Variations in Paranasal Sinus Anatomy: Implications for the Pathophysiology of Chronic Rhinosinusitis and Safety of Endoscopic Sinus Surgery

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1 ARTICLE Variations in Paranasal Sinus Anatomy: Implications for the Pathophysiology of Chronic Rhinosinusitis and Safety of Endoscopic Sinus Surgery S.A.R. Nouraei, MBBChir, MRCS, A.R. Elisay, MD, A. DiMarco, MRCS, R. Abdi, MD, H. Majidi, MD, S.A. Madani, MD, and P.J. Andrews, FRCS (ORL-HNS) ABSTRACT Objectives: To study the radiologic anatomy of the paranasal sinuses in patients with and without chronic rhinosinusitis to assess whether anatomic variations are associated with disease pathology, and to identify those variants that may impact operative safety. Setting: Tertiary referral otolaryngology unit. Main Outcome Measures: Incidence and nature of anatomic variants with potential impact on operative safety, and the presence or absence of sinus mucosal disease and its correlation with anatomic variants with a potential impact on mucociliary clearance. Methods: We reviewed 278 computed tomographic scans from patients with rhinosinusitis symptoms to investigate anatomic variations that may predispose to sinusitis or impact on operative safety. The incidence of variants with potential impact on sinus drainage was compared between patients with and without sinus mucosal disease with logistic regression. Results: A closed osteomeatal complex was identified in 148 patients (53%), followed by concha bullosa in 98 patients (35%). Closed osteomeatal complex and nasal polyposis were independent risk factors for sinus mucosal disease. Anatomic variants with a potential impact on operative safety included anterior clinoid process pneumatization (18%), infraorbital ethmoid cell (12%), sphenomaxillary plate (11%), and supraorbital recess (6%). In 92% of patients, the level difference between the roof of the ethmoid cavity and the cribriform plate was Keros I. Conclusions: Bony anatomic variants do not increase the risk of sinus mucosal disease. However, anatomic variants with a potential impact on operative safety occur frequently and need to be specifically sought as part of preoperative evaluation. SOMAIRE Objectif: Étudier l anatomie radiologique des sinus paranasaux chez les patients avec et sans rhinosinusite chronique pour évaluer si ces variations anatomiques sont associées avec la pathologie et identifier les variantes qui peuvent avoir un impact sur la sécurité de l intervention. Localisation: Unité deréférence tertiaire en otorhinolaryngologie. Variables évaluées: Incidence et nature des variantes anatomiques avec un impact potentiel sur la sécurité opératoire et la présence ou l absence de maladie de la muqueuse sinusale et sa corrélation avec les variantes anatomiques avec un impact potentiel sur la clairance muco-ciliaire. Méthode: Nous avons revu les tomodensitométries de 278 patients avec des symptômes de rhinosinusite pour investiguer les variations anatomiques qui peuvent prédisposer à la sinusite ou avoir un effet sur la sécurité de l intervention. L incidence des variantes avec un impact potentiel sur le drainage des sinus a été comparée entre les patients avec et sans maladie de la muqueuse sinusale en utilisant la régression logistique. Résultats: Nous avons identifié un complexe ostio-méatal occlus chez 148 patients (53%), suivi par une concha bullosa chez 98 (35%). Un complexe ostio-méatal occlus et une polypose nasale étaient des facteurs de risque indépendants de maladie sinusale. Les S.A.R. Nouraei: Department of Otolaryngology, Charing Cross Hospital, London, United Kingdom; Ali R. Elisay, R. Abdi, and H. Majidi: Department of Radiology, University of Mazandaran, Sari, Iran; Aimee DiMarco: Department of Anatomy, King s College London, London, United Kingdom; S.A. Madani: Department of Otolaryngology, University of Mazandaran, Sari, Iran; P.J. Andrews: Royal National Throat, Nose and Ear Hospital, London, United Kingdom. Presented at the summer meeting of the British Association of Clinical Anatomists (winner of the Conrad Lewin Prize), Keele, UK, July Address reprint requests to: Reza Nouraei, MBBChir, Department of Otolaryngology, Charing Cross Hospital, London, W6 8RF, UK; RN@cantab.net. DOI / # 2009 The Canadian Society of Otolaryngology-Head & Neck Surgery 32 Journal of Otolaryngology-Head & Neck Surgery, Vol 38, No 1 (February), 2009: pp 32 37

2 Nouraei et al, Variations in Paranasal Sinus Anatomy 33 variantes anatomiques avec un impact potentiel sur la sécurité opératoire incluaient une pneumatisation du processus clinoide (18%), une cellule ethmoidale infra-orbitaire (12%), une lame sphénomaxillaire (11%) et un récessus supra-orbitaire (6%). Chez 92% des patients, la différence entre le toit des ethmoides et la lame criblée était de type Keros I. Conclusion: Des variantes anatomiques osseuses n augmentent pas le risque de maladie de la muqueuse sinusale. Des variantes cependant, avec un impact potentiel sur la sécurité opératoire sont fréquentes et devraient être recherchées spécifiquement dans l évaluation pré-opératoire. Key words: anatomy of paranasal sinuses, chronic rhinosinusitis, computed tomography T he purpose of endoscopic surgery for chronic rhinosinusitis is to restore physiologic mucociliary flow. The area most commonly affected by disease is the middle meatus, where maxillary, frontal, and anterior ethmoid sinuses drain. 