Handbook of Clinical Neurology, Vol. 124 (3rd series) Clinical Neuroendocrinology E. Fliers, M. Korbonits, and J.A. Romijn, Editors © 2014 Elsevier B.V. All rights reserved

Chapter 19

Surgical approach to pituitary tumors DOMENICO SOLARI, LUIGI MARIA CAVALLO, AND PAOLO CAPPABIANCA* Department of Neurological Sciences, Division of Neurosurgery, Universit¼ degli Studi di Napoli Federico II, Naples, Italy

INTRODUCTION Pituitary surgery is a continuously evolving specialty of neurosurgery that requires precise anatomic knowledge, technical skills, and an integrated appreciation of pituitary pathophysiology. Thus, it cannot be considered to be solely a surgical procedure, but rather the result of a close cooperation between different specialists, i.e., the endocrinologist, neurosurgeon, neuroradiologist, pathologist, ophthalmologist, and others. In this teamwork environment each member plays a well-defined role, offering a contribution to the final result, specifically tailored to single patients. It is currently possible to manage many of the different pituitary syndromes with more than one option, including medical, surgical, and radiotherapeutic options, either alone or in various combinations. Pituitary surgery, perhaps more than other area of neurosurgery, requires careful and specific postoperative management and long-term patient follow-up; these can make the difference between a satisfactory result and a poor one. A patient may be operated on successfully, but the outcome may not be as brilliant as the surgical procedure promises if there is no mutual exchange among the members of the team or if their work is not implemented: each participant contributes to the final outcome for the patient while promoting growth of the other components, which calls for further work and better allocation of competencies and effectiveness: A virtuous circle develops. It is in such a context that pituitary surgery should exist today, where the neurosurgeon dealing with techniques, indications, and results is playing a refined role as a member of an expert team: he or she should know detailed anatomy, be experienced in neuroimaging, know pathophysiology and the natural history of pituitary disease, and be familiar with all the different therapeutic options (McLaughlin et al., 2012). The

neurosurgeon plays a crucial role, fully informed about current therapeutic possibilities in the interest of the patient and of the institution where the operation is done.

HISTORICAL BACKGROUND The first operation on a pituitary tumor was performed by Horsley in 1889; in 1906 he published the results obtained on a series of 10 patients first by means of a frontal craniotomy and later using a temporal approach (Handelsmann and Horsley, 1911). The first surgeon reporting on an operation specifically for a pituitary tumor was a British general surgeon, Paul, who, in 1893, performed a temporal decompression in an acromegalic patient without actually reaching the tumor (Caton, 1893). The next milestone was the first transsphenoidal approach, performed by the Viennese surgeon Schloffer in 1907 (Schloffer, 1907), based on the anatomic studies of the Italian physician Giordano (Giordano, 1911; Artico et al., 1998), chief surgeon of the hospital in Venice. The first totally endonasal procedure without complete dislocation of the nose was achieved in 1910 by Hirsch, a Viennese rhinologist, who was the first to incorporate a nasal speculum (Hirsch, 1910). Cushing performed his first transsphenoidal procedure in 1909 (Cushing, 1909, 1981), a classic sublabial, transseptal, transsphenoidal approach combining the evolution of his own technique and aspects of the different methods reported so far. He abandoned this procedure because of difficulties in achieving hemostasis and completeness of tumor removal in large suprasellar tumors, as compared to the transcranial procedure (Cushing, 1932; Rosegay, 1981; Lanzino and Laws, 2001). In 1918 the American neurosurgeon Dandy offered his view that “the nasal route is impractical and can never be otherwise”,

*Correspondence to: Paolo Cappabianca, MD, Division of Neurosurgery, Department of Neurological Sciences, Universita` degli Studi di Napoli Federico II, via S. Pansini 5, 80131, Naples, Italy. Tel: þ39-081-7462559, Fax: þ39-081-19560905, E-mail: paolo. [email protected]

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presenting his experience of 20 cases operated on by an intracranial intradural approach to the chiasm, according to a frontotemporal route to the pituitary (Dandy, 1934). The two main transcranial options, i.e., the subfrontal and the frontotemporal, are still used today together with more recent skull base approaches. The only pupil of Cushing who did not abandon the transsphenoidal method was Dott, a neurosurgeon at the Royal Infirmary of Edinburgh (Lanzino and Laws, 2001; Liu et al., 2001); he kept the procedure alive, improving the technique, and taught the method to the French neurosurgeon Guiot during the latter’s visit to the Royal Infirmary in 1956. Guiot at the Hoˆpital Foch in Paris, and his trainee Hardy in Montreal, deserve the credit for the “transsphenoidal renaissance” in the 1960s (Kanter et al., 2005). Modern transsphenoidal surgery takes advantage of the innovations of intraoperative image intensification and fluoroscopy, introduced by Guiot, and of the operating microscope as used by Hardy (1969, 1971), who introduced the concept of microadenoma and selective microsurgical resection. It was Gerard Guiot (Guiot et al., 1963; Guiot, 1973; Lanzino and Laws, 2001; Liu et al., 2001; Cappabianca et al., 2003; Kanter et al., 2005) who first proposed the use of the endoscope during a classic transsphenoidal transnasorhinoseptal approach in order to explore the sellar contents. Nevertheless, it was not until the 1990s that, embracing the experience of otorhinolaryngologists in functional endoscopic sinus surgery (FESS) (Kennedy, 1985; Stammberger and Posawetz, 1990; Jankowski et al., 1992), the “pure” endoscopic endonasal approach to the sellar area, with the endoscope as the sole visualizing tool during the whole procedure, was defined by the Pittsburgh duo of an otorhinolaryngologist and a neurosurgeon, namely Carrau and Jho (Carrau et al., 1996; Jho et al., 1996a); they were followed by our group in Naples (Cappabianca et al., 1998; de Divitiis et al., 2003; Cappabianca et al., 2004).

