation in molars) in the regions derian membrane. In two limited CBCTs, the

c 2011 John Wiley & Sons A/S 3|Clin. Oral Impl. Res. 10.1111/j.1600-0501.2010.02140.x Janner et al Characteristics and dimensions of the Schneiderian membrane

Fig. 3. Schematic overview of the nine measurement points in the evaluated maxillary sinuses (axial slice).

Table 1. Analysis of the thickness (in mm) of the Schneiderian membrane using coronal slices from limited CBCT images Measurement Anterior Middle Posterior alat amid amed mlat mmid mmed plat pmid pmed Mean 0.96 2.47 1.6 1.11 3.11 1.84 0.9 2.16 0.99 Median 0.63 1.13 0.66 0.56 1.41 0.66 0.52 0.88 0.56 Maximum 21.08 30 16.5 26.67 34.61 22.33 21.41 30.51 15.27 Minimum 0.16 0.28 0.18 0.18 0.25 0.25 0.25 0.25 0.16 95% CI 0.69–1.22 1.89–3.04 1.2–2.01 0.75–1.47 2.4–3.82 1.3–2.39 0.58–1.22 1.57–2.76 0.7–1.28

Measurements for ‘‘anterior,’’ ‘‘middle,’’ and ‘‘posterior’’ correspond to the regions shown in Figs 2a–c and 3. CBCT, cone beam computed tomography; CI, confidence interval.

analysis of the images was not possible due to exhibited 64 single tooth gaps, 37 multiple tooth mucosal dimensions on the lateral and medial movement artifacts; 20 patients had a history of gaps, and 50 distal extension situations, and 17 aspects of the maxillary sinus varied between 0.9 dental implant placement or bone grafting in the patients were edentulous. and 1.84 mm. The median values were lower for posterior maxilla; and in 34 patients the visible all regions analyzed, and more pronounced for the area of the maxillary sinus in the FOV did not three mid-sagittal measurements. For all three Descriptive analysis of the dimensions and meet the inclusion criteria mentioned above. characteristics of the Schneiderian membrane regions analyzed (anterior, middle, and posterior), This resulted in a total of 143 patients with 168 Therewasawiderangeinthethicknessofthe the mid-sagittal values were statistically signifi- CBCT scans included in the present study. This Schneiderian membrane as evaluated on the cantly different from the respective measure- groupcomprised67menand76womenwitha CBCT images, with a minimum value of ments in the lateral and medial walls of the mean age of 57.5 years ( 11.67). Of the included 0.16 mm and a maximum value of 34.61 mm maxillary sinus. patients, 21 were current smokers, 15 were former (Table 1). The highest mean values, ranging from In the descriptive analysis of the CBCT smokers, and 96 reported never having used to- 2.16 to 3.11 mm, were found for the mucosa images, 76 maxillary sinuses (45% out of a total bacco. In 11 patients, the status of tobacco use was located in the mid-sagittal regions of the max- of 168) were classified as healthy (Table 2). The not reported. The patients included in the study illary sinus, whereas the mean values of the most frequent pathologies diagnosed were flat

4|Clin. Oral Impl. Res. 10.1111/j.1600-0501.2010.02140.x c 2011 John Wiley & Sons A/S Janneretal Characteristics and dimensions of the Schneiderian membrane

Table 2. Types of pathology and thickness (in mm) of the Schneiderian membrane according to the season of image taking as diagnosed on CBCT images Season Number of Pathology in Type of pathology (0–5) Mean thickness Mean thickness Mean thickness Mean overall CBCTs, n maxillary sinus n (%) lat in mm mid in mm med in mm thickness in mm (yes/no), n (%) (95% CI) (95% CI) (95% CI) (95% CI) Spring 36 16 (44.44) 0 20 55% 1.8 (0.48–3.11) 4.11 (1.9–6.31) 2.36 (1–3.71) 2.75 (1.19–4.32) 1 7 20% 2 5 14% 3– – 4 4 11% 5– – Summer 39 18 (46.15) 0 21 54% 0.7 (0.54–0.86) 1.91 (1.29–2.54) 1.21 (0.8–1.62) 1.28 (0.92–1.63) 1 14 36% 225% 3– – 4– – 525% Autumn 57 36 (63.16) 0 21 37% 0.83 (0.58–1.08) 2.05 (1.49–2.61) 1.15 (0.78–1.52) 1.34 (0.97–1.72) 1 27 47% 212% 3– – 447% 547% Winter 36 22 (61.11) 0 14 39% 0.75 (0.57–0.92) 2.62 (1.38–3.86) 1.41 (0.46–2.36) 1.59 (0.85–2.33) 1 14 39% 2 4 11% 313% 438% 5– – Total 168 92 (54.76) 0 76 45% 0.99 (0.69–1.28) 2.58 (1.99–3.16) 1.48 (1.09–1.86) 1.68 (1.28–2.08) 1 62 37% 2127% 311% 4116% 564%

CBCT, cone beam computed tomography; CI, confidence interval.

