The forgotten foramina: a study of the anterior cribriform plate
Vincent Patron, Julie Berkaoui, Roger Jankowski, Emmanuelle LechaptZalcman, Sylvain Moreau & Martin Hitier Surgical and Radiologic Anatomy ISSN 0930-1038 Surg Radiol Anat DOI 10.1007/s00276-015-1471-2
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Author's personal copy Surg Radiol Anat DOI 10.1007/s00276-015-1471-2
The forgotten foramina: a study of the anterior cribriform plate Vincent Patron1 • Julie Berkaoui1 • Roger Jankowski2 • Emmanuelle Lechapt-Zalcman3 • Sylvain Moreau1,4 • Martin Hitier1,4,5
Received: 24 November 2014 / Accepted: 23 March 2015 Ó Springer-Verlag France 2015
Abstract Purpose The olfactory cleft has garnered interest since the advent of endoscopic skull base surgery. Its precise anatomy, however, is still partially unknown. According to Rouvie`re, an ‘‘ethmoidal foramen’’ is located in its anteromedial part and contains a process of the dura mater. In a more lateral and anterior location, a second foramen, the ‘‘cribroethmoidal foramen’’, contains the anterior ethmoidal nerve. The aim of this study was to verify the existence of these elements and to establish landmarks for surgery. Methods We performed an anatomical and histological study of eight olfactory clefts in four cadavers using both endonasal endoscopic and endocranial dissection. Results An ethmoidal and a cribroethmoidal foramen were found in, respectively, 100 and 75 % of cases. Their mean length was, respectively, 4.1 and 1.8 mm. They were located, respectively, in mean at 5.3 and 5.8 mm from the anterior ethmoidal artery. Conclusion Our anatomical study demonstrates the existence of both foramina. The ethmoidal foramen clearly represents an area of least resistance in the anterior part of
& Vincent Patron [email protected]
Department of Head and Neck Surgery, CHU de Caen, Avenue de la Coˆte de Nacre, Caen Cedex 9 14033, France
Department of Head and Neck Surgery, CHU de Nancy, Nancy 54035, France
Department of Pathology, CHU de Caen, Caen 14033, France
Department of Anatomy, UNICAEN, Caen 14032, France
INSERM U 1075 COMETE, Caen 14032, France
the olfactory cleft, which could predispose to anterior skull base cerebrospinal fluid leaks and meningoceles. Keywords Cribriform plate Skull base Anatomy Ethmoid Sinus surgery Cribroethmoidal foramen Ethmoidal foramen Cerebrospinal fluid leak Meningocele
Introduction The olfactory cleft (OC) has gained recent interest, thanks to the advent of endoscopic skull base surgery. Previously, it was known as a functional zone for olfaction, and the area of onset of rare pathologies such as olfactory neuroblastoma or olfactory glioma . In 2007, Jankowski et al.  showed that ethmoid adenocarcinoma originates in the OC and not in the ethmoid labyrinth. This led to refocusing surgery on this location, and to describing alternatives to external craniofacial resection, such as exenteration of the OC . As a result of this more focused surgery, which is both less invasive and more respectful of local anatomy, it became necessary to enhance the surgical anatomy of the OC and cribriform plate (CP). Few recent descriptions of the OC and CP are available for surgeons. Most recent works are radiological studies focusing on the thickness of the CP, or its height in relation to the ethmoidal roof, but there is no available literature providing an endoscopic description of the OC [1, 2, 6, 7, 24]. In addition, anatomical descriptions of the endocranial CP differ considerably. Most anatomical textbooks mention, but do not name, a hole at the anterior part of the CP for the passage of the anterior ethmoidal nerve and of a branch of the anterior ethmoidal artery (AEA) [9, 18–20, 27]. Lang  called this foramen the cribroethmoidal foramen (CF).
