A Prospective Study on the Anatomical Variations of the Frontal Recess and its Association with Computer Tomographic Signs of Sinusitis

Abstract

The frontal recess region has a complex anatomy and HRCT scans of the paranasal sinuses (PNS) are the gold standard in evaluating it. Classification systems have been established to identify the frontal recess cells. The objectives of this study are to describe the incidence of anatomical variations, classify the anatomy of the frontal recess using the IFAC & Kuhn’s classification systems, find the association between the anatomical variations and the incidence of CT signs of sinusitis.

A prospective study of patients undergoing HRCT-PNS was carried out. The frontal recess region was evaluated and classified as per both classification systems. The prevalence of each frontal cell was identified; presence of CT signs of sinusitis was noted and the correlation between the two was evaluated. 272 sides of HRCT scans were evaluated.

Prevalence of cells as per IFAC classification showed ANC - 98.2%, SAC-43.4%, SBC-33.1%, SAFC- 28.3%, FSC -25%, SBFC- 3.7% and SOEC- 2.2%. Prevalence of cells as per Kuhn’s classification showed ANC - 98.2%, Type 1- 38.2%, SBC-32.7%, FSC -24.3%, Type 3- 16.9%, Type 2- 12.9%, Type 4- 4.8%, FBC- 2.6% and SOEC-2.2%. Sinusitis was seen in 27.2% cases. A significant association was noted between the presence of SOEC, FSC and sinusitis as per both classification systems. (P=0.049 and P<0.001 respectively).

In conclusion the cells which lead to an anteriorly based drainage pathway are more common, but the presence of posteriorly based SOEC and medially based FSC have a higher association with sinusitis.

Introduction

The frontal sinus, its complex anatomy, and access to it have been a matter of concern since the late 19th century. The frontal recess was first described by Killian in 1903 and is shaped like an inverted funnel whose apex is at the frontal ostium [1]. The boundaries of the frontal recess are anteriorly the frontal process of maxilla, frontal beak, and agger nasi, posteriorly the basal lamella of the middle turbinate, medially the vertical lamella of the middle turbinate, and laterally the lamina papyracea [2]. Additional work by Van Aleya in the form of cadaveric dissections, helped identify the frontoethmoidal air cells [1]. The importance of these air cells became more pronounced with the advent of endoscopic sinus surgery and further developments in computed tomographic (CT) scans.

Kuhn et al. were credited for coming up with one of the first classification systems to help identify and describe these frontoethmoidal air cells using CT scans [1]. High Resolution multiplanar Computed Tomography (HRCT) scans became a gold standard in the pre-operative evaluation and diagnosis of the anomalies of the frontal recess region. Further advancements in anterior skull base surgery and the presence of critical structures such as the orbit and olfactory region, made the frontal sinus region a crucial navigation pathway. Further work was carried out by Wormald et al. to provide a consensus classification of these frontoethmoidal air cells with their effect on the frontal sinus drainage pathway. It was introduced to bring about more uniformity in the identification, teaching, and communication of outcomes of frontal sinus surgery [3].

This study deals with the anatomical variations of the frontoethmoidal air cells identified using HRCT scans of the nose and paranasal sinuses (PNS). The variations have been classified using both Kuhn’s classification and the recently devised International Frontal Sinus Anatomy Classification (IFAC) given by Wormald et al. in 2016. Although neither of the classification systems helps identify all the variations of the frontal recess area, each has its own merits and demerits. Using both classification systems help us get an idea about which classification system is easy to use, their drawbacks and helps us compare results with previous data which were compiled using Kuhn’s classification system. Given that the aetiology of frontal sinusitis is multifactorial, this study attempts to identify the variations, its prevalence, and its association with sinusitis.

The objectives of this study are to describe the incidence of anatomical variations of the frontal sinus using Kuhn’s and IFAC classification as seen on HRCT Paranasal Sinus (PNS) scans and to find the association between the anatomical variations and the incidence of radiological signs of opacification.

Materials and Methods

This is a prospective study conducted at our tertiary care center between January 2021 and October 2022 after approval by Institutional Ethics Committee (IEC 62/2021) and Clinical Trials Registry of India (CTRI) (CRTI/2021/05/03368).