Table 3. Tooth-related potential influencing factors in the analyzed region and thickness (in mm) of the Schneiderian membrane as diagnosed on CBCT images Region Endodontically treated teeth Apical lesions in ROI% Periodontal lesions in Mean midline-value in ROI% (95% CI) (95% CI) ROI% (95% CI) in mm (95% CI) Anterior 19.64 (13.57–25.71) 19.05 (13.05–25.05) 4.76 (1.51–8.02) 2.46 (1.89–3.04) Middle 13.69 (8.43–18.94) 13.69 (8.44–18.94) 7.74 (3.66–11.82) 3.11 (2.4–3.82) Posterior 10.71 (5.98–15.44) 9.52 (5.04–14.01) 8.33 (4.11–12.56) 2.16 (1.57–2.76) Total 14.68 (11.27–18.09) 14.09 (10.6–17.58) 6.94 (4.47–9.42) 2.58 (2–3.17)

ROI, region of interest; midline-value, thickness of the Schneiderian membrane as measured in the deepest aspect of the maxillary sinus floor; CBCT, cone beam computed tomography; CI, confidence interval. thickenings of the Schneiderian membrane (62 rior regions, 7.74% in middle regions, and 8.33% periodontal status (P ¼ 0.106) of the dentition in positive findings in 168 maxillary sinuses/37%). in posterior regions of the maxillary sinuses. The the region of interest, and the season of CBCT Only one case of a mucocele-like radioopacity in mean time elapsed since the last tooth removal in image taking (P-values from 0.335 to 0.663; Table the respective sinus was found. the analyzed segment as reported by the patient 4). For the multivariate linear regression model, was 146.26 weeks (SD 247.9). only gender had a statistically significant influ- For the univariate linear regression model, ence on the mean overall and mid-sagittal thick- Analysis of potential factors influencing the di- gender (P ¼ 0.004) of the patients and periapical ness of the Schneiderian membrane (P ¼ 0.01 for mensions and characteristics of the Schneiderian membrane status of the teeth in the region of interest overall mean thickness; P ¼ 0.015 for mean mid- The presence of endodontically treated teeth in the (P ¼ 0.0033) exhibited a statistically significant sagittal thickness; Table 5). region of interest decreased from 19.64% in the influence on the mean overall and mid-sagittal anterior region to 13.69% in the middle region to thickness of the Schneiderian membrane (Table 10.71% in the posterior region of the maxillary 4). The respective mean values were generally Discussion sinuses analyzed (Table 3). A similar distribution higher for male subjects and for teeth with evident was observed for apical lesions: 19.05% were periapical pathology. No statistically significant More than 90% of the epithelial cells of the diagnosed in the anterior, 13.69% in the middle, influence was seen for age (P ¼ 0.174), rhinologic Schneiderian membrane are ciliated and distrib- and 9.52% in the posterior region. Periodontal disease (P ¼ 0.727), tobacco use (P ¼ 0.411), last uted in a single, columnar, pseudostratified layer. lesions exhibited an inverse distribution pattern, tooth removal in the examined maxillary seg- The beat frequency of the cilia is approximately with 4.76% of the pathologies diagnosed in ante- ment (P ¼ 0.179), endodontic (P ¼ 0.312) and 60 kHz, thus moving mucus and debris actively

c 2011 John Wiley & Sons A/S 5|Clin. Oral Impl. Res. 10.1111/j.1600-0501.2010.02140.x Janner et al Characteristics and dimensions of the Schneiderian membrane