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Rouvie`re described in 1911 another foramen, more medial and posterior to the first . According to Rouvie`re, this foramen, that he called the ethmoidal foramen (EF), is occupied by a process of the dura mater. The aim of this study was first to describe the cribriform plate and the olfactory cleft located in ahead of the anterior ethmoidal artery, and then to verify the assertions made by Rouvie`re.
Materials and methods Four anatomical pieces were obtained from our University Anatomy Department: two pieces came from fresh male bodies injected with latex, when the two others, another male and one female came from frozen cadavers and were not injected. A bilateral dissection was performed each time. Anatomical dissections were performed in two successive steps: first, an endocranial dissection, second an endonasal dissection. Endocranial dissection First the cranial vault, and then the brain, were removed. The crista galli was also removed, and the orbital plates of the frontal bone were drilled, if necessary, to provide access to the anterior portion of the CP. The dura mater was very gently removed from the CP under microscopic magnification (Surgical microscope MC320 F12, Leica Microsystems, Wetzlar, Germany) using microsurgical instruments (Moria, Antony, France) (Fig. 1). The dissection began in the posterior CP and extended into its most
Fig. 1 Endocranial dissection steps. a Endocranial view after removal of the parietal bone and brain. b After partial microdissection of the dura mater. c After removal of the crista galli (black
anterior part. The olfactory fibers were sectioned just above their entry into the foramina, making it possible to elevate the dura. If present, the anterior foramina of the anterior CP were identified and samples of the anatomic structures they contained were extracted and sent to the pathologist for examination. Endoscopic dissection A total ethmoidectomy was performed, making it possible to identify the ethmoidal roof, the frontal recess and the anterior ethmoidal artery in its canal. The middle turbinate and its insertion into the ethmoidal roof were removed. The mucosa of the nasal vault was incised anterior to the CP on the horizontal process of the frontal bone. The mucosa was elevated in the subperiosteal plane and the dissection progressed in a posterior manner until the first nerve fibers of the CP were reached. The elevation of the mucosa was easily performed at the level of the CP as all the nerves had been cut during the endocranial dissection. The foramina were identified, if present, using a 23 gauge needle introduced from the endocranial side of the CP. The minimal distance between the most medial part of the AEA and the foramina was measured with a graduated instrument (Fig. 2). After the endonasal dissection, the anterior foramina of the anterior CP were measured from the endocranial side (length, shape). Pathological study Samples collected from the endocranial study were preserved in formaldehyde. Standard hematoxylin–eosin– safran staining was used to identify the structures.
asterisk) and sub-total removal of the dura mater (specimen N°3). Complete dissection of specimen N°3 is in Fig. 4
Author's personal copy Surg Radiol Anat Table 1 Length of the EF and distance from the AEA
Fig. 2 Endoscopic measurement of the foramina location. View of a left nasal fossa. White asterisk ethmoidal foramen, d distance between the medial part of the AEA and the foramen, Se septum, FO ostium of the frontal sinus
Results Endocranial and endoscopic studies The ethmoidal foramen was found in 100 % of cases. The EF was oval in shape (Fig. 3a–c) and was located in the medial part of the CP, in the continuity of the crista galli. Its mean length was 4.1 mm (±1.2) (Table 1) with a maximum of 6.5 mm in specimen N°4. Neither nerve nor vessel was seen macroscopically entering the EF, but fibrous tissue was observed lying on the nasal mucosa and very adherent to it.
Fig. 3 Endocranial view of the foramina after completed dissection. a Left cribriform plate of specimen N°2 after endocranial dissection with complete removal of the meninges, of the crista galli (black asterisk) and after endonasal dissection. We observe the large ethmoidal foramen located medially (white asterisk) and the
Distance from the AEA (mm)
N°4 right N°4 left
The mean distance measured endoscopically between the medial part of the AEA and the EF was 5.3 mm (±1.5). The shortest distance was 2 mm (specimen N°4 left) and the longest was 7 mm (specimen N°4 right). The CF was found in 75 % of the specimens. Macroscopically, a nerve was found entering the CF in all cases. In the two injected specimens, a vessel was seen following the course of the nerve. No individual CF was found in anatomic piece N°4 (Fig. 3c) but the CF seemed rather to have merged with the EF, conserving a nerve-like structure at its most anterior part. In all cases the CF was oval in shape and its location was both lateral and anterior to the EF (Fig. 3a, b). Its mean length was 1.8 mm (±0.6), with a maximum of 2.5 mm in specimen N°3 (Table 2). The mean distance measured endoscopically between the medial part of the AEA and the CF was 5.8 mm (±1.2; 4–7 mm) (Fig. 2).
