Keywords
carotid artery - internal - paranasal sinuses/surgery - skull base - sphenoid sinus
            - sphenoid bone - tomography - X-ray computed
Introduction
            Surgical access to the anterior region of the skull base via transsphenoidal surgery
               is commonly used by otorhinolaryngologists. Radiologic assessment of this region pre-
               and intraoperatively is fundamental for surgeons to identify the neurovascular structures
               and their anatomic relationships, thereby reducing possible complications during and
               after surgical intervention. Computed tomography (CT) of the paranasal sinus is the
               best method for studying the anatomy and variation of this region.[1]
               [2]
               [3]
               
            The sphenoid sinus (SS) may show varying degrees and directions of pneumatization.
               Its various extensions and critical relationship to neurovascular structures make
               intimate knowledge of the anatomy of the region and its variations something essential.
               The internal carotid artery (ICA) is the anatomic structure that must be assessed
               in the region of the skull base before and during the surgery. Axial and coronal CT
               scans are indispensable for disclosing the location of the ICA.[4]
               [5]
               [6]
               
            In the clinical practice, CT assessment prior to surgery allows the relationships
               between the SS and the ICA, and between the lesion and the ICA, to be established.
               This is fundamental, for example, for planning the endoscopic surgical approach and
               for safe removal of the lesion with ICA control.[6]
               [7]
               
            The objective of the present study is to use the CT to analyze the lateral and posterior
               extensions of pneumatization of the SS and their relationship with parasellar and
               paraclival segments of the internal carotid artery (psICA and pcICA, respectively).
               The study also aims to determine the frequency of possible local anatomic variations
               of the SS in relation to these segments of the ICA adjacent to it.
         Methods
            This study was approved by the Research Ethics Committee of the Institution (CAAE
               14725713.7.0000.5479). A cross-sectional retrospective study of 90 paranasal sinus
               CT scans was performed in patients clinically indicated for this supplementary exam.
               Inclusion criteria: tomography scans of individuals older than 18 years of age, with
               rhinosinusal symptoms and request from physician ordering tomography assessment of
               the nose and paranasal sinus. Exclusion criteria: tomography scans identifying individuals
               with facial bone fractures, rhinosinusal neoplasms, or rhinosinusitis of the posterior
               paranasal sinus.
            Tomography scans were performed using an electro spin resonance (ESR) Hispeed helicoidal
               tomography manufactured by GE, model CT/e (Computed Tomography/helicoidal), series
               1676 HMS (GE, Boston, MA, USA). The analysis of the variables was performed using
               the eFilm 2.1 computer software program (Merge Healthcare Inc., Chicago, IL, USA).
            The exam protocol included the acquisition of images using the helicoidal technique
               on axial, coronal and sagittal planes, with reconstruction of 1.0/1.0 mm to 1.0/1.0 mm
               slices (slice thickness/increment). The first image on coronal or axial plane, which
               identifies the structures of the SS and the ICA, was used for the tomographic analysis
               in the anterior to posterior and superior to inferior directions, respectively.
            Based on the images acquired by the tomography scans, the following variables were
               assessed: the type of pneumatization of the SS, the extensions of the sellar type
               pneumatization, the anatomic variations of the ICA, the presence of septations, and
               the position of the sphenoidal septum.
            Classification of Anatomic Variations of the SS
            
            
            
            
               
               - 
                  
                  Classification of the extensions of sellar-type pneumatization into: lateral (lesser
                     wing, greater wing, pterygoid and complete (greater wing and pterygoid process) ([Fig. 1A], [Fig. 1B]) and posterior (critical and non-critical) ([Fig. 1C], [Fig. 1D]). Analysis of the lateral extensions on coronal plane and the posterior extensions
                     on axial plane. Two types of posterior extension were considered according to the
                     width between the posterior boundary of the SS and the clivus identified on the axial
                     slices. The type was defined as critical for thickness < 2 mm and non-critical for
                     clivus thickness ≥ 2 mm. 
 Fig. 1 Coronal plane: (A) lateral extension to greater wing (arrow), (B) lateral extension to greater wing and pterygoid process (complete) (arrow) and lesser
                  wing (dotted line). Axial plane: (C) critical posterior extension (arrow) and protrusion of paraclival segment (dotted
                  line), (D) non-critical posterior extension (arrow).
                  Fig. 1 Coronal plane: (A) lateral extension to greater wing (arrow), (B) lateral extension to greater wing and pterygoid process (complete) (arrow) and lesser
                  wing (dotted line). Axial plane: (C) critical posterior extension (arrow) and protrusion of paraclival segment (dotted
                  line), (D) non-critical posterior extension (arrow).
            