Table 4. Univariate analysis of potential influencing clinical and anamnestic parameters of the mean Cagici et al. (2009). However, the median values overall and mean mid-sagittal thickness (in mm) of the Schneiderian membrane for all nine regions evaluated ranged from 0.52 Factor Overall mean thickness Mean mid-sagittal thickness to 1.41 mm. Coefficient T-value P-value Coefficient T-value P-value When comparing mean and median values, the Age 0.06 1.37 0.174 0.07 1.3 0.194 Schneiderian membrane was the thinnest in the Gender (female vs. male) 0.33 2.92 0.004 0.37 2.76 0.007 lateral measurements, with slightly higher values Rhinologic disease 0.08 0.35 0.727 0.14 0.51 0.631 in the median aspect, and statistically signifi- Tobacco use 0.13 0.83 0.411 0.15 0.84 0.402 Time since extraction 0.02 1.35 0.179 0.02 0.85 0.395 cantly higher values in the mid-sagittal aspect. It Endodontic status 0.12 1.02 0.312 0.148 1.03 0.305 can be speculated that the mid-sagittal thickness Periapical status 0.26 2.15 0.033 0.305 2.1 0.037 values are increased because of the seated patient Periodontal status 0.24 1.62 0.106 0.308 1.72 0.087 Season of imagingn position during CBCT image taking, which could 2 vs. 1 0.17 0.97 0.335 0.11 0.54 0.588 cause the accumulation of mucous secretions in 3 vs. 1 0.12 0.67 0.506 0.18 0.88 0.382 the deepest aspect of the maxillary sinus. Other 4 vs. 1 0.07 0.44 0.663 0.09 0.51 0.61 imaging techniques, such as MRI, CT, and some- The response variable (thickness of the Schneiderian membrane) was log-transformed for further analysis. Bold times CBCT, perform image taking on a prone indicates statistically significant results. patient. Moreover, CBCT imaging does not allow n Partial F test for all four seasons (1, winter; 2, spring; 3, summer; 4, autumn; overall mean thickness P ¼ 0.3612, differentiation between liquids and soft tissue. mean mid-thickness P ¼ 0.5087). Therefore, the high mean/median values for the mid-sagittal measurements couldalsobepartially due to mucous accumulation on the Schneider- Table 5. Multivariate analysis of potential influencing anamnestic and clinical parameters on the mean overall and mean mid-sagittal thickness (in mm) of the Schneiderian membrane ian membrane. Factor Overall mean thickness Mean mid-sagittal thickness A high prevalence of mucosal thickening in Coefficient T-value P-value Coefficient T-value P-value paranasal sinuses of asymptomatic patients is reported in the literature. The analysis of 9315 Age 0.04 0.82 0.412 0.04 0.75 0.454 Gender (female vs. male) 0.31 2.61 0.01 0.33 2.46 0.015 panoramic radiographs in a Finnish health survey Periapical status 0.2 1.54 0.124 0.23 1.49 0.139 revealed maxillary mucosal thickening in 12% of Periodontal status 0.1 0.64 0.525 0.15 0.78 0.435 the subjects, and a prevalence of mucous antral