cribroethmoidal foramen located more anterior and lateral (black arrow head). b Specimen N°3. EF must be differentiated from artifact fractures of the CP which exhibit irregular edges (white arrows). c Specimen N°4. Note the large right and left EF (white asterisk)
Author's personal copy Surg Radiol Anat Table 2 Length of the CF and distance from the AEA Specimen
Distance from the AEA (mm)
Table 3 Pathological study of the four specimens Specimen
Conjunctive tissue +
cells Left Right
tissue + nerves Fibrous
tissue + autolysis
Conjunctive tissue +
Conjunctive tissue + nerve root and ganglion + calcifications
Pathological study Histological analyses are summarized in Table 3. In the two fresh specimens, thin conjunctive tissue and nerve ganglion cells were found in both the CF and the EF (Fig. 4). It was impossible for the pathologists to ascertain the presence of the dura mater in the EF, considering that the tissue seemed too thin to be the dura mater. But calcifications similar to those described in the dura mater were found in specimen N°3. In the two specimens from frozen body, artifacts caused by autolysis made histological analysis impossible to interpret.
Discussion The CP is formed from the fetal age to the end of the first year, at which point its ossification is complete. The CP derives from the nasal capsule and starts its formation during the 5th week of gestation. At that time it is composed of cartilaginous pieces accompanying the formation of the cartilaginous crista galli and lamina mediana. In newborns, the ossification of the CP begins at its most
anterior part and proceeds in a posterior manner. From the first postnatal month, it progressively shifts from a vertical position to its final horizontal position at the age of 6 months [12, 17]. In adults, the dimensions of the CP, as well as its shape and inclination, the size of the crista galli and the relation of the CP to the sphenoid bone have been described in detail by several authors [8, 18, 20, 21]. The number of holes has also been studied . However, to our knowledge, no one before Rouvie`re mentioned the EF. Even now and in the most recent textbooks, the EF is rarely—or not at all—mentioned in the descriptive anatomy of the CP. We explain this by the fact that when observing the CP from above, the EF is almost always hidden by the bulge of the crista galli, which makes its identification difficult in most cases. Moreover, in its most anterior part, the CP is often narrowed by the bulge of the right and left ethmoidal roofs. In our study, we systematically had to drill through the crista galli to see the EF. This study is the first to focus on the anterior CP and its correlation with the anterior ethmoidal artery. We found that the ethmoidal foramen described by Rouvie`re was constant, and that the cribroethmoidal foramen was present in 75 % of cases. This lesser success in finding the CF may have several explanations: first, the CF can be inconstant. Second, the CF and EF may have merged naturally as the bone that separates them can sometimes be very thin. Third, the dissection of the CP may have led to the destruction of a thin bony bridge between the CF and EF. In addition, a nerve-like structure was present in the anterior part of the EF in the case with no apparent CF, which led us to consider the hypothesis that the second or the third theory is the most valid. Macroscopically, our results support Rouvie`re’s description of a process of the dura mater filling the EF. No nerves or vessels were seen in the EF during the dissection, only fibrous tissue overlying the nasal mucosa. Unfortunately, the histological examination in our dissection study failed to prove with certainty the presence of the dura mater in the EF. We found fibrous tissue and nerves in two anatomical pieces. In one piece, calcifications suggesting those of the dura mater were found, supporting the hypothesis of a process of the dura mater in the EF. This fibrous tissue was considered too thin by our pathologists to be the dura mater. However, there are a few descriptions of the dura mater at the level of the CP. Dare et al.  described a thinning of the dura mater during the passage of the olfactory fibers into the foramina of the CP. This may correspond to the observations of our pathologists. The histological examination found nerve structures in the EF. Clinically, no nerves were found during the dissection, contrary to the CF. An explanation for the presence of nerve ganglion cells within the connective tissue could