HRCT- Nose and PNS scans were conducted in a Phillips 128 slice Computer Tomographic scanner. Scans were acquired in the axial plane and coronal and sagittal images were reconstructed. 136 patients were included in the study and their scans were collected irrespective of indication for the scan with informed consent. Inclusion criteria were patients with complete multiplanar CT scans of the Nose and PNS with equal to or less than 3 mm cuts and patients more than 18 years of age. Exclusion criteria were patients < 18 years of age, patients with fungal sinusitis, sino-nasal neoplasms, history of sinus surgery, maxillofacial trauma, incomplete CT scans, or CT scans with cuts more than 3 mm.

272 sides were evaluated for the frontal recess region which was then classified using the Kuhn’s (Table 1) and IFAC classification (Table 2) systems. The prevalence of each type of frontal cell and the presence of opacification of frontal sinus and frontal recess was documented. A correlation between sinusitis and the presence of a particular type of frontal cell was then analyzed using SPSS v23 (IBM Corp.) and pertinent statistical methods.

Table 1.

Kuhn’s Classification

Frontal recess cell	Description
Agger nasi cell	Anterior most ethmoidal air cell which appears as a swelling along the lateral nasal wall anterior to the vertical attachment of the MT
Type 1 Frontal cell	Single cell above the ANC
Type 2 Frontal cell	Two or more cells which pneumatize above the ANC
Type 3 Frontal cell	Single cell above the ANC which pneumatizes along the anterior frontal sinus table
Type 4 Frontal cell	Isolated cell within the frontal sinus and above the ANC
Supraorbital ethmoid cell	Ethmoid cell that extends from the frontal recess and over the orbit
Frontal bullar cell	Ethmoid cell above the ethmoid bulla which pneumatizes along the skull base and into the frontal sinus from the posterior frontal recess
Suprabullar cell	Ethmoid cell above the ethmoid bulla which pneumatizes along the skull base but does not extend into the frontal sinus.
Interfrontal sinus septal cell	Pneumatization of the intersinus septum

Table 2.

IFAC Classification

Cell type	Cell name	Definition
Anterior cells	Agger Nasi Cell	The cell that sits either anterior to the origin of the middle turbinate or directly above the most anterior insertion of the middle turbinate into the lateral nasal wall
	Supra Agger Cell	Anterior-lateral ethmoidal cell located above the agger nasi cell
	Supra Agger Frontal Cell	Anterior lateral ethmoidal cell that extends into the frontal sinus
Posterior cells	Supra Bullar Cell	Cell above the bulla ethmoidalis that does not enter the frontal sinus
	Supra Bullar Frontal Cell	The cell that originates in the supra-bullar region and pneumatizes along the skull base into the posterior region of the frontal sinus. The skull base forms the posterior wall of the cell
	Supra Orbital Ethmoidal Cell	An anterior ethmoid cell that pneumatizes around, anterior to, or posterior to the anterior ethmoidal artery over the roof of the orbit
Medial cells	Frontal Septal Cell	Medially based cell of the anterior ethmoid or the inferior frontal sinus, attached to or located in the interfrontal sinus septum

Statistical Analysis

Data was coded and recorded on MS Excel spreadsheet program. SPSS v23 (IBM Corp.) was used for data analysis. Group comparisons for continuously distributed data was made using independent sample ‘t’ test when comparing two groups. Chi-squared test was used for group comparisons of categorical data. In case the expected frequency in the contingency tables was found to be < 5 for > 25% of the cells, Fisher’s Exact test was used. In case of non-normally distributed data, non-parametric tests like Wilcoxon Test were used. Statistical significance was kept at p < 0.05.

Results

136 HRCT PNS scans were analyzed, and each side was evaluated separately (n = 272). The age range was between 18 and 74 years and mean age was 38 ± 13.82 years. Males were more than females (n = 158 and 114 respectively).

Of the 272 sides that were analyzed and classified as per the Kuhn’s classification system, the prevalence of cells was as follows (Fig. 1): ANC-267 (98.2%), SOEC-3 (1.1%), Type 1-104 (38.2%), Type 2–35 (12.9%), Type 3–46 (16.9%), Type 4–13 (4.8%), FBC-7 (2.6%), SBC-89 (32.7%), and IFSC-66 (24.3%). The most common cell was found to be the ANC which was found in 267 sides (98.2%) followed by Type 1 frontal cell, seen in 104 sides (38.2%). The cell with least prevalence was the SOEC which was found only in 6 sides (2.2%).

