Basic Science Study Ear, Nose & Throat Journal “The Accessory Ethmoidal Canal Does Not 2022, Vol. 101(2S) 50S–55S © The Author(s) 2021 Article reuse guidelines: Necessarily Contain an Arterial Structure” sagepub.com/journals-permissions DOI: 10.1177/01455613211049656 journals.sagepub.com/home/ear Juan Ramón Gras-Cabrerizo, PhD1 , Maria Martel-Martin, PhD2, Juan Carlos Villatoro-Sologaistoa, PhD3, Francisco Reina De la Torre, PhD4, Rosa Mirapeix, PhD5, Anna Carrera, PhD4, Joan Ramon Montserrat-Gili, PhD6, Albert Pujol-Olmo, PhD6, and Humbert Massegur-Solench, PhD6 Abstract Introduction: The aim of our study is to describe the prevalence of the accessory ethmoidal artery in endonasal endoscopic cadaver dissections and to identify its intraorbital origin. Material and Methods: From 2018 to 2020, thirty-four nasal dissections were performed in seventeen adult cadaveric heads. We performed a complete ethmoidectomy to identify the ethmoidal canals. Then, we removed the bony canal and the lamina papiracea to verify the injected vessel and to confirm the vascular structure inside the canal. Results: We found the anterior ethmoidal canal (AEC) and the posterior ethmoidal canal (PEC) in 100% of nasal cavities (34/34). We identified 4 accessory ethmoidal canals (AcEC) in the 34 nasal fossae dissected (12%). All AEC contained an arterial vessel. The AcEC contained an arterial vascular structure in 2 cases, a neural structure in other specimen, and in the fourth case no structure could be verified. In 32 of 34 nasal cavities, the PEC contained an artery and only in 2 cases the PEC did not contain any vascular structure. In these specimens, we observed that the AcEC with an arterial vessel inside (6%) was closer to the posterior canal than the anterior canal. Conclusion: According to our findings, we can suggest that the presence of a canal does not necessarily imply the presence of an arterial vessel, and that presence of the accessory ethmoidal artery could be associated with the absence of posterior ethmoidal artery. Keywords ethmoidal, artery, middle, accessory, endoscopic 1 Department of Otolaryngology/Head and Neck Surgery, Hospital de la Santa Creu i Sant Pau, Universitat Autònoma de Barcelona and Corachán Clinic, Spain 2 Department of Otolaryngology/Head and Neck Surgery, Hospital Sant Joan Introduction Despı́ Moisès Broggi and Corachán Clinic, Barcelona, Spain 3 Department of Otolaryngology/Head and Neck Surgery, Hospital General de In the last years, there have been several reports published Cataluña, Universitat Autònoma de Barcelona and Corachán Clinic, about “another” ethmoidal artery different from the anterior Barcelona, Spain and posterior ethmoidal arteries. The authors refer to it in 4 Departamento de Ciencias Médicas (Grupo de Investigación en Anatomı́a different terms, such as supernumerary, tertiary, intermediate, Clı́nica, Embriologı́a y Neurociencia NEOMA) Universitat de Girona, Girona, accessory, or middle ethmoidal artery.1,2 The European po- Spain 5 Unit of Anatomy and Human Embriology, Universitat Autónoma de sition paper on the anatomical terminology of the internal nose Barcelona, Barcelona, Spain and paranasal sinuses suggests the term of accessory eth- 6 Department of Otolaryngology/Head and Neck Surgery, Hospital de la Santa moidal artery (AcEA) and it refers a prevalence of 40% ac- Creu i Sant Pau, Universitat Autònoma de Barcelona, Barcelona, Spain cording to the Lang J’s study.3,4 Received: August 6, 2021; revised: September 8, 2021; accepted: September However, neither the international anatomical terminology 10, 2021 nor the classical anatomy books make reference to AcEA,5-8 which creates serious doubts about its existence and if so about Corresponding Author: Juan Ramón Gras-Cabrerizo, PhD, Department of Otolaryngology/Head and its true anatomical origin. The different exploratory methods Neck Surgery, Hospital de la Santa Creu i Sant Pau, Universitat Autònoma and the various specimens used in order to identify the AcEA de Barcelona, Barcelona 08025, Spain. can explain this controversy. Email: jgras@santpau.cat Creative Commons Non Commercial CC BY-NC: This article is distributed under the terms of the Creative Commons Attribution-NonCommercial 4.0 License (https://creativecommons.org/licenses/by-nc/4.0/) which permits non-commercial use, reproduction and distribution of the work without further permission provided the original work is attributed as specified on the SAGE and Open Access pages (https://us.sagepub.com/en-us/nam/open-access-at-sage). Gras-Cabrerizo et al. 51S In addition, the anterior ethmoidal arteries are usually (Figure 1). All AEC contained an arterial vessel. The AcEC mentioned as possible cause of refractory epistaxis when the contained an arterial vascular structure in 2 cases, a neural sphenopalatine artery ligature fails. These arteries are re- structure in other specimen, and in the fourth case no structure sponsible for the nose bleeding in approximately 20% of could be verified (Figures 2–5). No case was bilateral. In 32 of cases.1,2 Exceptional intractable epistaxis can involve