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Fig. 4 Pathological slice of the EF from specimen 3L. Nerve ganglion (black arrow head), nerve tissue (white arrow head), and calcification (black arrow)
Fig. 5 Surgical endoscopic view of a left CP meningocele (Me). a After removal of the middle turbinate (black arrowhead). Anterior ethmoidal artery (white arrow), ethmoidal roof (ER), septum (Se), frontal ostium (FO). b After removal of the meningocele. White
dotted lines limits of the CP; hole at the place of the meningocele at the anterior part of the CP (white arrowhead). You can notice that the hole is in continuity with the AEA canal: this meningocele probably originates from the EF
be that the ganglion cells described belong to the N cranial nerve. The N cranial nerve or cranial nerve 0 is a nerve whose existence has long been debated. It was first described by Brookover  in 1914. This nerve is very distinct in human fetuses and infants but has also been observed repeatedly in adult humans [18, 21, 26]. Its fibers pass through the CP, medial to those of the olfactory nerve fiber and on the lateral surface of the crista galli, and end in the nasal mucosa . The fibers probably arise from autonomic/neuromodulatory as well as sensory neurons. The N cranial nerve has been shown to release luteinizing hormone-releasing hormone and is, therefore, thought to play a role in reproductive behavior. Therefore, our results
bring to light the EF as a spot of choice to carry further studies on the N cranial hypothesis in human. The length of the EF measured 4 mm in mean and even 6.5 mm in one specimen, representing a real bone that is lacking in the anterior CP. This area of weakness in the anterior CP may have two major clinical consequences. First it may promote spontaneous cerebrospinal fluid (CSF) leak and meningoceles. Stammberger et al.  have already outlined that the roof of the anterior ethmoid and the olfactory fossa are areas of least resistance of the skull base. CSF leak and meningoceles have been reported in adults by several authors, describing a spontaneous dehiscence of the anterior part of the CP [5, 10, 22, 25]
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(Fig. 5). Pulsations of CSF through the EF could lead to progressive thinning of the dura mater and to the occurrence of a meningocele or a CSF leak. Even if a nerve was passing through this foramen, it is unlikely that this nerve entirely fills the EF as the foramen can measure up to 6.5 mm. The hypothesis of a large dehiscence of the cranial base at this level must be taken seriously into consideration. The interest of the EF during the surgery of the olfactory cleft is indeed the 2nd clinical consequence of this study and concerns both malignant and benign lesion of the area. We described the anatomic relationships of the EF and CF with the AEA, which will help surgeons to locate these foramina during endoscopic surgery. From the medial part of the AEA, which is easily identified during surgery, the EF lies on average 5.3 mm in the continuity of the AEA. After this distance there is a big risk of injuring the anterior CP at the level of the EF and creating a CSF leak. To conclude, despite its limitation as the number of specimen and the partial histological results, this study is the first to focus on the anterior CP and its endoscopic anatomy. Our anatomical study demonstrates the existence of both the ethmoidal and cribroethmoidal foramen described a century ago by Rouvie`re. The two foramina represent an area of least resistance at the anterior part of the olfactory cleft, which could predispose to CSF leaks, encephaloceles or tumor spread. Surgeons and radiologists need to be aware of these foramina to ensure correct diagnosis and treatment of their patient’s condition. Acknowledgments We would like to thank M. Mickael Guyard and Ms. Isabelle Leclerc for their technical support, and Pr. M. Tschabitscher, and Pr. P. Herman for their comments. Conflict of interest
8. 9. 10.
11. 12. 13.
The authors declare no conflict of interest.
Ethical standards The authors declare that the experiments comply with the currents French laws.
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