            
            
            Classification of Anatomic Variations of the Parasellar and Paraclival Segment of
               the ICA in Relation to the Lateral and Posterior Extensions of the SS
            
            
               
               - 
                  
                  Absence of protrusion, with protrusion, and presence of dehiscence. Analysis of the
                     psICA on coronal plane ([Fig. 2A]) and the pcICA on axial plane ([Fig. 2B]). Protrusion was defined as > 50% projection of the structure into the sphenoid
                     sinus and dehiscence as the absence of visible bone separating the ICA from the SS
                     along its path. 
 Fig. 2 (A) Coronal plane, protrusion of parasellar segment of the internal carotid artery (psICA)
                  and lateral extension of the sphenoid sinus. (B) Axial plane, protrusion of paraclival segment of the internal carotid artery (pcICA)
                  and posterior extension of the sphenoid sinus (SS).
                  Fig. 2 (A) Coronal plane, protrusion of parasellar segment of the internal carotid artery (psICA)
                  and lateral extension of the sphenoid sinus. (B) Axial plane, protrusion of paraclival segment of the internal carotid artery (pcICA)
                  and posterior extension of the sphenoid sinus (SS).
            
            
            
            Classification Regarding the Presence or Absence of Septations
            
            Analysis on Axial and Coronal Planes ([Fig. 3A], [Fig. 3B])
            
             Fig. 3 (A) Axial plane, presence of septations (arrows), (B) Coronal plane, presence of septation to the left (arrow), (C) Axial plane, sphenoid septum on sagittal plane (arrow) and protrusion of paraclival
                  segment (pcICA) and (D) Axial plane, deviation of the sphenoid septum in the direction of the paraclival
                  segment of the internal carotid artery (pcICA).
                  Fig. 3 (A) Axial plane, presence of septations (arrows), (B) Coronal plane, presence of septation to the left (arrow), (C) Axial plane, sphenoid septum on sagittal plane (arrow) and protrusion of paraclival
                  segment (pcICA) and (D) Axial plane, deviation of the sphenoid septum in the direction of the paraclival
                  segment of the internal carotid artery (pcICA).
            
            
            
            
            
            The chi-square test was used for statistical analysis of the data, and a 5% level
               of significance was adopted.
            Results
            Total 90 tomographic imaging exams were studied in patients whose ages ranged from
               19 to 84 years with a mean of 46 years (SD = 16.4) and median of 44 years. The sample
               comprised 33% males and 67% females.
            The analysis of the pneumatization of the SS in relation to the sella turcica revealed
               a predominance of the sellar type in 98% of the patients, the presellar type in 2%
               of patients and no cases of the conchal type. Lateral extension of pneumatization
               of the SS for the lesser wing of the sphenoid was found in 13% of the individuals,
               with the greater wing type in 47%, the pterygoid type in only 1%, the complete type
               in 23% and absent in 16%. The presence of posterior extension was found in 78% of
               the individuals, comprising critical type pneumatization in 42%, non-critical type
               in 36%, and absent in 22%.
            Protrusion of the psICA was found in 26% of the individuals and it was absent in 74%,
               whereas protrusion of the pcICA was noted in 35% and absent in 64% of the patients.
               Dehiscence of the pcICA was observed in four cases (3.6%), two of which were right
               side and two were left sides.
            The statistical analysis using the chi-square test for the association between protrusions
               of the pcICA and psICA was statistically significant (p < 0.001), as was the association between the lateral extension of pneumatization
               of the SS and protrusion of the psICA (p = 0.014) ([Table 1]). A presence of protrusion of the pcICA in individuals of the posterior extension
               of pneumatization of the SS was present in 46% and absent in 54% of the cases.
            
