Anterior ethmoid and frontal sinus drainage pathways: five patterns formed and defined by their bony walls

Purpose To perform endoscopic sinus surgery safely and effectively, surgeons need to visualize the complex anatomy of the anterior ethmoid and frontal sinus region. Because this anatomy is so variable and individualized, the foundation of understanding lies in identifying, following, and visualizing the drainage pathway patterns and anticipating possible variations. Methods We studied 100 sides (50 cases: 22 male, 28 female, aged 12–86, average age 46.5 years, ± 19.5) using computed tomography (CT) and multiplanar reconstruction (MPR) to identify and classify the drainage pathways leading to the frontal sinus and anterior ethmoidal cells. Results Analysis revealed five patterns of drainage pathways defined by their bony walls: between the uncinate process and the lamina papyracea [UP–LP]; between the uncinate process and the middle turbinate [UP–MT]; between the uncinate process and the accessory uncinate process [UP–UPa]; between the uncinate process and the basal lamella of the ethmoidal bulla [UP–BLEB]; and between the basal lamella of the ethmoidal bulla and the basal lamella of the middle turbinate [BLEB–BLMT]. In most cases, BLEB formed the posterior wall of the drainage pathway of the frontal sinus, indicating BLEB could be one of the most important landmarks for approaching the frontal sinus. Conclusions As endoscopic sinus surgery depends on an understanding of this anatomy, this study may help surgeons to identify and follow the drainage pathways more accurately and safely through the anterior ethmoid to the frontal sinus.


Introduction
The anatomy of the anterior ethmoid and frontal sinus is complex, but improvements in imaging technology are helping us to understand these spaces more clearly. Many recent reports have identified and classified the cells of the anterior ethmoid and frontal sinus based on their location [1][2][3][4][5]. However, the drainage pathways of the frontoethmoidal region are variable and their paths tortuous due to multiple bony walls which form the pathways.
In our study, the drainage pathways are formed by some combination of two of the following: the middle turbinate (MT), the basal lamella of the middle turbinate (BLMT), the uncinate process (UP) and its variations (UPa), the basal lamella of the ethmoidal bulla (BLEB), and the lamina papyracea (LP). We followed each drainage pathway to its termination as a cell (in the anterior ethmoid or frontal bone) or as a frontal sinus (in the frontal bone). The frontal sinus was determined based on location and size. Rather than focusing on cells, this study identifies the drainage pathways themselves to improve our understanding of the anatomy of the anterior ethmoid and frontal sinus.

Materials and methods
Axial computed tomography (CT) scans were performed on Toshiba Alexion TSX-032A CT scanner using 1 mm thickness. InVesalius © was used for three-dimensional (3D) and multiplanar reconstruction (MPR). CTs were obtained from June 2020 through October 2020 from 100 sides (50 cases: 22 male, 28 female, aged from 12 to 86, average age 46.5 years, ± 19.5). Exclusion criteria included previous sinus surgery or the presence of sinusitis. Inclusion required confirmation of drainage pathways to the frontoethmoidal region.
To begin identification of a drainage pathway, we started in the middle meatus and followed the drainage pathway formed by the bony walls of the anterior ethmoid to its termination, which might be the frontal sinus or an anterior ethmoidal cell or cells. Anterior ethmoidal cells included any frontal cells at the transition from ethmoidal to frontal bone, not including the frontal sinus. The word "cell" in this paper may refer to a pneumatized DP or a terminal recess; these are difficult to differentiate. We considered the frontal sinus to be the largest cell in contact with the squamous portion of the frontal bone.
In the "fronto-ethmoidal transition region," coined by Zinreich et al., it can be difficult to distinguish between the uncinate process and the basal lamella of the ethmoidal bulla because of the labyrinthine nature of the ethmoidal complex [6]. We used MPR to trace continuity from the lower UP and BLEB to differentiate UP from BLEB. In some cases, an accessory lamella (UPa) forms from UP or BLEB. We counted only the frontal sinus, not other cells occurring in the frontoethmoidal region.

Results
After we had identified and named the five drainage pathway patterns, we calculated the prevalence for each pattern with 95% confidence interval (CI). Table 1 shows the prevalence of each drainage pathway pattern, the prevalence of each pattern terminating in a frontal sinus, and the prevalence of frontal sinus formation within each drainage pathway.
Note: For the figures, we selected 5 sides out of 100 total sides, both right and left. However, to reduce confusion and improve consistency, we inverted any left sides so that all figures appear as right sides.