The response variable (thickness of the Schneiderian membrane) was log-transformed for further analysis. Bold cysts of 7% (Vallo et al. 2010). Incidental para- indicates statistically significant results. nasal mucosal changes were also evaluated in MRI scans performed for diagnosis of neurological toward the natural ostium (van den Bergh et al. location of the measurement points utilized in pathologies (Cooke & Hadley 1991; Patel et al. 2000; Pikos 2008). Factors compromising mu- these studies varies greatly. Additionally, studies 1996). The highest prevalence was reported for cous production and clearance of the mucosa can apply different measurement scales and classifi- the ethmoidal sinuses, followed by the maxillary increase the risk of sinusitis development and cations from the maximum mucosal thickness in sinuses. The maxillary sinuses had a prevalence have to be avoided. A typical example of such a millimeters (Rak et al. 1991), to the simple of shallow/flat mucosal thickening ranging from risk factor in dentistry is the penetration of description of the shape of mucosal thickening 23% to 31%, and a prevalence of cystic lesions particulate graft material during sinus floor sur- (Soikkonen & Ainamo 1995; Patel et al. 1996), ranging from 7% to 10%. In these studies, the gery (Pikos 2008). The mean thickness of the and finally to the detection of changes in mem- authors did not use any threshold values for Schneiderian membrane was evaluated in a post- brane thickness over time (Min et al. 1994; Peleg classification of pathologies, but only a descrip- mortem study with values ranging from 0.3 to et al. 1999). Furthermore, early reports of thick- tion of the shape. A prospective radiographic 0.8 mm in 10 unfixed, fresh cadavers without ness measurements revealed difficulty in visua- analysis of 666 patients undergoing CT scans signs of sinusitis (Tos & Mogensen 1979). In a lizing normal mucoperiosteal structures in the for indications such as head injuries or seizures similar study using 20 fresh cadavers, Pommer paranasal sinuses through CT (Min et al. 1994) or reported abnormalities of one or more of the et al. (2009) found a mean thickness value of MRI (Patel et al. 1996). The mucosa could be paranasal sinuses in 42.5% of the patients (Havas 0.09 0.05 mm (range 0.02–0.35 mm). In a seen only at a thickness of 2 mm or above, and et al. 1988). In the present analysis, a higher study analyzing sinus biopsies from healthy sub- therefore historically 2 mm was considered a prevalence of mucosal pathologies (55%) was jects, Aimetti et al. (2008) measured a mean reliable threshold for pathological mucosal swel- found than in the studies mentioned above. thickness of 0.97 0.36 mm. All three groups ling (Cagici et al. 2009). Thiscouldbeduetotheuseofaprecisethreshold describe great interindividual variability in the The results of the present study confirmed the valuetodefineapathologicSchneiderianmem- thickness of the Schneiderian membrane. great interindividual variability of the thickness brane (2 mm). Nevertheless, the clinical signifi- Existing data on the dimensions and changes in of the Schneiderian membrane, with values ran- cance of this value has to be regarded with some the Schneiderian membrane based on radio- ging from 0.16 mm (minimum) to 34.61 mm caution, as it remains to be addressed in future graphic imaging are rare in the literature. In CT (maximum). Furthermore, a discrepancy be- studies, how many of these findings and which and magnetic resonance imaging (MRI) studies, tween mean and median values was evident, type of mucosal thickening require therapy. The coronal slices are well established for evaluating suggesting that some of the subjects analyzed prevalence of cystic-shaped lesions was 7%, the mucosal thickness in the maxillary sinus, exhibited very high mucosal thickness values demonstrating good correlation with previous and the measurements are always performed (Table 1). When only interpreting the mean studies (Cooke & Hadley 1991; Patel et al. perpendicular to the underlying bone (Rak et al. mucosal thickness values, the mid-sagittal find- 1996; Vallo et al. 2010). 1991; Min et al. 1994; Peleg et al. 1999; Pruna ings in anterior, middle, and posterior regions The available literature describing potential 2003; Cagici et al. 2009). Nevertheless, the have to be considered as pathological according to local or systemic influences on the thickness of

