대한비과학회

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INTRODUCTION

The frontal recess is an anatomically complex area with many variations. A thorough knowledge of the recess is essential for safe and successful endoscopic surgical man- agement of frontal sinus disease.¹⁾ This narrow space could be pneumatized by various frontoethmoidal cells (FECs), including the agger nasi cells (ANCs), frontal cells (FCs) type 1 to 4, suprabullar cells (SBCs), frontal bullar cells (FBCs), supraorbital ethmoid cells (SOECs) and interfrontal sinus septal cells (ISSCs).^{2) 3)} To differentiate FECs and understand the anatomy of the frontal recess, simultane- ous analysis with the axial/coronal computed tomographic

(CT) images and sagittal reconstruction is essential.^{4) 5)} The reported incidences of FECs vary widely in the literature.^6-12) The variation could be explained by differences in enrolled patients and/or interrater differences when examining CT scans.¹²⁾ Moreover, the CT scans used in previous studies had different cutting thicknesses or resolutions. The primary purpose of this study is to determine the prevalence of various FECs in patients with and without the frontal sinus/recess mucosal thickening sepa- rately through a detailed study of triplanar CT images.

Various FECs can narrow the frontal recess causing a partial obstruction of drainage and aeration of the frontal sinus.¹²⁾ To date, only few reports regarding the association between FECs and frontal sinus/recess disease exist, which is still unclear. Although there was a significant association of frontal sinus mucosal thickening with the presence of type 1, 2 and 3 FCs¹²⁾ or type 3 and 4 FCs,^{14) 15)} other authors were not able to find such association.^{6) 13)} In another report, rather than the FECs anterior to the frontal recess (ANCs and FCs), the FECs posterior and postero- - 31 -

Frontoethmoidal Cells on Computed Tomographic Analysis:

The Prevalence and Relationship to Frontal Sinus/Recess Mucosal Thickening

Seung Ju Lee, MD¹, Hyun Woo Kang, MD¹, Kwang Kyu Yu¹, MD and Hyun-Sook Kim, MD²

1Department of Otorhinolaryngology-Head and Neck Surgery;

2Department of Radiology, Eulji Hospital, Eulji Hospital, Eulji University College of Medicine, Seoul, South Korea

ABSTRACT

Objectives : To determine the prevalence of frontoethmoidal cells (FECs) in patients with and without frontal sinus/recess mucosal thickening and to establish the relationship between the FECs and the frontal sinus/recess mucosal thickening. Materials and Methods : We retrospectively reviewed 245 consecutive ostiomeatal CT scans (490 sides). The normal and frontal sinus/recess mucosal thickening groups were categorized based on these images. The latter group was sub-categorized into the frontal sinus mucosal thickening group (FS group) and the frontal recess mucosal thickening group (FR group). Results : Types 1, 2, 3 and 4 frontal cells were found in 17.5, 6.7, 8.3 and 0%of 326 normal sides, respectively. The prevalence of agger nasi, suprabullar, frontal bullar, supraorbital ethmoid and interfrontal sinus septal cells was 85.6, 43.3, 4.9, 4.3 and 17.2% of the same 326 normal sides, respectively. Type 3 frontal cells, frontal bullar cells and suprabullar cells were more prevalent in the FS and FR groups than in the normal group. All types of cells were more prevalent in the FS group, but only the suprabullar cells were more prevalent in the FR group than in the normal group. Conclusion : These findings suggest that type 3 frontal cells, frontal bullar cells and suprabullar cells may have a significant association with frontal sinus/recess mucosal thickening.

KEY WORDS : Frontoethmoidal Cells·Frontal Sinusitis·Computed Tomography.

Address correspondence and reprint requests to Seung Ju Lee, MD, Department of Otorhinolaryngology-Head and Neck Surgery, Eulji Hospital, Eulji University College of Medicine, 280-1 Hagye-dong, Nowon-gu, Seoul 139-711, South Korea.

Tel : +82-2-970-8276 · Fax : +82-2-970-8275 E-mail : [email protected]

Received for publication on October 30, 2013 Accepted for publicatoin on December 21, 2013

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lateral to the frontal recess (SBCs, FBCs and SOECs) were associated with the development of frontal sinusitis.⁶⁾ The secondary purpose of this study is to clarify the specific correlation of FECs to frontal sinus/recess mucosal thickening by comparing the frequency of these cells between groups of patients with and without frontal sinus/recess mucosal thickening.