Notation of drainage pathways
For example: [UP-LP] denotes the drainage pathway.
[UP-LP-> FS] denotes the drainage pathway leading to a frontal sinus.
[UP-LP-> C] denotes the drainage pathway leading to a cell or cells.  [UP-UPa] formed between UP and UPa, a lamella attached to FPM roughly parallel to UP. UPa is either a split UP or a pneumatized UP. We give an example of [UP-UPa] created by a pneumatized UP (Fig. 3).  (Fig. 4C). At a higher level of the ethmoid, the posterior margin of UP connected to BLEB (Fig. 4D), forming the suprainfundibular plate [7]. [UP-BLEB] ascended the anterior surface of BLEB along the junction with UP, then formed a cell or cells in the anterior ethmoid and FS in the frontal bone (Fig. 4A, , B  [BLEB-BLMT-> FS] was rare, found in only 5 sides (Fig. 5).

The five drainage pathways of the anterior ethmoid and frontal sinus
[BLEB-BLMT] began at the superior semilunar hiatus. [BLEB-BLMT-> C] formed posterior to the transition between the ascending and descending crus of BLEB is EB. However, this space may be occupied by a posteriorly extending [UP-LP-> C] or by a cell arising from the superior meatus.

Discussion
The developmental origins of the drainage pathways of the frontoethmoidal region can help us understand this complex region. Some authors, referencing Terracol and Ardouin, assert that the origin of FS lies in one of three primordial cell groups: orbital, nasal, or bullar [8][9][10]. When we apply their developmental model to our findings, the orbital cell group seems to correspond to [UP-LP] (ethmoidal infundibulum), the nasal to [UP-MT], and the bullar to [BLEB-BLMT] (superior semilunar hiatus). The developmental pattern seems to influence the drainage pathway pattern, and the drainage pathway pattern in turn is followed by surgeons during ESS. By following the bony walls of the five drainage pathways, the surgeon can imagine the drainage pathway itself and reach the targeted anterior ethmoid cell or frontal sinus. [UP-BLEB] forms from the anterior surface of BLEB, where the posterior margin of UP connects to BLEB forming the suprainfundibular plate. As noted earlier, unlike the other DPs, [UP-BLEB] tends to form a narrow opening as it is compressed by its lamellae. Pianta et al. describe a singular FSDP dividing the "agger complex" (between FPM and FSDP) and the "bullar complex" (between the FSDP and BLMT), which corresponds roughly to [UP-BLEB] [12]. However, our findings point to 5 possible FSDPs, none of which could be said to divide the anterior ethmoid into compartments.
[BLEB-BLMT] may be referred to as the superior semilunar hiatus.  In our study, 95% of the FS drainage pathways were anterior to BLEB; in almost all sides, the anterior margin of BLEB connected to the skull base to form the posterior wall of the drainage pathway. Therefore, BLEB, along with UP, may be the most important landmark for approaching the frontal sinus.
We are aware of the limitations of this study. Further study to assess interrater agreement may be necessary to address the possibility of familiarity bias. In addition, the CTs were from healthy subjects whose anatomy was free of bony remodeling. All of the subjects were Japanese; a more heterogeneous study population might reveal different results [13].
We believe, however, that this paper may clarify some issues related to the complex anatomy of the drainage pathways of the frontoethmoidal region: the developmental pathways leads to understanding of the drainage pathways, and the drainage pathways guide the surgeons through the anterior ethmoid to the frontal sinus.

Conclusions
Beginning in the middle meatus and following the drainage pathways, which themselves follow the developmental pathways, leads us to the cells and sinuses of the frontoethmoidal region. We hope this paper will help other surgeons to perform ESS more safely through a better understanding of the drainage pathways of the frontoethmoidal region.
Author contributions All authors contributed to the study conception and design. Material preparation, data collection and analysis were performed by TK. The first draft was written by TK and all authors commented on previous versions of the manuscript. All authors read and approved the final manuscript.

Conflict of interest
The authors have no relevant financial or non-financial interests to disclose.
Ethical approval This is an observational study. The Ethics Committee of Nose Clinic Tokyo has confirmed that no ethical approval is required.
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