The Variations in Anatomy of the Sphenoid Sinus and Sellar Floor to Perform Transsphenoidal Endoscopy in Adult

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The variations in anatomy of the sphenoid sinus and sellar floor to perform transsphenoidal endoscopy in adult age: a literature review As variações na anatomia do seio esfenoidal e assoalho selar para realização de endoscopia transesfenoidal em adultos : revisão de literatura Alicia Del Carmen Becerra Romero1,2 Garni Barkhoudarian1 Carlos Eduardo da Silva2 Paulo Henrique Pires de Aguiar3 Edward R Laws Jr1

RESUMO ABSTRACT A cirurgia transesfenoidal depende da habilidade de visualizar Transsphenoidal surgery depends on the ability to visualize e identificar referências anatômicas chaves durante cada fase and identify key anatomical landmarks during each phase of da operação. Um grau notável de variação anatômica existe the operation. A remarkable degree of anatomical variation no seio esfenoidal, sela túrcica e estruturas ao redor da base exists in the sphenoid sinus, sella turcica, and surrounding do crânio. Nosso objetivo é revisar as variações anatômicas skull base structures. Our purpose is to review the anatomical no seio esfenoidal e assoalho selar que são importantes variations in sphenoid sinus and sellar floor that are important para realizar uma cirurgia endoscópica transesfenoidal de to performing safe and effective transsphenoidal endoscopic modo efetivo e seguro em pacientes adultos. Uma detalhada surgery in adult patients. Detailed information regarding the informação em relação a anatomia é o meio mais confiável e anatomy is the most reliable and effective way of avoiding efetivo de evitar complicações de todos os tipos na cirurgia complications of all kinds in transsphenoidal surgery. transesfenoidal. Key words: anatomy, endoscopy, transsphenoidal surgery. Palavras-chave: anatomia, cirurgia transesfenoidal, endoscopia.

1 - Department of Neurosurgery, Brigham and Women’s Hospital, Harvard Medical School - Boston / Massachusetts / USA. 2 - Departamento de Neurocirurgia, Hospital Ernesto Dornelles - Porto Alegre / RS / Brazil. 3 - Curso Pós-Graduação em Cirurgia, Universidade Federal do Rio Grande do Sul - Porto Alegre / RS / Brazil.

Recebido em 08 de dezembro de 2011, aceito em 27 de dezembro de 2011 Romero ADCB, Barkhoudarian G, Silva CE, Aguiar PHP, Jr ERL - The variations in anatomy of the sphenoid sinus and sellar floor to perform transsphenoidal J Bras Neurocirurg 23 (1): 11-17, 2012 endoscopy in adult age: a literature review 12

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safe and effective transsphenoidal endoscopic surgery in adult Introduction patients. The posterior wall of the nasal cavity is formed by the sphenoethmoidal recess, which includes the sphenoid ostia.3 Transsphenoidal surgery depends on the ability to visualize Sheti et al identified the sphenoid ostia subtypes as round and identify key anatomical landmarks during each phase of (47%), elliptical (40%), and “pinhead” (13%), with the the operation.12 A remarkable degree of anatomical variation majority measuring less than 2.7 mm in diameter.17 In elderly exists in the sphenoid sinus, sella turcica, and surrounding patients, the sphenoid ostia may be quite wide.3 skull base structures.14 The direct endoscopic endonasal The sella lies along the posterior and superior walls of the approach because of its minimally invasive characteristics, is sphenoid sinus, which separates the pituitary gland from progressively gaining popularity. The application of endoscopy the nasal cavity.12 Hamberger et al5 in 1961 characterized 3 to pituitary surgery is based on multiple advantages, including anatomical variations of the sphenoid sinus: sellar, presellar, improved visualization,6 preservation of sinonasal function, and conchal, that are still employed today. The sphenoid sinus reduced length of stay, increased patient comfort, and reduced is extremely variable with respect to size, shape and relation serious complications.19 Despite this advance, complications of to the sella.9 The degree of pneumatization of the sphenoid endoscopic surgery can occur, and can be traced to a number bone is an important factor in the endoscopic approach.3 of causes, including the anatomy surrounding the operative Several studies have reported findings regarding the various approach.4 Our purpose is to review the anatomical variations in proportions1,5-7,13,14,17 (Table 1): sphenoid sinus and sellar floor that are important to performing

