Supplements and refinements to current classifications and nomenclature of the fronto-ethmoidal transition region by systematic analysis with 3D CT microanatomy*

Objective: The microanatomy of the fronto-ethmoidal transition region has been addressed in several classifications. CT stereoscopic imaging (3DCTSI) provides improved display and delineates three defined complex “spaces”, the Frontal Sinus/Frontal Recess Space, the Infundibular Space of the Ethmoid Uncinate Process, and the Ethmoid Bulla Space (FSRS, IS-EUP, EB), none of which were adequately described with the “cell” terminology. We present details on the 3D microanatomy, variability, and prevalence of these spaces. Methods: 3D stereoscopic imaging displays (3DCTSI) were created from 200 datasets. The images were analyzed and categorized by a radiologist (SJZ), and consultant otolaryngologists, focusing on 3D microanatomy of the fronto-ethmoidal transition, the frontal recess/frontal sinus, and drainage pathways, in comparison to established anatomical classification systems. Results: The anterior ethmoid is subdivided into seven groups with the following core properties and prevalence: 1. The horizontal roof of the IS-EUP is attached to the superior half of the frontal process of the maxilla (19%); 2. The IS-EUP extends into the frontal recess (6.5%); 3. The IS-EUP extends into the frontal recess and the frontal sinus (18.5%); 4. A bulla is seen in the medial frontal sinus (3%); 5. The ethmoid bulla and supra bullar space extend into the frontal sinus (7%); 6. Lamellae extend into the FSRS antero-superiorly (25 %); 7. FSRS expansion expands below the upper half of the frontal process of the maxilla (FSRS) (21%). Conclusion: 3-D analysis of the detailed anatomy provides important new anatomic information with the increased focus on precision surgery in the region.


Introduction
There have been several attempts, over the last 30 years to describe Frontal Recess (FR) anatomy and classify it into a system based on air cells. The intention has been to clarify the frontal sinus drainage pathway and enhance the surgical approach to the frontal sinus. Each of the proposed classification systems begin with the "simplest" pattern, the single agger nasi cell.
Most of the classifications were based on 2-dimensional CT coronal and multiplanar reconstructed images. As essential as these images are, they do not easily lead to an intuitive 3-D understanding of the frontal sinus drainage pathway's complexity (FSDP). Conversely, 3D CT stereoscopic imaging (3DCTSI) does provide the intuitive display of this regional anatomy, affording additional insight and details, which we feel complement the available practice-oriented classification systems (10,11) . All investigations and statements are made with reference to historic literature and currently used definitions referring to e.g. the frontal recess, the frontal sinus drainage pathway and the frontal bulla (12)(13)(14)(15)(16)(17)(18)(19)(20)(21)(22)(23)(24) .

Imaging equipment
Axial CT scans were performed on a Siemens CT scanner using 0.7 mm thick slices, which provided a volumetric image data set of the maxillo-facial structures. Studies were performed without administration of intravenous contrast material.
An advanced evolution of the Dextroscope imaging device was used to create 3D CT Stereoscopic Imaging displays (3DCTSI).
The device provides an "en bloc" 3D display of the imaging data.
The availability of a scrolling removal of the image data in any plane can be employed to display the anatomic information of interest. With a "virtual surgery" capability structures which obstruct the visualization of specific anatomic detail may be removed.
The 3DCTSI created by the Dextroscope imaging device are displayed on a stereoscopic monitor and are viewed with 3D electronic glasses. The stereoscopic display provides depth perception showing a structure, just as it would appear in nature.
The display of the 3D stereoscopic image on a "flat" surface presents a challenge, manifested by the 2.5 dimensional images presented in the manuscript.

Source of information
100 patients (200 sides) who had undergone CT of the sinuses over the past seven years, using an image guided protocol, aged 21-75 years old to evaluate the Frontal Sinus Drainage pathway.
The cases were selected from a pool of cases reported to have no inflammatory or neoplastic pathology. This was a retrospective study performed on de-identified CT data approved by The Johns Hopkins Medical Institutions IRB.

3D stereoscopic imaging evaluation
Our evaluation includes: the frontal sinus with the frontal recess (FSRS); the bony architecture of the uncinate process and its spatial configuration (IS-EUP); the relationship of these structures to the bulla lamella, and supra-bulla space; and the communicating/drainage passages, the middle meatus, the ethmoid and turbinal infundibulum; as well as the perimeter of these structures and interrelationships. The images were evaluated by SJZ with consultations provided by otolaryngologists (FAK, DK, AL, NRL, WH).