MATERIALS AND METHODS

We retrospectively reviewed 269 consecutive ostiomeatal triplanar CT scans of Korean adult patients performed from March 2012 to February 2013. Each patient’s information such as age, sex and the purpose of the scan has been collected. These patients underwent CT scan- ning for the assessment of nasal symptoms such as nasal obstruction, rhinorrhea, posterior nasal dripping, anosmia, facial pain, headache, etc. Out of 269 patients, 24 patients were discarded: 4 was younger than 18 years, 12 had previous surgical changes, 8 had poor frontal sinus development, leaving 245 patients.

CT scans of the nasal cavities and paranasal sinuses were performed with contiguous axial cuts of 2mm thick- ness (120 kVp, 210mAs, FOV 180 ×180 mm) on GE Discovery 750HD CT scanners (GE Medical Systems, Milwaukee, WI, USA). The CT data were then recon- structed into coronal and sagittal images by GE workstation Adw 4.5 software (GE, USA). Each CT scan was studied jointly by one ENT surgeon (Lee SJ) and one radiologist (Kim HS). We evaluated coronal, sagittal and axial images for the presence of FCs type 1 to 4, ANCs, SBCs, FBCs, SOECs and ISSCs by the definitions and criteria for FECs by Lee et al.²⁾ Triplanar scrolling at a computer workstation facilitated identification of FECs.

Appropriate magnification and window setting improved bony detail, which was particularly useful in significantly diseased sinuses.

All CT images were evaluated for the presence of frontal sinus/recess mucosal thickening greater than 3 mm as in previous studies.^{6) 12-14)} One hundred forty-two CT scans (284 sides) were normal or nearly-normal without any sinus disease, regardless of the purpose of the scans.

Forty two CT scans showed unilateral frontal sinus/recess lesions. Consequently, no radiographic evidence of frontal sinus/recess mucosal thickening was found in 326 sides.

Sixty one CT scans (122 sides) showed bilateral frontal sinus/recess lesions. From all CT images, two major groups were categorized; the normal group and the frontal sinus/recess mucosal thickening group (164 sides). Then, the later group was sub-categorized into two groups; the frontal sinus mucosal thickening group (FS group) and the frontal recess mucosal thickening group (FR group). The FS group had mucosal thickening involving the frontal sinus with or without the frontal recess (110 sides), and the FR group had mucosal thickening involving only the frontal recess (54 sides).

The prevalence of each type of FECs was presented as total numbers and percentages. Using Fisher’s exact test, we compared the frontal sinus/recess mucosal thickening group, FS group and FR group with the normal group, respectively. Univariate and multivariate logistic regression analyses between the normal group and the frontal sinus/

recess mucosal thickening group were also performed.

Then, odds ratio and 95% confidence interval were calcu- lated for each FEC. Data were evaluated statistically using the SPSS program for Windows version 12.0 (SPSS Inc, Chicago, IL, USA). P values < 0.05 were considered sta- tistically significant. The study protocol for a retrospective

Table 1. The prevalence of frontoethmoidal cells and their relationship to frontal sinus/recess mucosal thickening.

Cell type

Normal group (n = 326) Number (%)

Frontal sinus/recess mucosal thickening group (n = 164)

Number (%) P

FC1 57 (17.5) 32 (19.5) 0.620

FC2 22 (6.7) 6 (3.7) 0.216

FC3 27 (8.3) 25 (15.2) 0.029*

FC4 0 (0) 1 (0.6) 0.335

ANC 279 (85.6) 147 (89.6) 0.256

SBC 141 (43.3) 97 (59.1) 0.001*

FBC 16 (4.9) 17 (10.4) 0.034*

SOEC 14 (4.3) 11 (6.7) 0.279

ISSC 56 (17.2) 26 (15.9) 0.798

* Statistically significant.

FC: frontal cell, ANC: agger nasi cell, SBC: suprabullar cell, FBC: frontal bullar cell, SOEC: supraorbital ethmoid cell, ISSC: interfrontal sinus septal cell.

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chart and CT review for research purposes was approved by the Institutional Review Board.