other 34 nasal cavities, the PEC contained an artery and only in 2 different arteries. These reports mention posterior ethmoidal cases the PEC did not contain any vascular structure. In these artery, the palatovaginal artery, or branches from facial artery specimens, we observed that the AcEC with an arterial vessel as possible causes.9-11Most of these studies note the possibility inside (6%) was closer to the posterior canal than the anterior of cauterization of the AcEA in order to control the epistaxis. canal. The aim of our study is to calculate the prevalence of the The ophthalmic artery (OA) and the optic nerve (ON) were AcEA in endonasal endoscopic cadaver dissections and to identified through the anatomical window below and above identify its intraorbital origin. the medial rectus muscle. In their intraorbital route, the an- terior ethmoidal artery (AEA) and the AcEA were situated inferior to the superior oblique muscle (SOM) in all cases. The Material and Methods posterior ethmoidal artery (PEA) was found superior to the From October 2018 to October 2020, thirty-four nasal dis- SOM. In all cases, the origin of the ethmoidal arteries (AEA, sections were performed in seventeen adult cadaveric heads PEA, and AcEA) was the ophthalmic artery. with no history of ENT pathology or surgery. The specimens belonged to the voluntary body donation program of the Discussion Anatomy Departments from the University of Girona and the Autonomous University of Barcelona, which follows the legal In recent years, several reports, especially endonasal endo- procedures and ethical framework governing body donation in scopic studies in cadavers, have described the existence of a our country. middle or accessory ethmoidal artery. It has been described a Eight cadaveric specimens had been fixed with Cambridge prevalence between 25 and 42% and in 14% of cases this solution, whereas in the other 9 specimens, we used the modified artery can be bilateral. It seems to be smaller and thinner than Larsen solution. All cases had been previously injected with the AEA and is located between both ethmoidal arteries, colored latex into the internal and external carotid system. usually closer to the PEA.12 Cadaver dissection following endoscopic endonasal ap- However, practically, only contemporary anatomical proach was performed using 0° and 45° rigid endoscope. We studies mentioned this third ethmoidal artery and it is not performed an uncinectomy with antero-posterior ethmoidec- present in the classical anatomical descriptions. The pioneer tomy and sphenoidectomy in both nasal cavities, in order to workers in ophthalmic branch arteries are Hayreh SS and have a complete view of the ethmoidal roof. We defined anterior ethmoidal canal (AEC) as the most anterior canal in the anterior ethmoidal roof located posterior to the anterior wall of the bulla. The posterior ethmoidal canal (PEC) was defined as the most posterior canal in the posterior ethmoidal roof in front of the most superior aspect of the anterior wall of the sphenoid sinus. The accessory ethmoidal canal (AcEC) was defined when we found a canal between the anterior and posterior canals. Then, we removed the bony canal and the lamina papiracea to verify the injected vessel and to confirm the vascular structure inside the canal. Finally, we removed the periorbita and we dissected the intraorbital space until to identify the ophthalmic artery and the origin of the ethmoidal arteries. Ethics Statement The Institutional Review Board of Santa Creu i Sant Pau Hospital approved all protocols and procedures used. Results Figure 1. Three ethmoidal canals (1-2-3) can be observed at the We found the AEC and PEC in 100% of nasal cavities (34/34). right ethmoidal roof. P = periorbita; FS = frontal sinus; MT = We identified 4 AcEC in the 34 nasal fossae dissected (12%) middle turbinate. 52S Ear, Nose & Throat Journal 101(2S) Figure 2. Right endoscopic view of the ethmoidal roof, showing an ethmoidal artery inside the AcEC. We can observe how the ophthalmic artery is the origin of this accessory artery.The posterior ethmoidal canal does not contain neither vascular nor neural structure. O = orbit; AEA = anterior ethmoidal artery; AcEA = accessory ethmoidal artery; MRM = medial rectus muscle; SOM = superior oblique muscle;OA = ophthalmic artery; FS = frontal sinus; SS = sphenoidal sinus; MT = middle turbinate. Figure 3. Absence of the right posterior ethmoidal artery with presence of the middle ethmoidal artery This specimen presents the same finding as the Figure 2. O = orbit; AEA = anterior ethmoidal artery; AcEA = accessory ethmoidal artery; MRM = medial rectus muscle; OA = ophthalmic artery; FS = frontal sinus; SS = sphenoidal sinus; MT = middle turbinate. Meyer F.13 They described in detail the origin of all branches proving the active extravasation after angiography with arising from the ophthalmic artery and showed a topographical embolization. Active extravasation arose from sphenopala- classification of the branches. They described the medial tine artery followed by anterior ethmoidal artery and facial