Since its introduction in the 1970s, CT has become an important medical imaging tool used in the detection, prevention, and screening of disease. Later, the introduction of cone beam computed tomography (CBCT) in the late 1990s represented a revolution in the in vivo 3-dimensional (3D) study of the maxillofacial skeletal structures.1
For successful dental implant treatment, the alveolar bone quantity encompassing both the alveolar shape and the bone volumes at implant sites is an important factor. The posterior maxilla has been described as the most difficult and problematic intraoral area confronting the implant practitioner. In addition, an increasingly frequent use is being made of sinus lift techniques,2 3–5
At least 3 types of alterations can be observed when an approximation to the elevation of the maxillary sinus is made.
The first is the deficient bone quantity and quality resulting from alveolar bone reabsorption processes after tooth removal.
The second concerns sinus anatomical variations, such as pneumatization or hypoplasia, and the presence of maxillary sinus septa. This last phenomenon may be interpreted as the result of maxillary development or of irregular pneumatization after premature dental loss.6,7
The third alteration that may be observed is the presence of lesions, typically as a casual finding in the course of complementary tests performed for dental treatment. More specifically, such changes involve membrane thickening, mucus retention cysts, and polyps, which are often asymptomatic.5 6,7
The literature contains a number of studies describing sinus variations and alterations. Some of these studies are of an orthodontic nature while others involve different dental procedures,5,8–10
The aim of the present retrospective clinical study was to report the anatomical variations and anomalies of the maxillary sinus in asymptomatic patients, using CBCT.
Materials and Methods
Study Design
A retrospective analysis of randomly selected subjects presented for CBCT exploration in the Dental Clinic of the University of Murcia (Murcia, Spain).
All the patients had been referred for CBCT diagnosis and treatment planning, which included dental implants, maxillofacial surgery, orthodontics, endodontics, oral pathology, etc. No patient had been referred for a CT scan of the maxillary sinus area because of sinus symptoms or suspected diseases.
A retrospective radiographic study was made of 200 CBCT scans randomly selected from among the 826 radiological studies made in patients requiring exploration for the planning of dental treatment between June 2010 and December 2012. Random selection was performed using a random numbers sorting without repetition program* (http://nosetup.org/php_on_line/numero_aleatorio_2
The following inclusion criteria were established: (a) patients with no sinus disorders and subjected to CBCT exploration for the planning of dental treatment, (b) patients giving consent for the use of their clinical data for research purposes, and (c) patients older than 18 years.
The following exclusion criteria were established: (a) CBCT scans not allowing evaluation of the entire lower third of the maxilla; (b) the presence of artifacts precluding or complicating evaluation of the maxillary sinus; (c) patients with a history of systemic disease affecting bone (hyperparathyroidism, Paget disease, osteoporosis, maxillary osteonecrosis); and (d) patients with a history of surgery in the region of the maxillary sinus (sinus lift procedures, rhinosinusitis, mucoceles). Screening of the radiological records based on these criteria resulted in the exclusion of 40 subjects and the inclusion of 160 patients, of which 90 were females (56.3%) and 70 (43.8%) males. Their age ranged from 22 to 78 years (mean = 53.58, SD = 10.08).
Image Acquisition and Analysis
All the CBCT scans were made using the same calibrated system (Planmeca ProMax 3-D Max; Planmeca Oy, Helsinki, Finland). The scans were performed with the patient in prone decubitus, adjusting the head with the laser guide system of the scanner. The mean beam emission parameters were as follows: 96 kV, 8 mA, exposure time 12 seconds (11.94 seconds) with 501 × 501 × 466 voxels imaging (each voxel being equivalent to 200 μm).
The Romexis 2.5.1. software package (Planmeca Oy) was used to visualize the images in a multiple window displaying the axial, coronal, and sagittal planes at 0.2 mm intervals, as well as in 3D.
All measurements were made using the same trained and calibrated observer (A.C.B.). Both anatomical variations and lesions of the maxillary sinus were evaluated and classified, and their frequencies were recorded. Calibration and intraobserver reliability were determined based on 10 randomly selected cases measured twice on 2 different days. An interrater reliability analysis using Kappa statistic was performed to determine consistency among measurements. We consider as appropriate to control intraobservational bias.