RESULTS

A total of 490 sides from 245 patients were assessed and used for the final data analysis. There were 150 male (61.2%) and 95 female patients (38.8%). The mean age was 42.8 years (range, 18 to 85 years) . Table 1 shows the prevalence of FECs in sides with and without frontal sinus/recess mucosal thickening. Of the 326 normal sides (66.5%), type 1, 2, 3 and 4 FCs were found in 17.5% (57 sides), 6.7% (22 sides), 8.3% (27 sides) and 0%, respectively. The prevalence of ANCs, SBCs, FBCs, SOECs and ISSCs was 85.6% (279 sides), 43.3% (141 sides), 4.9%

(16 sides), 4.3% (14 sides) and 17.2% (56 sides), respectively.

Of the 164 sides with frontal sinus/recess mucosal thickening (33.5%), type 1, 2, 3, and 4 FCs were found in 19.5%

(32 sides), 3.7% (6 sides), 15.2% (25 sides) and 0.6%

(1 side), respectively. The prevalence of ANCs, SBCs, FBCs, SOECs and ISSCs was 89.6% (147 sides), 59.1%

(97 sides), 10.4% (17 sides), 6.7% (11 sides) and15.9%

(26 sides), respectively. Type 3 FCs, SBCs and FBCs were more prevalent in the frontal sinus/recess mucosal thick- ening group than in the normal group (p = 0.029, 0.001 and 0.034, respectively). From univariate and multivariate analysis, relatively higher presence of frontal sinus/recess mucosal thickening was observed in type 3 FCs, SBCs and FBCs (Table 2).

Table 3. The prevalence of frontoethmoidal cells in normal group, frontal sinus mucosal thickening group and frontal frontal recess mucosal thickening group.

Cell type

Normal group (n = 326) Number (%)

Frontal sinus mucosal thickening group (n = 110)

Number (%) P^†

Frontal recess mucosal thickening group (n = 54)

Number (%) P^‡

FC1 57 (17.5) 23 (20.9) 0.476 9 (16.7) 1.000

FC2 22 (6.7) 3 (2.7) 0.155 3 (5.6) 1.000

FC3 27 (8.3) 21 (19.1) 0.004* 4 (7.4) 1.000

FC4 0 (0) 1 (0.9) 0.252 0 (0)

ANC 279 (85.6) 96 (87.3) 0.752 51 (94.4) 0.083

SBC 141 (43.3) 65 (59.1) 0.004* 32 (59.3) 0.038*

FBC 16 (4.9) 13 (11.8) 0.024* 4 (7.4) 0.505

SOEC 14 (4.3) 10 (9.1) 0.087 1 (1.9) 0.705

ISSC 56 (17.2) 16 (14.5) 0.557 10 (18.5) 0.846

† Fisher’s exact test was performed between normal group and frontal sinus group.

‡ Fisher’s exact test was performed between normal group and frontal recess group.

FC: frontal cell, ANC: agger nasi cell, SBC: suprabullar cell, FBC: frontal bullar cell, SOEC: supraorbital ethmoid cell, ISSC: interfrontal sinus septal cell.

Table 2. Results of logistic regression analysis for normal group and frontal sinus/recess mucosal thickening group.

Cell type Univariate analysis Multivariate analysis

OR 95% CI P OR 95% CI P

FC1 1.14 0.71-1.85 0.583 1.25 0.74-2.10 0.411

FC2 0.53 0.21-1.32 0.171 0.72 0.27-1.89 0.504

FC3 1.99 1.12-3.56 0.020* 2.33 1.25-4.37 0.008*

ANC 1.46 0.81-2.63 0.211 1.22 0.64-2.30 0.546

SBC 1.90 1.30-2.78 0.001* 2.52 1.65-3.85 0.000*

FBC 2.24 1.10-4.56 0.026* 3.89 1.80-8.40 0.001*

SOEC 1.73 0.76-3.95 0.193 2.09 0.89-4.95 0.093

ISSC 0.91 0.55-1.51 0.711 0.96 0.57-1.64 0.892

OR: odds ratio, CI: confidence interval, FC: frontal cell, ANC: agger nasi cell, SBC: suprabullar cell, FBC: frontal bullar cell, SOEC:

supraorbital ethmoid cell, ISSC: interfrontal sinus septal cell.

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Table 3 shows the prevalence of FECs of patients in FS group and FR group. In the FS group, type 3 FCs, SBCs and FBCs were more prevalent than in the normal group (19.1%, 59.1% and 11.8%, respectively) (p = 0.004, 0.004 and 0.024, respectively). In the FR group, only the prevalence of SBCs was increased compared to the normal group (59.3%, p = 0.038).