1 3 This area of the lateral nasal wall is subject to significant anatomic variability, 2 4 which could potentially further narrow the middle meatal cleft and predispose the patient to sinusitis. Computed tomography (CT) is central to the modern management of chronic rhinosinusitis, owing to its ability to delineate mucosal disease, to demonstrate primary obstructive pathology, and to image distal structures such as the posterior ethmoid sinus, which cannot be viewed with direct endoscopy. 1,5 The ability to demonstrate the ethmoid sinus is critical as it has long been recognized that it provides the key to chronic infections of the maxillary and frontal sinuses. 1,5 10 Proctor described the ethmoid sinus as the primary site of infection and noted that failure to direct treatment appropriately resulted in failure of resolution of secondary maxillary or frontal sinus disease. 6,10,11 Another equally important aspect of performing endoscopic sinus surgery is the appreciation of anatomic variations that may impact operative safety. In close proximity to the paranasal sinuses lie vital structures like the skull base, optic nerves, internal carotid arteries, and the orbits. Certain anatomic variants increase the risk of injury to these structures, and a clear understanding of the individual patient s paranasal sinus anatomy through the study of paranasal sinus CT is therefore central to performing safe endoscopic sinus surgery. In this study, we reviewed the CT scans of patients with symptoms of rhinosinusitis to investigate the incidence of those anatomic variants, which could potentially impact on paranasal sinus drainage, correlating them with the presence or absence of radiologic evidence of sinus mucosal disease, as well as those variants with potential impact on operative safety. Materials and Methods We undertook a retrospective review of 300 coronal CT scans, taken at 2 mm thickness with a Siemens HiQ scanner (Siemens AG, Munich, Germany), from patients with symptoms suggestive of rhinosinusitis. The CT scans of 22 patients with a history of endoscopic sinus surgery were excluded from further analysis. All scans were reviewed by two consultant head and neck radiologists and an otolaryngologic surgeon. Information about individual anatomic variants, as well as nasal polyposis and the presence of sinus mucosal disease or pansinusitis, was recorded as binary variables. The configuration of the olfactory fossa was characterized based on the grading system proposed by Keros. 12 Descriptive statistics were used to document anatomic variants with a potential impact on sinusitis and operative safety. The chi-square test was used to assess the relationship between different anatomic variants and sinus mucosal disease, and binary logistic regression was used to identify independent risk factors for sinus mucosal disease. SPSS release 12.0 for Windows was used for statistical analysis (SPSS Inc, Chicago, IL). Results The average age at presentation was years. There were 172 males (62%) and 106 females. One hundred ninety-eight patients had radiologic evidence of sinus mucosal thickening, of whom 47 had pansinusitis. An airfluid level was seen only in 9 patients. The prevalence of anatomic variants with a potential impact on sinus drainage is provided in Table 1 and illustrated in Figure 1. Statistically significant risk factors (p,.05; chi-square test) for sinus mucosal disease on univariate analysis were concha bullosa, a closed osteomeatal complex, and nasal polyposis. Independent risk factors for sinus mucosal disease on multivariate analysis were a closed osteomeatal complex (relative risk 34; 95% confidence interval ) and nasal polyposis (relative risk 2.5; 95% confidence interval ). The prevalence of variations with a potential impact on operative safety is shown in Table 2 and illustrated in Figure 2. The most common anatomic variant with a potential impact on operative safety was a pneumatized

3 34 Journal of Otolaryngology-Head & Neck Surgery, Volume 38, Number 1, 2009 Table 1. Anatomic Variations with a Potential Impact on Sinus Drainage Anatomic Variation n (%) Middle turbinate Concha bullosa 98 (35.4) Paradoxical 2 (0.7) Congenital absence 1 (0.4) Uncinate process Pneumatized 4 (1.4) Absent 4 (1.4) Septum pneumatization 26 (9.4) Bulla ethmoidalis 8 (2.9) Table 2. Anatomic Variations with Potential Implications for Operative Safety Anatomic Variation n (%) Anterior clinoid process pneumatization 49 (17.6) Infraorbital ethmoid (Haller) cell 34 (12.2) Sphenomaxillary plate 31 (11.1) Supraorbital recess 17 (6.1) Sphenoethmoid (Onodi) cell 13 (4.7) Level difference between cribriform plate and ethmoid roof (olfactory fossa depth) Keros I 257 (92) Keros II 19 (7) Keros III 3 (1) anterior clinoid process, which was present in 49 subjects (17.6%), followed by infraorbital ethmoid (Haller) cells, which occurred in 34 patients (12%). With respect to the level difference between the ethmoid and cribriform plate, Keros grade I was by far the most common at 257 (92%), followed by grade II in 19 (7%) and grade III in 3 patients (0.4%) (Figure 3). Discussion The term concha bullosa was coined by Zuckerlandl in 1862 to describe pneumatization of the middle turbinate. The significance of this variant lies in the potential secondary deformity of the turbinate, which increases the likelihood of obstruction of the middle meatus and can lead to recurrent ethmoid sinusitis. Our findings of just over one- Figure 1. Anatomic findings potentially influencing paranasal sinus drainage. A, Closed osteomeatal complex and fovea ethmoidalis. B, Bilateral pneumatization of the uncinate process. Incidential finding of crista gali pneumatization. C, Pneumatization of the nasal septum. D, Bilateral concha bullosa and uncinate process pneumatization.