Table 1. Finding of sphenoid sinus anatomy in different studies from 1961 to 2011

n Type of study Presellar % Sellar % Conchal % Single Septum % No Septum % Hamberger et 163 - 11 86 3 - - al5 1961

Renn and 50 Anatomic 20 80 0 68 28 Rhoton14 1975

Banna and 70 Anatomic 11.4 85.7 2.8 61 11.4 Olutola1 1983

Ouaknine and 266 Surgery report 12 85 3 - - Hardy13 1987

Ouaknine and 100 Anatomic - - - 75 25 Hardy13 1987

Sethi et al17 30 Anatomic 27 73 0 - - 1995

Hamid et al6 296 MRI/CT 21 77 2 71.6 10.8 2007 pituitary adenomas

Zada et al21 178 MRI - - - 52.7 9 2011 healthy sellar lesions

MRI: Magnetic Resonance Imaging. CT: Computerized Tomography. - : No data.

Romero ADCB, Barkhoudarian G, Silva CE, Aguiar PHP, Jr ERL - The variations in anatomy of the sphenoid sinus and sellar floor to perform transsphenoidal J Bras Neurocirurg 23 (1): 11-17, 2012 endoscopy in adult age: a literature review 13

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1. The sellar sinus (73-86%) is well pneumatized with bulging The conchal type is common in children before the age of the sellar floor into the sinus. of 12 years, after which pneumatization begins within the sphenoid sinus.17 As age advances, the sphenoid sinus 2. The presellar sinus (11-27%) is situated in the anterior frequently undergoes further enlargement associated with bone sphenoid bone and does not penetrate beyond the perpendicular 1 plate of the tuberculum sellae (Fig. 1a). resorption. 3. The conchal sinus (0-3%) does not reach into the body of the There is typically only one sphenoid sinus septation in the sphenoid bone, and its anterior wall is separated from the sella majority of cases (Table 1). According to Cappabianca et al, turcica by approximately 10 mm of cancellous bone (Fig. 1b). in 20% of cases the posterior attachment of a lateral sphenoid septum extends to the carotid protuberance (Fig. 2a, 2b).3 Sethi et al found that in 40% of patients the septum deviates laterally and terminates on the internal carotid artery (ICA) protuberance.17 In contrast, Zada et al found that in 79% of healthy patients the vertical septum deviates towards one or the other ICA.21 Oauknine and Hardy described the bony septum as rarely being median in location.13 Sirikci et al affirmed that a deviated nasal septum or a thickened or pneumatized vomer, are the most frequent abnormalities encountered in sphenoid septum variations.18

B B

Figure 1. Sagittal MRIs demonstrating presellar (a) and conchal (b) subtypes, with relationship of the sphenoid sinus to the sella. Figure 2. Coronal MRI (a) and endoscopic view (b) of sphenoid sinus septations.