6|Clin. Oral Impl. Res. 10.1111/j.1600-0501.2010.02140.x c 2011 John Wiley & Sons A/S Janneretal Characteristics and dimensions of the Schneiderian membrane the Schneiderian membrane identifies many dif- mucosa thickness in the multivariate regression potential pathological conditions is necessary ferent factors. In a study using intraoral radio- analysis, with male subjects having higher mean before SFE. What therapeutic significance has to graphs, Engstro¨m et al. (1988) found a mean values. Endodontic, periodontal, and periapical be attributed to the relative high prevalence of sinus floor mucosal thickness of 5.6 6.1 mm status of the dentition in the region of interest mucosal findings (55%), and which of these need before and 0.6 1.6 mm after extensive perio- had no statistically significant influence. This further evaluation and eventual treatment, has dontal therapy in the corresponding sextant for 13 could be due to the difference in the populations not been analyzed in the present study. As there patients with advanced periodontal disease. Gin- analyzed. To further evaluate the potential im- are no guidelines for classification and treatment gival thickness and gender were the only geneti- pact of dental pathologies of teeth in the posterior of mucosal findings in the maxillary sinus before cally determined parameters to reliably predict maxilla on the dimensions of the Schneiderian SFE, future prospective studies are needed. These sinus membrane thickness, being higher in pa- membrane, prospective cohort studies with larger studies should also analyze patency of the osteo- tients with thick gingival biotype and lower in samples and specific problems (periodontal, peri- meatal complex and the condition of the bony women (Aimetti et al. 2008; Vallo et al. 2010). apical/endodontic) are needed. walls of the maxillary sinuses. An analysis of 330 maxillary sinuses on CT scans The most frequent surgical complication re- Because of the complex anatomical situation in revealed a statistically significantly higher ported to occur during SFE is an accidental the posterior maxilla, cross-sectional imaging prevalence of mucosal thickening in proximity perforation of the Schneiderian membrane, oc- (CT scan) has been proposed as the standard to restored teeth (Connor et al. 2000). Vallo et al. curring in 10–56% of the operated sinuses (Born- radiographic method for preoperative planning of (2010) found higher Schneiderian membrane stein et al. 2008; Pikos 2008). Other dental implant placement (Dula et al. 2001; thickness values in maxillary sinuses adjacent postoperative complications include acute or Harris et al. 2002). In the present study, limited to periodontal and endodontic lesions. Further- chronic sinus infection, bleeding, wound dehis- CBCT was used to visualize the posterior maxilla, more, smoking and the presence of rhinologic cence, exposure of the barrier membrane, and including the soft tissue morphology of the re- diseases correlated with increased mucosal thick- graft loss (Regev et al. 1995; Pikos 2006). To the lated maxillary sinus. Smaller FOV should al- ness. The month in which images were taken best of our knowledge, the impact of the condi- ways be used when possible, thus adhering to the was reported to have an influence on pathologic tion of the Schneiderian membrane on the suc- ALARA (as low as reasonably achievable) princi- findings in the maxillary sinuses, with Septem- cess and long-term outcome of dental implant ple in medical radiology (McCollough et al. ber, October, and November having a higher placement has not yet been evaluated in the 2009). In comparison with CT, modern CBCT prevalence of cystic lesions (Rodrigues et al. literature. Nevertheless, a recent case series ana- devices have the advantage of administering less 2009; Vallo et al. 2010), and an increased pre- lyzing failures of SFE procedures reported that out radiation to the patient (Cohenca et al. 2007; valence of mucosal thickening during winter of 13 patients included, preoperative chronic Suomalainen et al. 2009; Okano et al. 2009). (Tarp et al. 2000). maxillary sinusitis had been present in four Therefore, CBCT can be regarded as an alterna- In the present study, only gender was identi- patients (Anavi et al. 2008). The authors there- tive to CT for three-dimensional imaging before fied as an influencing factor for maxillary sinus fore stated that elimination of sinusitis and other SFE.