4 Nouraei et al, Variations in Paranasal Sinus Anatomy 35 Figure 2. Anatomic findings with potential implications for operative safety. A, Sphenomaxillary plate. B, Supraorbital recess. C, Onodi cell. D, Anterior clinoid process pneumatization. Figure 3. Level difference between the cribriform plate and ethmoid roof. Keros grades I (1 3 mm), II (4 7 mm), and III (8 16 mm).

5 36 Journal of Otolaryngology-Head & Neck Surgery, Volume 38, Number 1, 2009 third of cases having concha bullosa are in agreement with those of Arslan and colleagues and Calhoun and colleagues. 7,8 Our study shows that this anatomic variation is not associated on multivariate analysis with sinus mucosal disease, a finding that is consistent with previous reports. 13 The paradoxical curvature of the middle turbinate, that is, lateral instead of medial convexity, may also impact on drainage of the middle meatus. We found only two cases with a paradoxical curve. The rates in the previous publications on this subject are highly variable, with incidences of 3%, 7.9%, 26%, and even 40% having been reported. 5,7 9 The uncinate process is another important structure in relation to paranasal sinus drainage, given that, with the ethmoidal bulla, it defines the boundaries of the hiatus semilunaris, which is the outlet for the infundibulum recess. We found that the uncinate process was pneumatized in just over 1% of patients in the present study. The rate of uncinate process pneumatization in previous studies has been reported to be between 2 and 9%. 5,7,9 The only anatomic factor that was significantly associated on multivariate analysis with sinus mucosa disease was a closed osteomeatal complex, which was present in 52% of patients in this series, including almost all of the patients with pansinusitis. The most common anatomic variant with potential implications for operative safety in this series was pneumatization of the anterior clinoid process. This usually occurs from the most posterior ethmoid cells and can surround the optic nerve, which increases the risk of injury to the nerve during surgery. 14,15 Our finding of 17.6% anterior clinoid pneumatization is reasonably close to that of Bolger and colleagues at 13.3%, 9 but both are higher than the findings of Arslan and colleagues at 6%. 7 The next most common anatomic variant was the presence of infraorbital ethmoid cells, which are also known as Haller cells. These are found between the maxillary sinus and the orbit and can increase the risk of orbital injury during ethmoidectomy. 7 A variable incidence of infraorbital ethmoid cells in previous studies has been noted before and is thought to be due to inconsistencies in their definition between different authors. Zinreich and colleagues and Meloni and colleagues both reported rates of 10%, which is close to our incidence of 12.2%. 1,15 Arslan and colleagues reported an incidence of 6%, and Bolger and colleagues 45%. 7,9 Another anatomic variant that can potentially increase the risk of orbital damage during endoscopic sinus surgery is the presence of supraorbital cells, which are also known as fronto-orbital cells, supraorbital ethmoid cells, or supernumerary frontal sinus. These cells are important in both endoscopic sinus surgery and neurosurgical anterior cranial fossa approaches to the orbit, where breaching the wall of a supraorbital cell may jeopardize sterility. Our findings of an incidence of 6% correlate with those of Arslan and colleagues. 7 Two anatomic variants that increase the risk of inadvertent and unappreciated entry to the sphenoid sinuses, with subsequent risk of injury to the optic nerves or the carotid arteries, are sphenomaxillary plate and sphenoethmoid (Onodi) cells, which were present in 31 (11%) and 13 (4.7%) of the patients in our series, respectively. The sphenomaxillary plate is a thin-walled partition between the sphenoid and maxillary sinuses, which occurs when extensive pneumatization of the ethmomaxillary plate takes place. It is of significance because it may be mistaken for a posterior ethmoid cell during ethmoidectomy, increasing the risk of inadvertent entry into the sphenoid sinus. The incidence of sphenomaxillary plate in our series, which was 11%, is similar to the 13 to 14% incidence reported. 