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Two bulges on the lateral wall of the sphenoid sinus are of considerable clinical significance. They are produced by the optic nerve and the ICA.9 The optic canal bulges into the anterior superior part of the sphenoid sinus.14 The ICA bulges into the superolateral wall of the posterior part of the sinus in 71-93%.13,14,17 Depending on the degree of pneumatization, these two bulges may be barely noticeable or quite prominent.9 Lateral to their junction is the lateral optico-carotid recess. This corresponds to the optic strut connecting to the anterior clinoid process. The medial optico-carotid recess correlates to the partially calcified clinoidal dural ring around the carotid artery. The bone over the ICA and/or optic nerve bones may be dehiscent in approximately 4% of cases.14 The measurements between the ICAs in different studies range from 4 to 23 mm, as determined in the sphenoid sinus, cavernous sinus or supraclinoid area.6,14,21 Sphenoethmoidal cells (or large Onodi cells) are anatomical B variations that pneumatize lateral and to some degree superior 8 to the sphenoid sinus (Fig. 3a, 3b). They are identified in Figure 3. Coronal (a) and sagittal (b) MRI of an Onodi cell. 3-14% of cases8,11,17,21 and can be mistakenly identified as part Van Lindert et al reported a series of 185 patients who had 20 of the sphenoid sinus. endoscopic endonasal transsphenoidal surgery to the pituitary through a binostril approach and found 89 (48.1%) with anatomical variations.20 The most common were spinae septi and septal deviation. The other anatomical variations were concha bullosa, synechia, extremely narrow pathway, absent chondroid septum, pansinusitis, hypercongestive mucosa and polyps.20 In 5% of patients, the binostril approach was converted to a mononostril approach because of severe nasal septal deviation; whereas in 18% of patients with an anatomical variation, a correction had to be made in order to allow satisfactory entrance into the sphenoid sinus. Complications related to the endonasal phase occurred in 3.8% and the majority were postoperative epistaxis.20 Bolger et al2 reported paranasal sinus bony anatomic variations and mucosal abnormalities assessed by coronal computerized tomography (CT) in 202 patients and found these problems in 64.9% and 83.2%, respectively. This study excluded patients with previous surgical alterations of the paranasal sinus anatomy. A deviated nasal septum in this report was detected in 18.8%.2 However, the literature reveals a lack of consensus among investigators with respect to the prevalence of the different anomalies in anatomical structures.2 This may be due to factors such as inherent differences in study populations and sensitivity of the method of analysis. The definition of mucosal abnormalities ranged from minimal mucosal thickening to total sinus opacification. Abnormality in the sphenoid sinus mucosa A was found in 22.3% in this report.2

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Another anatomical landmark that Hamid et al6 considered to soft tissue of the nasal cavity, and enlarged, hypertrophic bony be one of the most important to the transsphenoidal approach nasal turbinates, both of which can compromise the endoscopic is the prominent sella (Table 2). Zada et al found that patients view and working space. When nasal polyps were encountered, with intrasellar lesions were more likely to have a prominent they were coagulated and removed to improve visualization. sella turcica (43%) than were healthy adults.21 Another Due to the size and rigidity of the nasal turbinates, they often finding of this study shows that intrasellar lesions were require more lateral displacement than in other patients; this noted to have a wider sphenoid sinus, wider sellar face, and can result in increased bleeding if the mucosa is injured. wider separation between the parasellar ICAs (19 mm) when compared to healthy controls.21 Many authors emphasize that the most reliable intraoperative midline markers are the vomer, superior sphenoid rostrum, and bilateral parasellar and clival carotid protuberances.13,21 Its midline location makes vomer an essential landmark in the transsphenoidal approach to the sella.13 In case of large tumors that destroy the sellar floor, invade the cavernous sinus, and occlude the sphenoid sinus the usual anatomical landmarks are absent or poorly demarcated.

Table 2. Findings of sellar configuration anatomy in different studies.

n Type of study Sellar configuration % Ouaknine and 266 Surgery report 94.7 regular/ Hardy13 1987 symmetrical 5.3 asymmetrical/ oblique Hamid et al6 296 MRI/CT 75 prominent 2007 pituitary adenomas Zada et al21 100 MRI 25 prominent A 2011 healthy 63 curved 11 flat 1 no floor Zada et al21 78 MRI 43 prominent 2011 sellar lesions 47 curved 10 flat MRI: Magnetic Resonance Imaging. CT: Computerized Tomography.

In acromegaly, specific anatomical variations are seen (Fig. 4a, 4b & 5a, 5b). They include soft-tissue edema, nasal polyps, and bony remodeling. These often contribute to the complexity of the operation, as natural working corridors are typically more constricted and deeper than in other patients.10,15 Zada et al22 reported 169 endoscopically operated acromegalic patients and found ICA injury in 1 patient (0.6%), postoperative delayed epistaxis (arterial bleeding) in 5 patients (3%), and transient diabetes insipidus in 5 patients (3%). Four patients had delayed hyponatremia secondary to the syndrome of inappropriate antidiuretic hormone hypersecretion (2%), 2 (1%) developed postoperative cerebrospinal fluid leaks, and 2 patients (1%) underwent conversion to a microscopic approach. B Intraoperatively they divided transsphenoidal surgery into nasal, sphenoid and sellar phases. In the nasal phase, the primary Figure 4. Sagittal MRIs comparing normal sphenoid sinus (a) to changes produced challenges are typically related to edematous and/or redundant by a GH secreting pituitary macroadenoma (b).

