Are Variations of Paranasal Sinuses and Infundibular Trace Length Responsible for Development of Maxillary Sinusitis?

The Ostiomeatal Complex (OMC) is a drainage mechanism for maxillary, frontal, anterior and posterior ethmoid cells. The OMC is composed of ethmoid infundibulum, uncinate process, ethmoid bulla, semilunar hiatus and medial meatus. Normal mucociliary drainage is related to ostium opening. Even with open ostium, a breakdown of mucociliary drainage, accumulating mucus and resulting with infection are claimed to occur in the contact of two opposing mucosal surface. Obstruction with mucociliary drainage dysfunction resulting in repeated inflammatory sinonasal diseases is thought to occur. Ethmoid Infundibulum (EI) which forms the main constitution of OMC was found to be wider and shorter than normal in children with acute complicated sinusitis and the uncinate process which forms the medial wall of the EI was found shorter in another study conducted on adults with chronic sinusitis.


Introduction
The Ostiomeatal Complex (OMC) is a drainage mechanism for maxillary, frontal, anterior and posterior ethmoid cells. The OMC is composed of ethmoid infundibulum, uncinate process, ethmoid bulla, semilunar hiatus and medial meatus. Normal mucociliary drainage is related to ostium opening. Even with open ostium, a breakdown of mucociliary drainage, accumulating mucus and resulting with infection are claimed to occur in the contact of two opposing mucosal surface. Obstruction with mucociliary drainage dysfunction resulting in repeated inflammatory sinonasal diseases is thought to occur. Ethmoid Infundibulum (EI) which forms the main constitution of OMC was found to be wider and shorter than normal in children with acute complicated sinusitis and the uncinate process which forms the medial wall of the EI was found shorter in another study conducted on adults with chronic sinusitis.
The relation between sinonasal anatomical variations and sinonasal infections is not clear. While some researchers have claimed that anatomical variations increase chronic sinusitis risk, other researchers have not found a relation between sinonasal variations and sinusitis. Showing sinonasal anatomical variations before functional endoscopic sinus surgery blocks the possible complications. Computed Tomography (CT) is the preferred imaging modality for demonstrating sinonasal variations and pathologies. In this study, the anatomical variations of the OMC, in particular the length and width of EI are studied in relation to maxillary sinusitis and ostiomeatal disease to detect whether a correlation exists .

Material and Methods
Local ethics committee approval was obtained. Images of 200 (40.7%) females average age 40.36 ± 13.99 and 291 (59.3%) male with average age of 38 (12-85) totaling 491 cases with clinically proven rhinosinusitis are studied by use of scanning paranasal CT without contrast. Postoperative cases, those having sinonasal polyposis or sinonasal malignancy cases are excluded from the study. Paranasal CT images are acquired from the PACS retrospectively. Scans are performed with 64 slice (Aquilion 64, Toshiba Medical Systems, 2011, Japan) CT device. Scanning parameters in 64 detectors CT were as follows: FOV: 16 cm, collimation 64 × 1, gantry rotation time 0.6 s, slice thickness 1 mm, step value 0.64, 120 kV and 250 mA. Anterior and lateral scanogram are performed after patients lying down in supine position. Scanning in axial plan is realized from frontal sinus roof to mandible. The images are evaluated using Osirix soft ware (7.0, 64 bit, Switzerland). CT images of all the cases are evaluated by two exprienced radiologists. Coronal and sagittal Multiplanar Reconstruction (MPR) images are obtained through axial images. Infundibulum widths are calculated coronal plan images with 950% augmentation from uncinate process to outward contour of orbital medial wall ( Figure 1). Infundibulum length is measured coronal plan 3-D curved multiplanar reconstruction imaging with 100% augmentation drawing trace from
There was no relation between sinusitis scores and infundibulum length (p>0.05).
Length of EI are similar between scores 0-2 maxillary sinusitis (p>0.05) but width was much more in patients with having score 1 and ostium to semilunar hiatus (Figures 2 and 3). Uncinate process adhering with lamina papyracea is classified as type 1, cribriform plate as type 2, middle concha as type 3 EI (Figures 4-6). Anatomical variations such as Haller cell, uncinate aeration, ethmoid bulla, middle turbinate lamella aeration, bullous middle turbinate, paradoxical middle turbinate, septum deformity are recorded. Maxillary sinusitis is graded according to Lund and MacKay score.

Statistical Analysis
One way variance analysis (One way ANOVA) is used to compare between maxillary sinusitis score and EI length, width. Chi square test is used to compare between sinusitis score and nominal variants (sinus type, variations). Score 0 maxillary sinus is grouped as sinusitis is absent. Score 1 and 2 grouped as "sinusitis is present". T test is used to evaluate the difference between length and width, chi square test is used to compare with nominal variants and sinusitis status (present-absent)     2 maxillary sinusitis compared with those not having sinusitis (score 0) (p<0.05) ( Table 1).
The relation between sinusitis scores, infundibulum type and paranasal variations is summarized in Table 2. A relation between sinusitis scores and infundibulum types is not found (p>0.05). Haller cells are more frequent in score 1 (p<0.05). Sinusitis scores and uncinate aeration are not related to each other (p>0.05).
There is relation between sinusitis score and ethmoidal bulla (p<0.001). Ethmoid bulla is more frequent in score 1 maxillary sinusitis. Middle turbinate lamellar aeration is similar in score 0 and 1-2 patients. Any relation is not detected between sinusitis score and bullous middle concha (p>0.05). There were no significant difference between sinusitis score and paradoxical middle concha frequencies. Score 1 sinusitis is more frequent compared with score 0 and 2 sinusitis in patients with septum deformity (p<0.05). The relation between infundibulum type, paranasal variations and sinusitis scores is shown in Table 3. Ethmoid bulla is more frequent in patients who had score 1-2 sinusitis in comparison with those score 0 maxillary sinuses (p<0.01). Independent variants (infundibulum type, length, variations) that can affect existence of sinusitis are inserted in a logistic regression analysis and risk factors affecting sinusitis existence are analyzed by retrospective elimination method. An end logistic model is generated with statistically significant variants. Ethmoid bulla is found to be an independent risk factor affecting the existance of sinusitis with regard to this model. Sinusitis risk is increased 1.489 fold in patients had ethmoid bulla (Table 4).