               
                  Table 1 
                     Percentage distribution of lateral extension of pneumatization of sphenoid sinus in
                        relation to protrusion of the psICA
                     
                  
                     
                     
                        
                        | Extension | Protrusion of psICA | Total | 
                              p
                               | 
                     
                     
                        
                        | absent | present | 
                     
                  
                     
                     
                        
                        | 
                              Lateral
                               | absent | 46 | 54 | 100 | 0.014 | 
                     
                     
                        
                        | present | 17 | 83 | 100 | 
                     
               
               
               
               Abbreviation: psICA, parasellar segment of internal carotid artery.
               
                
            
            
            Septations were present in 39% and absent in 61% of the individuals. On the chi-square
               test, no significant difference was observed between individuals exhibiting septations
               with or without posterior extension (p = 0.908).
            The deviation of the sphenoid septum either to the right or left was found in 60%
               of the individuals; on the sagittal plane, in 26%; deviation in the direction of the
               ICA, in 14%, and in one or more septum, in 5% of the CT scans. In those individuals
               exhibiting posterior extension, the position of the sphenoid septum most commonly
               observed was deviation. No significance was reached on the chi-square test (p = 0.289) ([Table 2]).
            
               
                  Table 2 
                     Percentage distribution of the position of sphenoid septum, confirmed by paranasal
                        sinus CT, according to the presence or absence of posterior extension of pneumatization
                        of sphenoid sinus
                     
                  
                     
                     
                        
                        | Extension | Sagittal plane | Deviation | ICA path deviation | Total | 
                              p
                               | 
                     
                  
                     
                     
                        
                        | 
                              Posterior
                               | present | 23 | 60 | 17 | 78 | 0.289 | 
                     
                     
                        
                        | absent | 35 | 60 | 5 | 22 | 
                     
                     
                        
                        | 
                              Total
                               |  | 26 | 60 | 14 | 100 |  | 
                     
               
               
               
               Abbreviations: CT, computed tomography; ICA, internal carotid artery.
               
                
            
            Discussion
            Extensive pneumatization of the SS can be associated with irregularities in the sinus
               wall featuring protrusions and recesses, such as prominences of the ICA. Computed
               tomography can help to identify the relationship of the ICA with the lateral and posterior
               extensions of pneumatization of the SS, and alert the surgeons to regions for possible
               injury occurrences.[8]
               [9]
               
            The present study evaluated the degree and types of pneumatization of the SS and their
               relationship with the paraclival (pcICA) and parasellar (psICA) segments of the ICA.
               These segments of the ICA are adjacent to the SS and can be damaged during expanded
               endoscopic approaches (EEA) to the skull base.[5]
               [7]
               [10]
               [11]
               
            In the literature, protrusion of the ICA ranges from 8 to 70%.[12] In the present study, however, the presence of psICA protrusion occurred in 26%
               of the individuals, while the presence of protrusion of the pcICA was detected in
               35%. In this study, a statistically significant association was found between protrusion
               of the psICA and pcICA (p < 0.001). Dehiscence in the pcICA was found in 3.6% of the individuals compared with
               5% of cases identified by Meloni et al,[1] 1.5% by Kazkayasi et al,[3] 14.4% by Johnson et al,[4] and 5.3% of cases by Unal et al.[13] In the current study, the pcICA and psICA were evaluated separately and no cases
               of dehiscence in the psICA was detected. Axial and coronal CT scans are indispensable
               for disclosing the location of these segments adjacent to the SS.[4]
               [5]
               [6]
               