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In the sphenoid phase the challenges are: atypical bony anatomy (chronic bony remodeling) accomplishing adequate exposure within the sinus, and maintenance of hemostasis. Thickened sphenoid sinus mucosa is often found and once stripped can cause venous bleeding from the sinus walls.10 In the sellar phase, patients with acromegaly have been reported to develop anatomical changes in the caliber, location and tortuosity of the ICA (narrow intercarotid distance) that comes into play during the sphenoid and sellar phases of the surgery.15 Saeki et al emphasize that acromegalic patients may have marked carotid prominences.15 In the sellar phase, a complex bony sellar floor may also be present. In addition to the macroscopic anatomical changes, microvascular changes related to chronic Growth Hormone elevation can be seen. These include alterations in the structural integrity of surrounding structures like the cavernous sinus dura and the ICA with deterioration of vessel endothelium causing parasellar and intrasellar ICA aneurysm formation.16 The risk of ICA A injury is more common in acromegalic patients as a result of the anatomical and microvascular changes mentioned.22 What are the most challenging anatomic variations for transphenoidal endoscopy? Zada et al concluded that the flat sellar type and complex sphenoid sinus configuration may make intraoperative correlation substantially more challenging, and are a prime argument for the use on image guidance during surgery.21 Renn and Rhoton studied 50 adult brain specimens and considered the following anatomical variations in the sphenoid and sellar floor disadvantageous for transsphenoidal approach: carotid arteries exposed in the sphenoid sinus with little or no bone over them; optic canals with bone defects in the sphenoid sinus; thick sellar floor; sphenoid sinus with no major septum or a septum that is off midline; and the presellar type with no obvious bulge of the sellar floor.14 In summary anatomic abnormalities may be frequently encountered during routine surgery. Detailed information regarding the anatomy is the most reliable and effective way of avoiding all kinds of complications in transsphenoidal surgery.

eferences Figure 5. Coronal MRIs comparing normal nasal anatomy (a) to hypertrophy of R bone and mucosa characteristic of acromegaly (b). Localization of the sphenoid ostia is found about 1.5 cm above the superior aspect of the choanae may be more difficult, 1. Banna M, Olutola PS. Patterns of pneumatization and septation of as the sphenoid ostia are often hidden by redundant tissue. the sphenoidal sinus. J Can Assoc Radiol. 1983; 34(4):291-3. The intranasal working space is narrow and restricted, and therefore the mobility and range of endoscopic instruments 2. Bolger WE, Butzin CA, Parsons DS. Paranasal sinus bony may be limited, resulting in conflict of the instruments. anatomic variations and mucosal abnormalities: CT analysis for Delayed epistaxis in this series occurred in 3%, due to the endoscopic sinus surgery. Laryngoscope. 1991; 101:56-64. sphenopalatine artery.