Results
The study is focused on the 3DCTSI appearance of the anterior ethmoid sinus spaces and the fronto-ethmoidal transition anatomy, and lack a uniformity in terminology and definitions" (8) . Attempts to clarify the anatomy of the paranasal sinuses, its description and definitions was attempted by Stammberger and Kennedy, with a panel of international experts in 1991 (13) , followed by the "Terminologia Anatomica" publication in 2011 (14) , and in 2014 the European Position Paper on the Anatomical Terminology of the Internal Nose and Paranasal Sinuses (8) . Furthermore, the description of the anterior ethmoid sinus anatomy and its relationship to the FSDP has been addressed by several classifications, the primary ones are above described (1)(2)(3)(4)(5)(6)(7)(8)(9) . Our aim is to augment the previous observations with those provided by 3DCTSI.
Table2. Grouping according to core features and individual variability of microanatomical spaces of the anterior ethmoid.

Core features (groups) and individual variability of microanatomical spaces of the anterior ethmoid.
Group 1. Standard IS-EUP with a singular space at the agger nasi (the "simple ANC"). (38/200 -19%   From the start of our evaluation, we were faced with the issue: Is the construct of the FS/FR, and anterior Ethmoid Sinuses assembled by "cells" or "spaces"? Conventional terminology (12)(13)(14)(15)(16)(17)(18)(19)(20)(21)(22)(23)(24) has long referred to the ethmoid sinuses as being a collection of individual air cells and the planar 2-dimensional CT images have cemented this concept in our minds, as a given fact  . Van Alyea, in his summary of the manuscript on "Frontal Cells" states "considerable confusion exists concerning the classification of minor cells in the frontal area, and that the term "frontal cells" is regarded as a fitting title for these cavities, and should not be confused with the major cavity of the frontal bone, the frontal sinus". Here Van Alyea shows his ambivalence regarding which term to use "cell vs. space" (20,21) .
However, in this case, Dorland's Medical Dictionary provides clarity in that "a cavity is a space within the body or in one of its organs" (22) . Terrier et al. described the structure of the paranasal sinuses to be the result of a centrifugal pneumatization giving shape to spaces with openings into common pathways for , and that compartment #1 drains into the EI (red arrow) and subsequently into the TI and maxillary sinus (black asterisk). The inferior compartment #2 drains into the TI (dashed red arrow), and into the Maxillary Sinus.
Larger red arrow: points to the TI which inferiorly then communicates with the maxillary sinus (hidden in these images).
A mucus clearance and exchange of air (42) . Pianta et al. referred to air spaces within their ABC classification, not cells (44) . Arun et al.
described the Frontal Recess as a "three-dimensional space connecting the Frontal Sinus with the nasal cavity" (27) . Thomas and Pallanch in their 3D CT reconstructions and virtual endoscopy of the frontal recess, reported explicit difficulties in subdividing the actual spaces of the anterior ethmoid into cells, blind pockets, recesses and segments of the frontal sinus drainage pathway (45) .
However, 3DCTSI demonstrates an alternative explanation, that The Uncinate Process, as previously detailed (11) , and shown in b.-d. 3D sagittal images viewed sequentially from medial to lateral reveal the multi chambered IS-EUP (IS-EUP, red and blue asterisks). The superior chamber (red asterisk) has an individual direct drainage into the MM and indirect drainage into the EI (red outline) (Fig. b). The FSRS (green outline) drains posteriorly and medially into the MM (curved red arrow) (Fig. b). The images also show the appearance of an infundibular space (Figs. c and d) (black asterisk) created by the convergence of the Bulla Lamella (blue outline), posteriorly and the uncinate lamella anteriorly (brighter gold outline).
This space has a supero-lateral opening affording communication with the FSRS, and infero-medially opens into the IS-EUP (black arrows).
Larger red arrow: points to the TI which inferiorly then communicates with the maxillary sinus (hidden in these images).
B C to posteriorly fuse, in the majority of cases, to the bulla lamella (BL). In its fusion with the mentioned anatomy the UL creates a 3-dimensional polyhedral space which communicates with the inferior EI and the TI (Figures 1-7), therefore creating two infundibular spaces: the IS-EUP, and the TI.
It is not our intention to change previously held beliefs, but to clarify previously held beliefs which do not adhere with the actual anatomic configuration(s) present. "Point in view" is the use of the term Agger Nasi Cell (ANC), which has a surgical inference i.e., the space lateral to the "mound" in the lateral nasal wall. The relationship between the ANC and the UP was first addressed by Zuckerkandl (1892) who described "the UP to form a "body" with the agger nasi, the free part of which is the agger, and the covered part is the uncinate process" (16) . Lang, similarly states: "the processus uncinatus represents the immediate continuation of the agger nasi and shows numerous variations of its setting, width, thickness, as well as connections with neighboring bones" (24) . In fact however, the "cell" is a polyhedral space, with borders above described, as well as an opening to the TI, therefore, is an infundibular space i.e., the IS-EUP (Figures 1-7).