We evaluated the presence of pneumatization, septa, hypoplasia, polypoid lesions, and discontinuities of the sinus wall, air-liquid levels, bone thickening, antroliths, opacifications, and the presence of foreign bodies. Observations were made only in central sections of a sagittal plane.
To determine sinus pneumatization, 3 lines were drawn on a panoramic reconstruction. The first one was an interorbital line joining the most inferior points of both orbital margins. The second and third lines were zygomatic process lines, each passing through the most inferior margin of the zygomatic process on each side of the jaw. These lines were parallel to the interior margin of the zygomatic process on each side of the jaw and parallel to the interorbital line.3 Fig. 1 ).
Fig. 1: The following anatomical landmarks were determined: The suborbital points (left and right). The most caudal point of the zygomatic arch (right and left). The most caudal point of the maxillary sinus (right and left). The first measurement is referred to as “A.” A second measurement is taken between the line joining both zygomatic ridges and the lowest point of each maxillary sinus separately (right and left) and individually. This distance is called “B.” B/A = C, the pneumatization index.
The thickness of the Schneiderian membrane was measured in the coronal section of a sagittal plane using the software digital tool. As reference, we used the most caudal point on the floor of the sinus. Thickening of the mucosal membrane was graded according to the classification proposed by Lu et al11 11,12 13
The cortical thickness of the floor of the sinus was assessed at this same reference point.14 Fig. 2 ). In agreement with Misch,15
Fig. 2: Membrane thickness (2.40 mm in this case) and the cortical sinus floor in the most caudal point of the sinus.
The thickness of the cortical bone is the most important determinant of initial stability, and this can be ensured with thicknesses equal to or greater than 5 mm.
Statistical Analyses
The data were processed using the SPSS version 19.0 statistical package (SPSS Inc., Chicago, IL), with the calculation of descriptive and inferential statistics. The interrater reliability was found to be Kappa = 0.98 (P < 0.05). The quantitative and qualitative variables were compared by means of a nonparametric test for the comparison of 2 means (Mann-Whitney U test), following a comparison of variances. The thickness of the Schneiderian membrane and the cortical thickness of the floor of the sinus were correlated by means of the Pearson correlation coefficient.
Correlations were explored between the variables: presence/absence of septa, membrane thickening, and cortical thickening of the sinus floor. Likewise, correlations were evaluated between Schneiderian membrane thickening and the presence of maxillary sinus disease defined as discontinuity of the floor of the sinus or of the lateral wall, air-liquid levels, opacification, or the presence of polypoid lesions.
Contingency tables with the Pearson chi-square test were used, complemented by residual analysis, to explore the relationships between qualitative variables.
Results
The 160 valid CBCT scans comprised 71 males (44.3%) and 89 (55.6%) females, with a mean patient age of 50 (range, 18–74) years.
Table 1 shows pneumatization as the most common anatomical finding of the maxillary sinus, which was detected in 130 cases (81.3%). Pneumatization in turn was observed in several regions in 103 cases (78.5%)—bilateral pneumatization being the most frequent presentation. Underwood septum was present in 42 patients (26.3%) while maxillary sinus hypoplasia was identified in 14 of the CBCT scans (8.8%) and exostosis in 4 cases (2.5%).
Table 1: Anatomical Variations of the Maxillary Sinus Observed in 160 CBCT Scans
Table 2 shows that 22 patients had polypoid lesions (13.7%) while discontinuity of the sinus floor was identified in 29 cases (18.1%). Of these 29 cases, 11 were associated with periapical lesions, 7 to endodontic filling material, 6 to tooth extractions, and 4 to implant-related fenestration. No underlying cause was established in one case (Figs. 3 and 4 ). Finally, 5 patients showed a residual ridge height of less than 5 mm.
Table 2: Lesions of the Maxillary Sinus Observed in 160 CBCT Scans
Fig. 3: A , Schneiderian membrane thickness <2 mm. B , Schneiderian membrane thickness >2 mm. Discontinuity due to (C ) and (D ) dental implants, (E ) and (F ) periapical infection, (G ) extrusion of endodontic material, and (H ) extraction.