Discussion and Conclusion
The OMC is comprised of ostium of the frontal sinus, frontal recess, maxillary sinus ostium, ethmoid infundibulum and middle meatus. Ethmoid infundibulum is the air passage connecting the maxillary sinus ostium to the middle meatus. The uncinate process comprises the medial wall. The lateral wall is formed by the lamina papyracea and frontal process of maxilla and the ethmoid bulla form the posterior wall. EI mainly drains the maxillary sinus [4,10]. It is thought that interference with the drainage process causes sinusitis. Whether bony alterations or mucosal pathologies at the OMC cause the obstruction, is a matter of ongoing debate. Study researching the relation between EI length, width and maxillary sinusitis is limited in   literature. Thorp et al. [21] report that the infundibulum is shorter and wider in children with acute sinusitis than in healthy children. Also they report that mucosal changes play a role more than bony changes in the ostiomeatal complex for sinusitis pathogenesis. Pruna [16] made 15 different quantitative measures of structures forming the OMC and report the uncinate process length is shorter in patients with sinusitis. Messerklinger [14] reports the anatomical variations of the middle meatus and infundibulum trigger inflammation by narrowing sinus ostia and the disease extends from there to the other related sinuses.

Sinusitis present (N=294) Sinusitis absent (N=688) p Average ± SD Average ± SD
Treatment modalities are also based upon the bony narrowing concept and therefore aim to widen the drainage routes for example by removing the uncinate process. Our study contradicts this while showing EI length measured drawing trace is not a risk factor for maxillary sinusitis. The ostium is found closed in patients with sinusitis. The infundibulum is widened probably due to the mass effect of inflammatory secretion and decreased mucociliary activity.
A lot of anatomical variations are seen in paranasal sinuses. Certain studies claim some anatomical variations cause inflammation and chronic rhinosinusitis by obstructing sinus drainage ways [6,7,17,20]. On the contrary, Kim et al. [9], Lerdlum et al. [11], Stallman et al. [20] and Katia et al. [17] report there is no relation between anatomical variations and rhinosinusitis as well as that local, systemic, environmental factors and intrinsic mucosal disease are more important in chronic rhinosinusitis pathogenesis. In the study any relation between Haller cell and sinusitis is not detected, on the contrary Haller cell is rarer in patients with sinusitis. A statistical relation between Haller cell existence and maxillary sinusitis is not detected by cone beam CT imaging in Mathew et al. [13]. Also, the relation is not detected in some other studies [9,15,19,20]. On the other hand, there is one study claim that Haller cell existence and narrow infundibulum are related to recurrent acute rhinosinusitis [1]. Nasal septum deformity is seen in 90% of population [1,6,17,22]. Orlandi et al reported that type 3 nasal deformity according to Mladina's classification has the higher frequency among chronic rhinosinusitis patients [23]. In our study, septal deformities are more frequent in score 1 maxillary sinusitis.
Fadda et al. report ethmoid bulla and ethmoid sinusitis are not related to each other [6]. A study claims there is assosiation between a big ethmoid bulla and maxillary sinusitis [18]. A relation between maxillary sinusitis and bullous concha is not statistically significant in some studies [16,17]. In our study ethmoid bulla is more frequent in patients who had score 1-2 sinusitis in comparison with those score 0 maxillary sinuses so there is correlation of maxillary sinusitis and ethmoid bulla. Ethmoid bulla can narrow the EI and cause maxillary sinusitis.
Bullous concha characterized by bullous part of middle concha pneumatization is reported 9-20%. Maxillary and ethmoid sinusitis can be formed because of bullous and deformed middle concha narrowing middle meatus in some studies [18]. Bullous concha and maxillary sinusitis are not related to each other in Smith et al. study with 883 patients [19]. Bullous middle concha paradoxical middle concha and maxillary sinusitis are not related to each other in our study. Also no significant difference is seen between the sinusitis score, bullous middle concha and paradoxical middle concha rates. However septal deformity is found more frequent in score 1 maxillary sinusitis.
There are some limitations in our study. The concurrence of different anatomical variations has not researched. Medial and lateral deviations of uncinate process are not evaluated. We did'nt calculate the volume of EI. EI volume may be more useful for evaluating the relation with the maxillary sinusitis. Before functional endoscopic sinus surgery reporting anatomical variations is necessary. Because existence of these anatomical variations can affect surgical approaches. These are important for preventing possible complications during surgery [12]. Our study declares the researched variations do not increase sinusitis risk except ethmoid bulla. It is thought that even if a long infundibulum tends to be obstructed and causes sinusitis in general, this condition is not important in the case of sufficient mucociliary activity.

Disclosure of Interest
The authors whose names are listed immediately below certify that they have NO affiliations with or involvement in any organization or entity with any financial interest (such as honoraria; educational grants; participation in speakers bureaus; membership, employment, consultancies, stock ownership, or other equity interest; and expert testimony or patent-licensing arrangements), or non-financial interest (such as personal or professional relationships, affiliations, knowledge or beliefs) in the subject matter or materials discussed in this manuscript.