That said, one should consider the "ANC" to be a compartment within the IS-EUP. c. 3D sagittal image reveals that the superiorly expanding space into the FSRS, is a "Terminal Recess" created by the superior merge between the uncinate lamella (gold outline) and the Bulla Lamella (blue outline), and that this space communicates directly with the EI (red arrow).  d.-e. Communication between the frontal "bulla" space (red star) with the IS-EUP (yellow asterisk) (red arrow) as well as the EI (yellow arrow).
f.-h. 3D sagittal images at various obliquities revealing the anteriorly "string shaped" lamella emerging from the EB with a proximal "v" shaped configuration (+) (Fig. f ) with its medial "branch" (black arrow) in figs. f and g, fusing with the uncinate lamella (gold outline), and the "lateral branch" is shown arising from the EB (red arrow) (Fig. h).
Group 2. The IS-EUP space may have 2 or more compartments, which expand into the FR (previously "type 1 & 2 K cells"; Wormald, single or group of cells above ANC). The compartments are within the outline of the UL and may extend to skull base.
In this group we also include a TR space, created by superiorly merging UL with BL, draining into the EI (an infundibular space).
Drainage of the IS-EUP is direct into the inferior EI, and TI ( Figure   2 A-C). isthmus, losing its connection to the frontal recess, resulting in a cell completely contained within the frontal sinus" (5) . In 2020 Altunay and Onerci reported communication with "the anterior and posterior cell systems" (9) . 3DCTSI reveals that the "Frontal Bulla Space" is a "balloon like" space within the FS attached by a "string like" or "thicker lamella" to the UL/BL or UL/CL. Opening  (Figs. c.-d.), reveal a fronto-bullar space (brown outline/yellow asterisk) expanding into the frontal sinus. The fronto-bullar space originates from the supra-bullar space, and noted to "balloon" anteriorly within the frontal sinus, similar to a "Frontal Bulla" space (Fig. 4). A second commonality with the "Frontal Bulla" is its lateral opening which communicates with the frontal sinus (yellow arrow). The fronto-bullar space communicates directly with the middle meatus, as does the supero-posterior compartment of the IS-EUP (red asterisk). The inferior IS-EUP communicates directly with the TI (red arrow). Note that the supra-orbital frontal spaces ( Note is to be made that The Fronto-Bullar Space, as previously described is the expansion of the Supra-Bullar Space anterosuperiorly into the FS, whereas the "Frontal Bulla" is a "balloon" like space within the FS attached by lamellae arising from the UL and BL as described above in the description of group 4. Group 6. "Compression / reduction" of the FSRS by antero-superiorly expanding lamellae. The following is Hajek's, reference to this entity: "The nasal opening of the FS is formed from parts of the ethmoid bone, that is, from the EB or its 'ground lamellas' and the UP. The anteriorly extended 'ground lamellas' diminish the nasal portion of the FS (23) . 3DCTSI reveals that in a number of instances, the Bulla, Uncinate, and the Common Lamellae Van Alyea first referred to the TR with the description "blind ending infundibulum" (21) . Stammberger described the superolateral fusion of the uncinate lamella to the FPM and LP as a "blindly ending infundibulum" later referred to as a Terminal Recess (12,13) .
The 3DCTSI reveals, that in certain cases, the superior Uncinate into the EI. The ILS should not be confused with Grunwald's "interlamellar cell" (18) , which was described by Stammberger to be a concha bullosa (12) (Figures 6 C, 7 A, C).   1-7). Note is to be made that our use of the word drainage refers to the opening in a defined space, affording mucus drainage and air exchange from that space.
The FSRS also communicates and empties into the Ethmoidal Infundibulum (EI), directly, or indirectly when the middle meatus joins the EI usually distal to the fused "suprainfundibular plate" (23) , between UL and BL, or as referred to by Bolger as the "genulike" feature in the anterior ethmoid (39) (Figures 2-7). The FSRS complex cases. To improve the display of the FSDP we were able to create a 3D CT display of the air within the FSRS, the IS-EUP, the EB, spaces, the maxillary sinuses as well as the FSDP, thus highlighting the drainage pathways and their association with the respective anterior ethmoid spaces. These air spaces are in blue color and appear in Figures 1-7.

Conclusions
Since the early publications by Van Alyea, Schaeffer, and others sometimes communicates through an opening in the IS-EUP roof directly into the IS-EUP space, with clearance into the nasal cavity through the TI and MM (Figure 7). The TI mucociliary drainage pathway is posterior into the nasal cavity through the Hiatus Semilunaris into the MM, and communicates directly and inferiorly with the maxillary sinus.