Fig. 4: A , Polypoid lesion, (B ) bilateral opacification, (C ) Underwood septum , (D ) air-fluid level, (E ) and (F ) antrolith and opacified maxillary sinus, (G ) left maxillary hypoplasia, (H ) bone thickening of the maxillary sinus wall, and (I ) pneumatization.
The Pearson chi-square test was used to study the relationship between thickening of the Schneiderian membrane and the presence or absence of maxillary sinus disease. The assumption of sinus pathology is simply based on the identification of radiographic lesion candidates to be compatible with sinus pathology by the evaluator. The results showed that the presence of pathological conditions is associated with a thickening of the Schneiderian membrane that reaches >2 mm (grades 3, 4, and 5) (P < 0.05). In turn, 70.4% of the patients with maxillary sinus disease had a membrane thickness of >2 mm (grades 3, 4, and 5), whereas 83% of the patients without disease showed a membrane thickening of <2 mm (grades 1 and 2 according to the classification of Lu et al).11
The above-mentioned correlation between signs of disease (discontinuity of the sinus floor, polypoid lesions, air-liquid levels, and sinus opacification) and the presence of a Schneiderian membrane measuring >2 mm thickness led us to associate discontinuity of the sinus floor and the presence of polyps with membrane thickening to reach >2 mm (P < 0.05). No statistically significant correlation was noted between opacification or air-liquid levels and membrane thickening. On the other hand, maxillary sinus opacification was found to be significantly more common in males than in females (P < 0.05).
Table 3 describes the thickness of the Schneiderian membrane and the cortical thickness of the floor of the maxillary sinus in the presence or absence of septa. The comparison of 2 means yielded a significant inverse relationship between the presence of septa and membrane thickness—the presence of Underwood septum being associated with a lesser thickness of the Schneiderian membrane.
Table 3: Descriptive Statistics of the Thickness of the Schneiderian Membrane and Cortical Thickness of the Sinus Floor in the Presence and Absence of Septa
No statistically significant differences were observed in the thickness of the Schneiderian membrane and the cortical thickness of the sinus floor according to gender. Likewise, no significant differences were observed between the left and right sides of the maxillary sinus with respect to the presence of septa, membrane thickness, or cortical thickness.
Discussion
CBCT is useful for evaluating the maxillary sinus and for the correct planning of treatment.6,16–18
Incidental findings in the maxillary sinus have been the focus of our study, which offers information on their frequency. In this context, anatomical variations and lesions of the maxillary sinus may imply a need for specific treatment or for modifying the planning of dental implant placement.19 20–24
In our series, pneumatization was found in 78.75% of the patients and was the most frequent of all observed anatomical variations. This percentage is lower than that reported by Lana et al20 14,25
In comparison, hypoplasia of the maxillary sinus is a much less frequent anatomical variation, with a reported incidence of 1.5%–10%.20,26–28
One of the most interesting features in sinus anatomy is the presence of bone excrescences, such as exostosis or septa. According to the literature, the presence of septa ranges between 13% and 66.7%.2,16,20,23,24,28–36 37
It is important to identify septa because they increase the risk of membrane perforation during implant placement.35 38,39
Membrane thickening is a characteristic feature of both acute and chronic sinusitis. According to Momeni et al,40 20 41
Few studies have examined the relationship between the thickness of the Schneiderian membrane, the presence of Underwood septum , and the thickness of the inferior cortical layer of the maxillary sinus. In our series, and in agreement with the observations of Cakur et al,42 P < 0.005). An increased incidence of membrane perforation has been reported when its thickness is less than 1.5 mm43,44 Underwood septum is present. In this context, when such septa are found to be present, the sinus lift procedure must be modified to avoid the risk of perforation.2 42
Opacification was observed in 7.5% of the examinations, which would suggest the occurrence of rhinosinusitis (formerly known as sinusitis). However, opacification can sometimes be found in abnormalities other than rhinosinusitis, such as mechanical trauma, barotraumas, and hemorrhage.45
Rhinosinusitis is clinically defined as an inflammation of the nose and the paranasal sinuses characterized by 2 or more symptoms, one of which should be either nasal congestion or nasal discharge (anterior/posterior nasal drip) in addition to facial pain/pressure and/or the reduction or loss of smell. We only considered the characteristic radiographic findings as air-liquid levels, membrane thickening, and opacification of the sinus.