Fig. 1.

Graphical representation of the prevalence of cells as per Kuhn’s classification

While using the IFAC classification system the prevalence of cells was as follows (Fig. 2): ANC-267 (98.2%), SAC-118 (43.4%), SAFC-77 (28.3%), SBC-90 (33.1%), SBFC-10 (3.7%), SOEC-6 (2.2%), and FSC-68 (25.0%). The most common cell was the ANC which was found in 267 sides (98.2%) followed by SAC seen in 118 sides (43.4%). The cell with least prevalence was the SOEC which was found only in 6 sides (2.2%).

Fig. 2.

Graphical representation of prevalence of cells as per IFAC classification

Computer tomographic signs of frontal sinus opacification were identified on 74 sides (27.2%). (Fig. 3)

Fig. 3.

Pie chart showing the distribution of sinusitis

Using Kuhn’s classification, we noted that 66.7% of the participants with an SOEC had sinusitis. Fisher’s exact test was used to find the association between sinusitis with the presence of SOEC and a significant difference was found (p = 0.049) (Odds ratio 5.6). Similarly, 35.1% of the participants who were identified to have IFSC, also had sinusitis. Chi-squared test was used to find the association between the two and a significant difference was noted (p = 0.011) (Odds ratio- 2.14). (Table 3)

Table 3.

Correlation of Kuhn’s cells and sinusitis

	ANC	SOEC	Type 1	Type 2	Type 3	Type 4	FBC	SBC	IFSC
Sinusitis	72 (97.3%)	4 (5.4%)	30 (40.5%)	5 (6.8%)	16 (2.6%)	6 (8.1%)	2 (2.7%)	24 (32.4%)	66 (24.3%)
OR	0.55	5.6	1.14	0.41	1.54	2.41	1.67	0.98	2.14
p-value	0.616	0.049	0.229	0.066	0.205	0.122	1.00	0.951	0.011

Fig. 4.

Type 4 cell or Supra-agger frontal cell (SAFC)

Fig. 5.

Supra Bullar Frontal Cell (SBFC) or Frontal Bullar Cell (FBC)

Fig. 6.

Supra Orbital Ethmoidal Cell (SOEC)

Using the IFAC classification system, 66.7% of the participants with sinusitis also had an SOEC. Fisher’s exact test showed a significant difference of p = 0.049 (Odds ratio 2.53). Similarly, 40.5% of participants in the group with sinusitis had a FSC and Chi-squared test was used to find the association between the two variables which showed a significant difference of p = < 0.001 with an Odds ratio 2.05. (Table 4)

Table 4.

Correlation of IFAC cells and sinusitis

	ANC	SAC	SAFC	SBC	SBFC	SOEC	FSC
Sinusitis	72 (97.3%)	21 (41.9%)	24 (32.4%)	26 (35.1%)	5 (5.4%)	4 (5.4%)	30 (40.5%)
Odds ratio	0.55	0.92	1.31	1.3	1.83	5.6	2.87
p-value	0.616	0.762	0.356	0.661	0.468	0.049	< 0.001

Discussion

Van Aleya carried out cadaveric dissections between 1939 and 1946 to give the first description of the fronto-ethmoidal sir cells [4]. As the frontal sinus and the endoscopic approach to it gained steady popularity, more and more studies were carried out to help identify and define the anomalies in this region. This study has identified these anomalies using two of the most commonly used classification systems- Kuhns and IFAC.

Kuhn’s Classification

Prevalence of the fronto-ethmoidal air cells in the HRCT scans of 136 patients is found to be as follows. Type 1 cell- 38.2%, Type 2 cell- 12.9%, Type 3-16.9%, Type 4 cell- 4.8%, ANC- 98.2%, SOEC-2.2%, FBC-2.6%, SBC-32.7% and IFSC-24.3%. A positive correlation was noted between sinusitis and the presence of SOEC (p = 0.049) and IFSC (p = 0.011) cells.