7,15 Sphenoethmoid cells were present in 4.7% of patients in our series. These cells lie immediately medial to the optic nerve and distort the anterior wall of the sphenoid sinus. When present, performing a sphenoidotomy by following ethmoid cells backward carries the risk of optic nerve damage. 7 The configuration of the cribriform plate in relation to the roof of the ethmoid sinus is of particular significance with respect to the risk of skull base injury and cerebrospinal fluid leak. The cribriform plate is generally lower than the ethmoid roof, which gives off lateral lamellae, creating the floor, walls, and upper limit of the olfactory fossa. The system divised by Keros describes the depth of the olfactory fossa. 12 In Keros grade I, there is a flat olfactory fossa (1 3 mm); in II (4 7 mm), the lateral lamella is higher, the fovea ethmoidalis has a steeper course, and the fossa is consequently deeper; and grade III (8 16 mm) has the deepest fossa and therefore presents the most operative risk as the lateral lamella is particularly long and thin. Our figures of 92%, 7%, and 1% for grades I, II, and III, respectively, are in accordance with those of previous publications. 7,15 Conclusion We have found that, with the exception of a closed osteomeatal complex, most of the anatomic variants that can be intuitively considered to narrow mucociliary drainage passages were not, in fact, independent risk factors for sinus mucosal disease. This observation is in keeping with previously published studies 13 and is congruent with an

6 Nouraei et al, Variations in Paranasal Sinus Anatomy 37 emerging consensus of opinion regarding the contribution of anatomic variation to the pathogenesis of paranasal sinus disease. The CT was very effective, however, in demonstrating the presence and extent of sinus mucosal disease and the sites of obstruction. Furthermore, we found marked differences in, and significant numbers of, anatomic variants with major implications for operative safety. It is therefore imperative that preoperative CT scans are obtained in all patients undergoing sinus surgery, and that a detailed study of the scans is undertaken with reference to the location and extent of the disease and the presence of specific anatomic variants with implications for operative safety, before endoscopic sinus surgery is undertaken. Acknowledgement We wish to express our warm thanks to Professor Harrold Ellis for his helpful suggestions and critical appraisal of the manuscript. References 1. Zinreich SJ, Kennedy DW, Rosenbaum AE, et al. Paranasal sinuses: CT imaging requirements for endoscopic surgery. Radiology 1987; 163: Messerklinger W. On the drainage of the normal frontal sinus of man. Acta Otolaryngol (Stockh) 1967;63: Messerklinger W. Endoscopy of the nose. Baltimore: Urban & Schwartzenberg; Mackay IS, Lund VJ. Surgical management of sinusitis. In: Scott- Brown s otolaryngology. Oxford: Butterworth-Heinemann; Earwaker J. Anatomic variants in sinonasal CT. Radiographics 1993;13: Stammberger H. Functional endoscopic sinus surgery. Philadelphia: BC Decker; Arslan H, Aydinhoglu A, Bozhurt M, Egeli E. Anatomic variations of the paranasal sinuses: CT examination for endoscopic sinus surgery. Auris Nasus Larynx 1999;26: Calhoun KH, Waggenspack GA, Simpson CB, et al. CT evaluation of the paranasal sinuses in symptomatic and asymptomatic populations. Otolaryngol Head Neck Surg 1991;104: Bolger WE, Butzins CA, Parsons DS. Paranasal sinus bony anatomic variations and mucosal abnormalities: CT analysis for endoscopic sinus surgery. Laryngoscope 1991;101: Proctor DF. The nose, paranasal sinuses and pharynx. In: Walters W, editor. Lewis-Walters practice of surgery. Hagerstown, MD, USA: Prior; p Proctor D. Disease and the upper respiratory tract. Bacteriol Rev 1966;30: Keros P. Uber die praktische Bedeutung der Niveauunterschiede der Lamina cribrosa des Ethmoids. Laryngol Rhinol Otol (Stuttg) 1965;41: Stallman JS, Lobo JN, Som PM. The incidence of concha bullosa and its relationship to nasal septal deviation and paranasal sinus disease. AJNR Am J Neuroradiol 2004;25: Gean AD, Pile-Spellman J, Heros RC. A pneumatized anterior clinoid mimicking an aneurysm on MR imaging. Report of two cases. J Neurosurg 1989;71: Meloni F, Mini R, Rovasio S, et al. Anatomic variations of surgical importance in ethmoid labyrinth and sphenoid sinus. A study of radiological anatomy. Surg Radiol Anat 1992;14:65 70.