DISCUSSION

The reported prevalence of FECs varies widely in the literature. The variation could be explained firstly by in- clusion of patients with frontal sinus/recess inflammation.

The presence of mucosal thickening or polyps within the frontal recess makes it more difficult to distinguish FECs from nearby structures on a CT scan. A number of previous studies have not specifically divided the enrolled patients into those with and without frontal sinus/recess mucosal thickening. In this study, we have determined the prevalence of various FECs in normal group first. Then, the prevalence in the patients with frontal sinus/recess mucosal thickening was determined and compared. Re- cent studies of FECs in frontal recess by CT have focused on Asian adult population, therefore the ethnic difference must be considered.^{6-8) 16)} Finally, a small number of enrolled patients in the earlier studies may be a factor.^{2) 8-10)}

In the previous studies, the prevalence of type 1 (20~20.4%), 2 (7~14%) and 3 (7~8.2%) FCs in normal Asian patients,^6-8) increased a little to 28~37%, 17~20.7%

and 8~11% in normal Western patients.^{2) 8-10)} The prevalence in our study was more consistent with that in the Asian patients, predictably. Similar to most studies, we identified type 1 cells as the most common.2) 6-13) 17) How- ever, the second most common type of FCs was type 2,²⁾

6) 8) 12) 17) or type 3.7) 9-11) 13) We found that type 3 FCs were more frequently found than type 2 FCs in normal group, and the prevalence of type 3 FCs increased markedly in those with frontal sinus/recess mucosal thickening. Type 4 FCs seemed to be quite rare and we found only one side in FS group with a type 4 FC and mucosal thickening involving the dependent portion of the frontal sinus (Fig. 1). This episodic occurrence of type 4 FCs may make it difficult to decide any correlation of type 4 FCs to frontal sinus/

recess mucosal thickening. The prevalence of the ANCs in the earlier studies was 86~94.1%, without much difference between the ethnic groups or between the groups with or without frontal sinus/recess mucosal thickening.

Our results are consistent with the above studies.

Anatomically, ANCs and FCs which are found above ANCs occur anteriorly in the frontal recess,²⁾ and together they may narrow the frontal recess. Thus Langille et al reported that type 1, 2 and 3 FCs had association with fron-

Fig. 1. A type 4 frontal cell (white arrow) is seen in the left frontal sinus on the sagittal (A), coronal (B) and axial (C) CT images with the mucosal thickening involving the dependent portion of the sinus (asterisk).

A B C

Fig. 2. On left sagittal and axial CT images, the type 3 frontal cell (white arrow) attaches to the anterior wall of the frontal sinus whereas the frontal bullar cell (dashed arrow) to the posterior wall (A, C). This frontal bullar cell is seen above the type 3 frontal cell on the left side of coronal CT image (B). The frontal sinus shows total haziness (asterisk). On the right side of coronal CT image, a type 3 frontal cell (white arrow) above the agger nasi cell (black arrow) is also seen.

A B C

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tal sinus mucosal thickening, but their conclusion lacked detailed data.¹²⁾ In an analysis of 768 coronal CT scans which probably are not optimal for visualizing and char- acterizing all FECs, Meyer et al found a higher incidence of frontal mucosal thickening in patients with FCs type 3 and 4.¹⁴⁾ But, DelGaudio et al and Lien et al reported that FCs and ANCs were not associated with frontal sinusitis.^{6) 13)} Despite above controversies, our data show clear and statistically significant association between type 3 FCs and the development of frontal sinusitis by the high prevalence of type 3 FCs in frontal sinus/recess mucosal thickening group and especially in FS group. We think that type 3 FCs are more likely to narrow the frontal recess because they do extend into frontal sinus (Fig. 2). For the ANCs and type 1 or 2 FCs, the size or spatial relationship with other FECs clearly weighs heavier than the presence per se in the occurrence of frontal sinus/recess mucosal thickening.