Correlating with previous studies which have been carried out we found that in the study by Lee et al., the first descriptions of the frontal recess cells were given using CT scans with 5 mm cuts, they found the prevalence of ANC to be the highest at 89%, which is similar to our study and the lowest to be a Type 4 cell at 0% and SOEC-62%, which stand in contrast to our study. [2] DelGaudio et al. carried out the first multiplanar CT scan study and identified the prevalence of frontal recess cells to be only 25.5%. Their study noted the highest prevalence to be that of a meagre 15.6% of Type 1 cells and just 1.4% of Type 2 cells. They also noted no association between the prevalence of these cells and sinusitis, which aligns with the results of our study [5].

A study on the Turkish population by Tuncyurek et al. showed a very low prevalence of frontal cells in the entire study population at 32.1%. Type 1 is the most common at only 15.7% and Type 4 cells are the least at 0.4% [6]. Another study on an Egyptian population noted the prevalence of frontal cells to be 78.571% with Type 2 being the most common at 26.429% and Type 4 being the least at 8.571%, which is almost comparable to our study. No significant difference between the presence of these cells and sinusitis was found [7]. Although the studies have been carried out in populations with a similar racial profile, a distinct difference has been noted in the prevalence of frontal cells.

Studies on the Asian populations in China carried out by Han et al. with multiplanar-thin slice CT scans showed frontal recess cells to be present in 39.6% of cells. ANC- 94.1%, Type 1- 24.4%, Type 2–7%, Type 3- 8.2% and no Type 4 cells, SBC-36.6%, SBFC-9% and IFSC-12.4%. SOEC cells were not identified [8]. A similar study conducted in Japan by Kubota et al. showed ANC, Type 1 cells, Type 2 cells, type 3 cells, Type 4 cells, SOEC, SBC, FBC, and IFSC to be at 88%, 37%, 6.3%,4.3%, 1.3%, 6%, 37%,7%, and 8.6% respectively. A significant association was noted between the presence of FBCs and frontal sinusitis (p = 0.043). These two studies show a similar prevalence of frontal recess cells which can hint towards a racial predisposition in the prevalence of frontal cells [9].

A study was carried out in the Indian population by Sagar et al. using multiplanar CT scans and Kuhn’s first classification on patients with chronic sinusitis who underwent FESS. The results showed Type 1, Type 2, Type 3, and Type 4 cells were 44%, 8%, 48%, and 2%. Type 3 cells were at a higher prevalence in this study as compared to ours, while the rest of the cells have a comparable prevalence to our study [10].

International Frontal Sinus Anatomy Classification

In 2016, Wormald et al. developed a consensus document termed the IFAC which was built on the works of Van Alyea, Kuhn, and others [3]. In our study using the IFAC system, we noted the prevalence of frontal recess cells as follows. Anteriorly based cells- ANC- 98.2%, SAC-43.4%, SAFC-28.3%; Posteriorly based cells- SBC- 33.1%, SBFC-3.7%, SOEC-2.2%; and medially based cell- FSC-25%. A positive correlation was found between sinusitis and the presence of SOEC (p = 0.049) and FSC (p < 0.001).

Anteriorly Based Cells

The cell with the highest prevalence in almost all studies is the ANC. Prevalence of SAC and SAFC was 16.3% and 13% in the study conducted by Tran et al.; 28.7% and 15.8% in the one conducted by Pham et al. which shows a lower prevalence of anteriorly based cells in the East Asian population as compared to our study which showed 43.4% and 28.3% of SAC and SAFC respectively and other studies as depicted in the table above [11, 12].

Posteriorly Based Cells

In most studies, posteriorly based cells were more common in comparison with the anteriorly based cells except the ANC. SBCs were more prevalent in the studies as 72% [13], 88.8% [14], 77.2% [15], 60.8% [16], and 59.7% [12]. The Indian study by Seth et al. showed a prevalence of 36.1% which is comparable to our study (33.1%). On the other hand, SBFCs have been found to have a lesser prevalence among the studies including ours (3.7%), the highest being 26.5% as identified by Sommer et al. The prevalence of SOECs has been variable, in our study we found SOECs in only 2.2% of the population but other studies showed a prevalence to be as high as 39.4% [14, 17].