References

Aimetti, M., Massei, G., Morra, M., Cardesi, E. & Digital volume tomography (DVT) as a diagnostic Engstro¨m, H., Chamberlain, D., Kiger, R. & Egelberg J . Romano, F. (2008) Correlation between gingival phe- modality of the anterior base. Acta Oto-Laryn- (1988) Radiographic evaluation of the effect of notype and Schneiderian membrane thickness. The gologica 31: 1–9. initial periodontal therapy on thickness of the max- International Journal of Oral & Maxillofacial Im- Cagici, C.A., Yilmazer, C., Hurcan, C., Ozer, C. & illary sinus mucosa. Journal of Periodontology 59: plants 23: 1128–1132. Ozer, F. (2009) Appropriate interslice gap for screen- 604–608. Anavi, Y., Allon, D.M., Avishai, G. & Calderon, S. ing coronal paranasal sinus tomography for mucosal Fatterpekar, G.M., Delman, B.N. & Som, P.M. (2008) (2008) Complications of maxillary sinus augmenta- thickening. European Archives of Oto-Rhino-Laryn- Imaging the paranasal sinuses: where we are and tions in a selective series of patients. Oral Surgery, gology 266: 519–525. wherewearegoing.The Anatomical Record 291: Oral Medicine, Oral Pathology, Oral Radiology, and Cohenca, N., Simon, J.H., Roges, R., Morag, Y. & 1564–1572. Endodontics 106: 34–38. Malfaz, J.M. (2007) Clinical indications for digital Guerrero, M.E., Jacobs, R., Loubele, M., Schutyser, F., Bornstein, M.M., Chappuis, V., von Arx, T. & Buser, imaging in dento-alveolar trauma. Part 1: traumatic Suetens, P. & van Steenberghe, D. (2006) State-of- D. (2008) Performance of dental implants after staged injuries. Dental Traumatology 23: 95–104. the-art on cone beam CT imaging for preoperative sinus floor elevation procedures: 5-year results of a Connor, S.E., Chavda, S.V. & Pahor, A.L. (2000) planning of implant placement. Clinical Oral Inves- prospective study in partially edentulous patients. Computed tomography evidence of dental restoration tigations 10: 1–7. Clinical Oral Implants Research 19: 1034–1043. as aetiological factor for maxillary sinusitis. The Harris, D., Buser, D., Dula, K., Grondahl, K., Haris, D., Bornstein, M.M., Lauber, R., Sendi., P. & von Arx, T. Journal of Laryngology and Otology 114: 510–513. Jacobs, R., Lekholm, U., Nakielny, R., van Steen- (2010) Comparison of periapical radiography and lim- Cooke, L. & Hadley, D. (1991) MRI of the paranasal berghe, D. & van der Stelt, P. (2002) European ited cone beam computed tomography in mandibular sinuses: incidental abnormalities and their relation- Association for Osseointegration. E.A.O. guidelines molars for analysis of anatomical landmarks prior to ship to symptoms. The Journal of Laryngology and for the use of diagnostic imaging in implant dentistry. apical surgery. Journal of Endodontics (accepted for Otology 105: 278–281. A consensus workshop organized by the Euro- publication). Draper, N.R. & Smith, H. (1998) Applied Regression pean Association for Osseointegration in Trinity Col- Bornstein, M.M., Wo¨lner-Hanssen, A.B., Sendi, P. & Analysis. 3rd edition. New York: Wiley-Interscience. lege Dublin. Clinical Oral Implants Research 13: von Arx, T. (2009) Comparison of intraoral radio- 567–584. 566–570. graphy and limited cone beam computed tomography Dula, K., Mini, R., van der Stelt, P.F. & Buser, D. Havas, T.E., Motbey, J.A. & Gullane, P.J. (1988) Pre- for the assessment of root-fractured permanent teeth. (2001) The radiographic assessment of implant valence of incidental abnormalities on computed Dental Traumatology 25: 571–577. patients: decision-making criteria. The Internatio- tomographic scans of the paranasal sinuses. Archives Bremke, M., Sesterhenn, A.M., Murthum, T., Hail, nal Journal of Oral & Maxillofacial Implants 16: of Otolaryngology – Head & Neck Surgery 114: A.A., Kadah, B.A., Bien, S. & Werner, J.A. (2008) 80–89. 856–859.