FBCs, SBCs and SOECs occur posteriorly in the frontal recess along the skull base.²⁾ Contrary to the ANCs and FCs, the effect of these cells on frontal sinusitis has been dealt with in few reports.^{3) 12)} Both the FBCs and SBCs might obstruct the frontal recess posteriorly.^{2) 6)} SBCs have been more frequent in the normal Asian patients with the prevalence of 36~39.5%,^{6) 8)} than in the normal West- ern patients with the prevalence of 11~20%.^{2) 8) 10)} In our study, the prevalence of SBCs and FBCs in normal group, which was consistent with the previous studies increased significantly in the frontal sinus/recess mucosal thickening group and in the subdivided FS group. We think that this increase in the current study may support the recent conclusions by Lien et al which suggested that both the FBCs and SBCs might have significant association with the development of frontal sinusitis.⁶⁾

Uniquely and for the first time, we assumed that the patients with minimal mucosal thickening involving only the frontal recess may have different characteristics in the prevalence of FECs compared with those with more extensive frontal sinus mucosal thickening. Interestingly,

in the FR group, the prevalence of FECs did not differ significantly compared with the normal group. Only the prevalence of SBCs noticeably increased to that in the FS group, suggesting that SBCs might have a role in the development of frontal recess mucosal thickening (Fig. 3).

SOECs which extend over the orbit from the frontal recess open into the lateral aspect of the frontal recess.^6-12) On coronal CT images, SOECs are found lateral to the frontal sinus, whereas the FBCs are medial to it.¹⁶⁾ SOECs were overwhelmingly more frequent in the Caucasian group (64.6%) than in the Korean group (2.6%).⁸⁾ The presence of SOECs was reported to reveal significant association with the development of frontal sinusitis.⁶⁾ Zhang et al reported 11 cases of chronic rhinosinusitis with 12 SOECs, which hints at a possible effect of SOEC on chronic rhinosinusitis.¹⁶⁾ In our study, the prevalence of SOECs was consistent with the Asian studies,^6-8)but did not differ between those with and without frontal sinus/recess mucosal thickening, unpredictably.

The limitation of our study is that 2 mm cut CT images may not reveal all the cells, especially small type 1 or 2 FCs. However, small cells that are indistinguishable by the 2 mm cut CT slices may not have any effect on the frontal sinus/recess mucosal thickening. We believe that the suffi- cient number of patients have been enrolled for this study.

Also, the proportion of sides with frontal sinus/recess mucosal thickening was adequate (33.5%), compared to the previous study (14%).⁶⁾ However, the number of sides in FR group was relatively small to confirm more confined results. Lastly, the etiologic factors of frontal sinusitis are anatomic variations, mucosal inflammation, polypo- sis, etc. Thus, it is not possible at this stage to designate the cause-and-effect relationship between the presence of FECs and frontal sinus/recess mucosal thickening.

Despite these limitations, our data are statistically significant with considerable consistency to indicate an association between the presence of type 3 FCs, FBCs and SBCs and frontal sinus/recess mucosal thickening. We believe that directly extending cells to the frontal sinus

Fig. 3. On sagittal and axial CT images, mucosal thickening of left frontal recess (asterisk) is seen between the type 3 frontal cell (white arrow) and the suprabullar cell (dashed arrow) (A, C). On coronal CT image, a type 3 frontal cell on the left (white arrow) and an interfrontal sinus septal cell (black arrow) on the right are seen (B).

A B C

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and SBCs, along with the above etiologic factors will in- fluence the development of frontal sinus/recess mucosal thickening. For this reason, during endoscopic sinus surgery for frontal sinus, complete removal of these obstruct- ing cells is required in order to perform successful frontal sinus surgery.

CONCLUSIONS

In this study, the prevalence of FECs in patients without frontal sinus/recess mucosal thickening was consistent with that of the previous Asian studies. Type 3 FCs and FBCs that directly extend anteriorly and posteriorly to frontal sinus from the frontal recess and SBCs were more prevalent in the frontal sinus/recess mucosal thickening group than in the normal group. They all were more prevalent in the FS group, but only the SBCs were more prevalent in the FR group than in the normal group. These findings suggest that type 3 FCs, FBCs and SBCs may have significant association with frontal sinus/recess mucosal thickening.

저자역할(Author Contributions)

이승주, 강현우, 유광규, 김현숙은 본 연구에서 모든 자료에 접근 할 수 있었으며 자료의 완전성과 자료 분석의 정확성에 책임을 지 고 있습니다. 연구 기획 : 이승주. 자료 수집 : 강현우, 유광규. 자 료의 해석 및 분석 : 이승주, 김현숙. 논문 초안 : 이승주, 강현우.

논문 수정 : 이승주, 유광규. 통계 분석 : 이승주, 강현우, 유광규.

연구 총괄 : 이승주.

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