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3. Cappabianca P, Cavallo LM, Esposito F, Stagno V, De Notaris MG. 19. Tabaee A, Anand VK, Barrón Y, Hiltzik DH, Brown SM, Kacker Endoscopic transphenoidal surgery: anatomy, instrumentation, A et al. Endoscopic pituitary surgery: a systematic review and techniques. In: Laws Jr ER, Lanzino G, editors. Transphenoidal meta-analysis. J Neurosurg. 2009; 111:545-54. surgery. Philadelphia: Elsevier Saunders; 2010. p. 128-42. 20. Van Lindert EJ, Ingels K, Mylanus E, Grotenhuis JA. Variations 4. Ciric I, Ragin A, Baumgartner C, Pierce D. Complications of of endonasal anatomy: relevance for endoscopic endonasal transphenoidal surgery: results of a national survey, review of transphenoidal approach. Acta Neurochir. 2010; 152:1015-20. the literature, and personal experience. Neurosurgery. 1997; 40(2):225-37. 21. Zada G, Agarwalla PK, Mukundan Jr S, Dunn I, Golby AJ, Laws Jr ER. The neurosurgical anatomy of the sphenoid sinus and sellar 5. Hamberger CA, Hammer G, Marcusson G. Experiences in floor in endoscopic transphenoidal surgery. J Neurosurg. 2011; transantrosphenoidal hypophysectomy. Trans Pac Coast 114:1319-30. Otoophthalmol Soc Ann Meet. 1961; 42:273-86. 22. Zada G, Cavallo LM, Esposito F, Fernandez-Jimenez JC, Tasiou 6. Hamid O, Fiky LE, Hassan O, Kotb A, Fiky SE. Anatomic A, De Angelis M et al. Transsphenoidal surgery in patients with variations of the sphenoid sinus and their impact on trans-sphenoid acromegaly: operative strategies for overcoming technically pituitary surgery. Skull Base. 2008; 18:9-15. challenging anatomical variations. Neurosurg Focus. 2010; 29(4):E8. 7. Jane Jr JA, Laws Jr ER. The surgical management of pituitary adenomas in a series of 3,093 patients. J Am Coll Surg. 2001; 193(6):651-9. 8. Kantarci M, Karasen RM, Alper F, Onbas O, Okur A, Karaman orresponding uthor A. Remarkable anatomic variations in paranasal sinus region and C A their clinical importance. Eur J Radiol. 2004; 50:296-302. Alicia del Carmen Becerra Romero,M.D., Ph.D. 9. Laws Jr ER, Jane Jr JA, Jagannathan J, Katznelson L. Presentation Av.Pirapó,250/201, Porto Alegre, Brazil and clinical features of tumors of the pituitary and sellar region. CEP 90470-450 In: Mehta MP, editor. Principles and pratice of neuro-oncology: [email protected] a multidisciplinary approach. New York: Demos Medical Publishing; 2010. p. 291-6. 10. Laws Jr ER, Piepgras DG, Randall RV, Abboud CF. Neurosurgical management of acromegaly. Results in 82 patients treated between 1972 and 1977. J Neurosurg. 1979; 50:454-61. 11. Leunig A, Betz CS, Sommer B, Sommer F. Anatomic variations of the sinuses; multiplanar CT-analysis in 641 patients. Laryngorhinootologie. 2008; 87(7):482-9. 12. Oskouian RJ, Kelly DF, Laws Jr ER. Vascular injury and transphenoidal surgery. In: Laws Jr ER, Sheehan JP, editors. Pituitary surgery- a modern approach. Basel: Karger; 2006. p. 256-78. 13. Ouaknine GE, Hardy J. Microsurgical anatomy of the pituitary gland and the sellar region. 2. The bony structures. Am Surg. 1987; 53(5):291-7. 14. Renn WH, Rhoton Jr AL. Microsurgical anatomy of the sellar region. J Neurosurg. 1975; 43:288-98. 15. Saeki N, Iuchi T, Higuchi Y, Uchino Y, Murai H, Isono S et al. Bone CT evaluation of nasal cavity of acromegalics - its morphological and surgical implication in comparison to non-acromegalics. Endocrinol J. 2000; 47:S65-S68. 16. Seda JR L, Cukiert A, Nogueira KC, Huayllas MKP, Liberman B. Intrasellar internal carotid aneurysm coexisting with GH-secreting pituitary adenoma in an acromegalic patient. Arq Neuropsiquiatr. 2008; 66(1):99-100. 17. Sethi DS, Stanley RE, Pillay PK. Endoscopic anatomy of the sphenoid sinus and sella turcica. J Laryngol Otol. 1995; 109:951-5. 18. Sirikci A, Bayazit YA, Bayram M, Mumbuc S, Gungor K, Kanlikama M. Variations of sphenoid and related structures. Eur Radiol. 2000; 10:844-8.