            Assessment of pneumatization of the SS helps surgeons to elect the optimum approach
               and determine the impact of anatomic variations on the surgery.[9]
               [14]
               [15] In this study, the sellar type was the most frequent, found in 98% of the cases,
               the presellar type occurred in 2% of cases, while no instances of the conchal type
               were detected, mirroring the results of the study by Wang et al.[8] On CT, the configuration of the SS can be identified on sagittal plane, where the
               sellar type facilitates EEAs, with lower risk of injury to the neurovascular structures
               surrounding the SS, although there is less bone to remove during exposure of the operative
               region. However, it becomes easier to identify the landmarks, whereas for the presellar
               type, the SS walls tend to be thicker and more difficult for transsphenoidal approaches.
               Lateral and posterior extension may occur in sellar-type pneumatization, and a classification
               of these extensions is important as a guide to the approaches extending beyond the
               sella turcica.
            In the present study, the greater wing lateral type extension was the most frequently
               found, in contrast to Wang et al,[8] who predominantly found the complete type when the extension is to the greater wing
               and the pterygoid process. Both types facilitate access to the cavernous sinus, middle
               cranial fossa and petrous apex because there is less bone to remove. These disparities
               may be explained by individual variations in the population. The posterior extension,
               in turn, was identified in 78% of all CTs, comprising 42% critical and 36% non-critical
               types, demonstrating the high incidence of this anatomic variation. Haetinger et al[16] detected posterior extension in 69% of the cases and 44% of these were of the critical
               type. The critical type facilitates access to lesions located in the clivus and petrous
               apex, but there is an associated risk of perforation of the clivus due to the bone
               thickness of this region.[16] This classification of the lateral and the posterior extensions in the CT provides
               a guide to evaluate the degrees and directions of the pneumatization of the SS and
               its relationship with the psICA and the pcICA.
            In this study, extensions of pneumatization into the lesser wing were considered lateral
               type extensions because this definition better fits the classification of the lateral
               extensions on CT scans, given the location of this extension in the superior and lateral
               region of the SS and its relationship with both the optic nerve and psICA. On the
               other hand, Wang et al[7] classified the lesser wing type separately from the lateral extensions. This extension
               was found in 13% of the current cases.
            A statistically significant association was found between pneumatization of the lateral
               extension and the presence of protrusion of the psICA (p = 0.014). Pneumatization of the posterior extension and presence of protrusion of
               the psICA were relevant in 46% of the cases. This association disclosed on CT alerts
               surgeons of the impact of these variations on the surgery, whose outcome is linked
               to the increase of the SS to beyond normal anatomic limits. Thus, preoperative CT
               can identify areas with potential risk of complication, such as ICA injury in the
               SS featuring these extensions.
            The local variations of the SS identified on CT include deviations of the sphenoid
               septum and the presence of septations in the SS.[2] The computed tomography provides preoperative anatomic information regarding the
               course of the ICA to these local variations of the SS. Injury to the ICA can thus
               be avoided during surgery. In this study, for those individuals exhibiting posterior
               extension, the position of the septum most commonly observed was deviation, found
               on 60% of scans, although this association was not statistically significant (p = 0.289), 14% of the individuals had deviation of the septum in the direction of
               the pcICA, and septations were identified in 39% of the cases. No statistically significant
               difference between individuals exhibiting septations with and without posterior extensions
               was found (p = 0.908).
            The sphenoidal septum is often deflected to one side or the other, and can attach
               to the bone wall that protects the ICA, where fracture of the septum in order to gain
               access to the ICA can damage this artery.[2]
               [3]
               [9]
               [13]
               [17] There is a potential risk of injury when septations are located near the prominence
               of the ICA. Therefore, identifying the artery is crucial to keep a safe distance during
               tumor resection.[9]
               [18]
               [19]
               [20]
               
            An analysis of the anatomic variations of the SS observed on CT scans and their relationships
               with the segments of the ICA adjacent to the SS allows for more specific descriptions
               by the radiologists regarding patients who require EEA to the skull base, where key
               anatomic features are highlighted such as: the types of pneumatization of the SS and
               their extensions; irregularities in the walls of the psICA and pcICA; position of
               the septum in relation to the ICA and presence of septations in the SS. This information
               acquired, in conjunction with a preoperative assessment of imaging exams by the surgeon
               and their team, alert to all the aspects outlined above. Therefore, identifying the
               anatomic boundaries of this region for surgery can be done with more accuracy and
               reliability.
         Conclusion
            The evaluation of the SS preoperatively using a CT scan can aid surgeons to be prepared
               before performing an endoscopic skull base surgery. Particularly, it provides essential
               tools to know what will be found at the surgery, avoiding any iatrogenic lesion, such
               as damage to the ICA or noble structures, and thus allowing to better plan the surgery.
               The anatomic variations and their relationship should be reported by the radiologist.
            Preoperative recognition of the type of extensions of pneumatization of the SS, deviation
               of the sphenoid septum and presence of septations are beneficial to identify safely
               the psICA and pcICA adjacent to the SS. This information may be helpful if intraoperative
               surgical navigation is used.