Medially Based Cells

The lowest prevalence of FSC was given by Fawzi et al. at 8.3%, though there has been a uniform distribution among other studies- Choby et al-at 30%, Sommer et al-at 27.7%, Gotlib et al-at 27.2%, Seth et al- 21.1% which is also comparable to our study- 25%. [13–17]

Frontal Cells and Sinusitis

The analysis of the presence of sinusitis by identification of computer tomographic signs of opacification and its association with the frontal cells was carried out in 4 studies. The studies carried out by Sommer and Seth et al. identified no correlation between the two variables [14, 17]. Whereas the studies carried out by Fawzi and Pham et al. identified a positive correlation between the two variables. Fawzi identified SOEC and FSC to correlate with sinusitis (p = 0.001 and p = 0.044 respectively) which is similar to the results of our study, SOEC (p = 0.049) and FSC (p < 0.001). Pham et al. identified that SAFC (p = 0.002) and SBFC (p = < 0.001) correlate with the development of sinusitis. [12, 16]

Comparison Between the Two Classification Systems

Although Kuhn’s classification system gave an elaborate classification system for the frontal recess cells, the need for a new classification system was predominantly for a better description of the cells as per position, to identify its effect on the drainage pathway, and to make it easier for teaching and communication purposes. The inter and intra-rater studies also suggest that the IFAC classification system is much more reliable and reproducible as compared to Kuhn’s classification [18, 19].

In this study, we noted that Kuhn’s classification system has certain advantages over IFAC. First is the distinction between Type 1 and Type 2 cells, which helps identify multiple cells above the ANC which can have significant intra-operative importance during frontal recess clearance, which in IFAC has been clubbed into the SAC. The second is the distinction between a Type 3 and Type 4 cell which has been termed an SAFC. Clearing a Type 4 cell may require a combined external and endoscopic approach, while a Type 3 cell may be cleared endoscopically. The disadvantage of Kuhn’s lies in its difficulty in identifying the adequate height of 50% or more of the frontal sinus, depending on the parasagittal CT slice, and an additional ambiguity in the definition of the supra- bullar cell.

The advantages of IFAC lie in its more specific description of the cells, easy-to-recall terms, and its effect on the FSDP which plays a major role during clearance of the frontal recess cells and the establishment of the FSDP. A better description of the cells with easier terms such as SAFC and SBFC help in fluid understanding of the origins of the cell which has further helped in easier identification of the cells.

The limitations of this study are, that not all HRCT scans were in the required 1 mm cuts as the scans included in this study involved any patients undergoing HRCT scans of the nose and PNS, irrespective of the indication, to get a better idea of the prevalence in the general population. Additionally, no specific criteria regarding the type of sinusitis, or isolated frontal sinusitis were considered. The prevalence has been identified as per only one identifier and doubts if any were resolved with the help of the other authors.

The frontal cells have a varying prevalence, a hypothesis regarding variation in the pneumatization patterns as per race/ethnicity is ongoing as there is a difference in the prevalence of cells in Caucasians, Indians, and Southeast Asians as per most studies. Further studies are required to confirm this hypothesis. However, this was not the focus of our study. Although the frontal sinus and frontal recess anatomy can play a role and predispose a patient to frontal sinusitis, as is proved by our study, it cannot be stated as the only cause. Multiple other factors such as mucociliary clearance, comorbidities, inflammation, polyp formation, fungal infections, trauma, and fibrosis can also lead to frontal sinusitis.

Conclusion

The prevalence of frontal cells is largely variable. Multiple factors are responsible for the development of sinusitis, anatomical factors being one of them. Similar to other studies, the most commonly found variant was the ANC. In Kuhn’s classification, the second most common cell was the Type 1 cell, and the least common cell was the SOEC. As per the IFAC, SAC was the second most common and SOEC was the least common. Sinusitis was associated with the presence of SOEC and IFSC cells. Meticulous pre-operative evaluation of these cells with the help of CT scans is essential to carry out successful frontal sinus surgery.

Funding

Nil.

Declarations

Conflict of Interest

None.

Ethical Approval

The study was conducted after receiving approval from KMC & KH Institutional ethics committee.