Two types of rhinosinusitis—acute (<12 weeks) and chronic (≥12 weeks symptoms)—can be identified, according to the time elapsed from the onset. In reference to acute rhinosinusitis, Lindbaek et al44 46,47
In chronic rhinosinusitis, CBCT supports the clinical diagnosis and can be used to assess the extent of the disease, as well as to determine whether the process is unilateral or bilateral. On the other hand, CBCT also plays an important role in establishing a differential diagnosis with regard to other causes of opacification, such as mechanical trauma, barotrauma, bleeding, or neoplasms.48
Discontinuity of the sinus floor was relatively frequent in our series (18.1%), and it should be noted that 69.7% of the patients with this disorder also presented membrane thickening (>2 mm). Such discontinuity can have a number of causes, including dental infections with periapical lesions, the extrusion of endodontic filling material, apicoectomies,48
Polypoid lesions, in turn, are represented as mucosal retention cysts and antrochoanal polyps.
Because both lesions have a fluid density effect on the sinus, they cannot be distinguished by imaging techniques such as CBCT.49
On the other hand, antrochoanal polyp is a benign polypoid lesion that originates from the maxillary sinus mucosa and extends through its ostium to the choana. Its etiology remains unclear, and the lesion is more common in children and young adults. Due to the inability to distinguish by the radiographic study, both have been grouped under the same heading.
We observed the presence of polypoid lesions in 13.75% of cases, and most were unilateral. On the other hand, we found a statistically significant relationship between the presence of opacification and the male gender (P < 0.02).
Antroliths result in the calcification of masses of mucus or tissue detritus within the maxillary sinus. They can also develop in the presence of root fragments, bone particles, or foreign bodies.50–52 52 49 20
Foreign bodies can access the maxillary sinus through orosinusal communications that may persist as fistulas. Such invasion of the sinus can be caused by tooth extraction, endodontic treatment, or surgery.53–55
A high incidence of casual findings and anomalies in the maxillary sinus was recorded. We therefore recommend that a systematic and thorough examination of the sinus should be carried out before surgery in this anatomical region. Fortunately, most of the findings were benign, and in this context, inflammation of the paranasal sinuses is a very common alteration.
Inadequate residual bone height in the posterior maxillary region often limits standard implant placement. Lifting the maxillary sinus floor represents a solution to this problem. Sinus floor elevation using the lateral approach and the osteotome technique is an effective and well-documented therapeutic option for the rehabilitation of atrophic posterior maxilla. Although the use of short implants seems promising, the technique needs further investigation before it can be considered as effective as other techniques in the long term. One of its advantages is to reduce the occurrence of surgical complications and the impact on patients' quality of life.56
The present study is limited by its retrospective cross-sectional design and by the fact that a single trained observer evaluated the body of data. Nevertheless, the intraobserver reliability was adequate (98%). On the other hand, some conditions could not be differentiated because different fluids (eg, blood or pus) are radiologically identical. Larger series are needed to extrapolate the findings to the general population.
We did not encounter any correlation between the presence/absence of posterior teeth and the sinus findings, which may be explained by the fact that we did not consider the time elapsing since edentation.
Conclusion
Within the limitations of this retrospective study as an observational study and that CBCT does not have a Hounsfield Unit and thus is not able to differentiate liquids from soft tissue and different soft tissues themselves, we can conclude that the main finding in our study was a high prevalence of pneumatization of the maxillary sinus (present in 81.3% of the patients). We also documented other anatomical variations. A significant correlation was observed between a sinus membrane thickness of >2 mm and the presence of pathological alterations, as well as between a membrane thickness of <2 mm and the presence of septa.
Disclosure
The authors claim to have no financial interest, either directly or indirectly, in the products or information listed in the article.
Approval
The study was approved by an ethics committee (11/17/2014), and informed consent was obtained from all patients.
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