branches of the OA as the ethmoidal arteries, the supraorbital artery. In no case was observed active extravasation from any artery, and muscular arteries. None of these arteries cross the accessory ethmoidal artery. Mostafa BE and cols14 per- ethmoidal complex except the anterior and posterior eth- formed a selective angiography of the ICA and ECA for 100 moidal arteries that were found in the ethmoidal roof. They did patients undergoing routine angiography. The ethmoidal not identify any artery between them. arteries were found in 95% of cases, while in 5% they were The angiography studies show very interesting findings. De absent, but none of them were listed as a third ethmoidal Bonnecaze G. and cols11 evaluated the origin of nasal bleeding artery. Gras-Cabrerizo et al. 53S Figure 4. No vascular or neural structure can be showed in the right middle ethmoidal canal (*). O = orbit; AEA = anterior ethmoidal artery; PEA = posterior ethmoidal artery; ON = optic nerve; FS = frontal sinus; SS = sphenoidal sinus; MT = middle turbinate. Figure 5. A neural structure can be exposure in the middle ethmoidal canal with both right anterior and posterior ethmoidal arteries present. O = orbit; AEA = anterior ethmoidal artery; PEA = posterior ethmoidal artery; EN: ethmoidal nerve; FS = frontal sinus; SS = sphenoidal sinus; MT = middle turbinate. Some studies have tried to explain the presence of the All these authors based their studies in the discovering of AcEA demonstrating the presence of multiple skull orbital foramina on the medial orbital wall in dry skull or cadavers foramina. Regoli M and cols,15,16 according to dry skulls, heads. But the presence of multiple foramina does not nec- observed 2 ethmoidal canals between 63% to 80% of cases, 3 essarily imply the presence of an arterial vessel inside. canals between 17% to 31% of cases, and in less than 2% we Other authors have adopted the use of computed tomog- observed 4 canals. raphy (CT) to research the anatomy of the ethmoidal canals Muller SK and cols17 found more than 2 ethmoidal foramina and have indeed identified the presence of middle ethmoidal in the 35% of 273 bone orbits examined of several ethnic artery. Yamamoto19 analyzed the CT images of 100 patients, groups. Abed SF18 reported similar data with approximately identifying a third canal in 21% cases and similar results 42% more than 2 ethmoidal foramina. (28%) were obtained by Ferrari M20 using cone beam CT. 54S Ear, Nose & Throat Journal 101(2S) The limitation of these studies was that the arteries were not research can potentially increase mankind’s overall knowledge that injected. can then improve patient care. Therefore, these donors and their Mason E and cols21 studied computed tomographic angi- families deserve our highest gratitude. ographies in fifty patients and had evidence of middle ethmoidal vessels in 38% of cases. Instead, in those patients where they Declaration of Conflicting Interests could not identify contrast, they decided to interpret bony fo- The author(s) declared no potential conflicts of interest with respect to ramina as evidence for a middle ethmoidal vessel. So, they the research, authorship, and/or publication of this article. considered the presence of foramina as an indication of an artery. Conversely, Monjas I and cols22 described forty CT- Funding injected cadaver nasal fossae and they did not find any The author(s) received no financial support for the research, au- middle ethmoidal artery. They interestedly found 1 case of thorship, and/or publication of this article. common ethmoidal trunk for the anterior and posterior eth- moidal artery arising for the ophthalmic artery. ORCID iD Finally, other studies based their finding in cadaver dis- section demonstrating more than 2 canals in the ethmoid roof. Juan Ramón Gras-Cabrerizo  https://orcid.org/0000-0001-9674- Probably the first dissection study about the AcEA in injected 1783 specimens was published by Lang and cols in 1990.23 They examined 71 arterial-injected orbits after the frontal bone was References removed and in 33% of cases showed a third ethmoidal fo- 1. Berens AM, Davis GE, Moe KS. Transorbital endoscopic iden- ramina that contains an artery. tification of supernumerary ethmoid arteries. Allergy Rhinology Berens AM1 dissected thirty-eight orbits using a trans- (Providence). 2016;7(3):144-146. orbital endoscopic approach identifying more than 2 eth- 2. Vatanasapt P, Thanaviratananich S, Chaisiwamongkol K. Land- moidal arteries in 58% of the orbits. However, these results mark of ethmoid arteries in adult Thai cadavers: application for have been analyzed with caution because of only 2 orbits were sinus surgery. J Med Assoc Thai. 2012;95(suppl 11):S153-S156. latex injected. Wang L and cols12 released a more exhaustive 3. Lund VJ, Stammberger H, Fokkens WJ, et al. European position paper about the presence of the AcEA. They dissected forty- paper on the anatomical terminology of the internal nose and four nasal cavities after intravascular injection and they paranasal sinuses. 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