c 2011 John Wiley & Sons A/S 7|Clin. Oral Impl. Res. 10.1111/j.1600-0501.2010.02140.x Janner et al Characteristics and dimensions of the Schneiderian membrane

Jemt, T. & Lekholm, U. (1995) Implant treatment in Okano, T., Harata, Y., Sugihara, Y., Sakaino, R., Tsu- anatomic variations. Journal of Endodontics 29: edentulous maxillae: a 5-year follow-up report on chida, R., Iwai, K., Seki, K. & Araki, K. (2009) 773–775. patients with different degrees of jaw resorption. The Absorbed and effective doses from cone beam volu- Rodrigues, C.D., Freire, G.F., Fonseca da Silveira, M.M. International Journal of Oral & Maxillofacial Im- metric imaging for implant planning. Dentomaxillo- & Estrela, C. (2009) Prevalence and risk factors of plants 10: 303–311. facial Radiology 38: 79–85. mucous retention cysts in a Brazilian population. Kasaj, A. & Willershausen, B. (2007) Digital volume Patel, K., Chavda, S.V., Violaris, N. & Pahor, A.L. Dentomaxillofacial Radiology 38: 480–483. tomography for diagnostics in periodontology. The (1996) Incidental paranasal sinus inflammatory Soikkonen, K. & Ainamo, A. (1995) Radiographic International Journal of Computerized Dentistry changes in a British population. The Journal of Lar- maxillary sinus findings in the elderly. Oral Surgery, 10: 155–168. yngology and Otology 110: 649–651. Oral Medicine, Oral Pathology, Oral Radiology, and Lofthag-Hansen, S., Huumonen, S., Gro¨ndahl, K. & Patel, S. (2009) New dimensions in endodontic imaging: Endodontics 80: 487–491. Gro¨ndahl, H.G. (2007) Limited cone-beam CT Part 2. Cone beam computed tomography. The Inter- Suomalainen, A., Kiljunen, T., Ka¨ser, Y., Peltola, J. & and intraoral radiography for the diagnosis of periapi- national Endodontic Journal 42: 463–475. Kortesniemi, M. (2009) Dosimetry and image quality cal pathology. Oral Surgery, Oral Medicine, Oral Peleg, M., Chaushu, G., Mazor, Z., Ardekian, L. & of four dental cone beam computed tomography Pathology, Oral Radiology, and Endodontics 103: Bakoon, M. (1999) Radiological findings of the post- scanners compared with multislice computed tomo- 114–119. maxillary sinus: a computerized tomography graphy scanners. Dentomaxillofacial Radiology 38: Low, K.M., Dula, K., Bu¨ rgin, W. & von Arx, T. (2008) follow-up. Journal of Periodontology 70: 1564– 367–378. Comparison of periapical radiography and limited 1573. Tarp, B., Fiirgaard, B., Christensen, T., Jensen, J.J. & cone-beam tomography in posterior maxillary teeth Pikos, M.A. (2006) Complications of maxillary sinus Black, F.T. (2000) The prevalence and significance of referred for apical surgery. Journal of Endodontics 34: augmentation. In: Jensen, O.T., ed. The Sinus Bone paranasal sinus abnormalities on MRI. Rhinology 38: 557–562. Graft. 2nd edition, 103–113. Chicago: Quintessence 33–38. McCollough, C.H., Primak, A.N., Braun, N., Kofler, J., Publishing. Tos, M. & Mogensen, C. (1979) Mucus production Yu, L. & Christner, J. (2009) Strategies for reducing Pikos, M.A. (2008) Maxillary sinus membrane repair: in the nasal sinuses. Acta Oto-Laryngologica 360: radiation dose in CT. Radiologic Clinics of North update on technique for large and complete perfora- 131–134. America 47: 27–40. tions. Implant Dentistry 17: 24–31. Vallo, J., Suominen-taipale, L., Huumonen, S., Soikko- Min, Y., Lee, J. & Shin, J. (1994) Radiologic assessment Pommer, B., Unger, E., Su¨ to¨ , D., Hack, N. & Watzek, nen, K. & Norblad, A. (2010) Prevalence of mucosal of diseased mucosa of the maxillary sinus after func- G. (2009) Mechanical properties of the Schneiderian abnormalities of the maxillary sinus and their rela- tional endoscopic sinus surgery. Acta Otolaryngolo- membrane in vitro. Clinical Oral Implants Research tionship to dental disease in panoramic radiography: gica (Stockholm) 114: 657–662. 20: 633–637. results from the Health 2000 Health Examination Misch, K.A., Yi, E.S. & Sarment, D.P. (2006) Accuracy Pruna, X. (2003) Morpho-functional evaluation of os- Survey. Oral Surgery, Oral Medicine, Oral Pathol- of cone beam computed tomography for periodontal teomeatal complex in chronic sinusitis by coronal ogy, Oral Radiology, and Endodontics 109: e80–e87. defect measurements. Journal of Periodontology 77: CT. European Radiology 13: 1461–1468. van den Bergh, J.P., ten Bruggenkate, C.M., Disch, F.J. 1261–1266. Rak, K.M., Newell, J.D. II, Yakes, W.F., Damiano, M.A. & Tuinzing, D.B. (2000) Anatomical aspects of sinus Mozzo, P., Procacci, C., Tacconi, A., Martini, P.T. & & Luethke, J.M. (1991) Paranasal sinuses on MR floor elevations. Clinical Oral Implants Research 11: Andreis, I.A. (1998) A new volumetric CT machine images of the brain: significance of mucosal thickening. 256–265. for dental imaging based on the cone-beam tech- American Journal of Roentgenology 156:381–384. Walter, C., Kaner, D., Berndt, D.C., Weiger, R. & nique: preliminary results. European Radiology 8: Regev, E., Smith, R.A., Perrot, D.H. & Porgel, M.A. Zitzmann, N.U. (2009) Three-dimensional imaging 1558–1564. (1995) Maxillary sinus complications related to en- as a pre-operative tool in decision making for furca- Naitoh, M., Suenaga, Y., Kondo, S., Gotoh, K. & dosseous implants. The International Journal of Oral tion surgery. Journal of Clinical Periodontology 36: Ariji, E. (2009) Assessment of maxillary sinus & Maxillofacial Implants 10: 451–461. 250–257. septa using cone-beam computed tomography: Rigolone, M., Pasqualini, D., Bianchi, L., Berutti, E. & Ziegler, C.M., Woertche, R., Brief, J. & Hassfeld, S. etiological consideration. Clinical Implant Bianchi, S.D. (2003) Vestibular surgical access to the (2002) Clinical indications for digital volume tomo- Dentistry & Related Research 11 (Suppl. 1): e52– palatine root of the superior first molar: ‘‘low-dose graphy in oral and maxillofacial surgery. Dentomax- e58. cone-beam’’ CT analysis of the pathway and its illofacial Radiology 31: 126–130.

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