SURGERY Pituitary surgery performed by means of a transsphenoidal or transcranial approach has been developing through advances in medical science and technological progress; the surgical procedure for the removal of pituitary adenomas is, however, targeted at achieving multiple goals (Laws, 1993b; Laws and Lanzino, 2010): 1. 2. 3. 4.

Normalization of excess hormone secretion Preservation or restoration of normal pituitary function Relief of mass effect Preservation or restoration of normal neurologic function, usually visual acuity or visual field (or both)

5. 6. 7.

Prevention of tumor recurrence Achievement of a complete histologic diagnosis Obtaining tissue for scientific studies.

It should be remembered that biologically, endocrinologically, and pathologically, pituitary tumors represent a heterogeneous group of lesions, so that the role of surgery will be different for different pituitary tumor subtypes. Indications for surgery have changed through time, due to the refinement of surgical techniques and the evaluation of results and experiences, the development of knowledge about the molecular biology of diseases, and the use of effective new pharmacologic agents and radiation techniques (Cappabianca et al., 2010). Nonetheless, the primary role of surgery has been established (Laws and Ebersold, 1982; Cardoso and Peterson, 1984; Bevan et al., 1992; Bills et al., 1993; Davis et al., 1993; Brisman et al., 1996; Fahlbusch et al., 1996; Colao et al., 1997, 2003; Abosch et al., 1998; Swearingen et al., 1998; Shomali and Katznelson, 1999; Jane et al., 2001; Lohmann et al., 2001; Simmons et al., 2001; Chen et al., 2003; Casanueva et al., 2006; Esposito et al., 2006; Losa et al., 2006) for the following: ● ● ●

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Nonfunctioning pituitary tumors Pituitary apoplexy Progressive mass effect, producing compression of the surrounding neurovascular structures, regardless hormonal status Cushing’s disease, because of the present inadequacy of pharmacologic agents Acromegaly, in combination with medical treatment (preoperatively and postoperatively, if necessary) Secondary hyperthyroidism.

The role of surgery in prolactinoma is secondary (Molitch et al., 1985; Bevan et al., 1992; Colao et al., 2003), but still necessary in selected conditions. Indications for surgery also include: ● ●

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Failure of, or resistance to, medical treatment; intolerable side-effects of medical therapy Complications of medical therapy such as cerebrospinal fluid (CSF) leakage due to tumor shrinkage, or apoplexy (e.g., in prolonged and massive cabergoline treatment) Recurrences, in combination or in association with the other therapeutic options, medical and/or radiotherapeutic Patient choice.

The surgical approach, with respect to the basic principles for resecting pituitary adenomas, can be performed via two main routes, each of them amenable to several different approaches:

SURGICAL APPROACH TO PITUITARY TUMORS 1.

Transsphenoidal a. microsurgical (i) transnasal (ii) sublabial (iii) endonasal b. endoscopic. 2. Transcranial a. subfrontal unilateral b. frontolateral or pterional c. subfrontal bilateral interhemispheric. In recent decades, this field of surgery has been taking advantage of evolving ideas and surgical tools in the attempt to attain the lowest possible rates of morbidity and mortality in a safe, feasible, and practical way. The transsphenoidal midline route, however, has become the standard approach to the pituitary area, being the less traumatic, direct route to the sella, avoiding brain retraction, and providing excellent visualization of the pituitary gland and adjacent pathology, with a lower morbidity and mortality rate as compared with transcranial procedures (Perneczky et al., 1999; Leonhard et al., 2003; Cappabianca and de Divitiis, 2004; Doglietto et al., 2005; Kanter et al., 2005). Transsphenoidal surgery today is used in over 95% of surgical procedures to the sellar area and in about 97% of all surgery for the treatment of pituitary adenomas. Absolute indications were established about 30 years ago and are still valid today:

● ● ● ● ● ● ● ● ●

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elevated surgical risk of the transcranial route in the elderly in longstanding compression of the chiasm in case of acute endosellar hypertension in most cases of pituitary apoplexy in paninvasive not radically removable adenomas in cases of adenoma with downward development in cases of microadenoma in non-neoplastic intrasellar cysts (Baskin and Wilson, 1984; Ross et al., 1992; el-Mahdy and Powell, 1998; Cavallo et al., 2008) in craniopharyngiomas, especially cystic, extraarachnoidal, and infradiaphragmatic (Guiot and Derome, 1972), with an enlarged sella (Laws, 1980; Abe and Ludecke, 1999).

To these classic guidelines for the transsphenoidal option, in more recent decades (Zada and Cappabianca, 2010) the following can be added: ●

The extended transplanum-transtuberculum approach (Weiss, 1987; Kelley et al., 1996; Kato et al., 1998; Kim et al., 2000; Kouri et al., 2000; Maira et al., 2004; Laws et al., 2005; Locatelli et al., 2006; Castelnuovo et al., 2007; Kitano and Taneda, 2009), for the removal of suprasellar craniopharyngiomas,

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Rathke’s cleft cysts, some tuberculum sellae meningiomas, and anterior cranial base CSF leaks; the extended approach to the clival area and to the parasellar compartment for invasive adenomas (Fraioli et al., 1995; Alfieri and Jho, 2001; Kitano et al., 2008; Dallan et al., 2011; Di Maio et al., 2011) and chordomas (Hardy and Vezina, 1976; Laws, 1993a; Jho et al., 1996b; Maira et al., 1996; Jho et al., 1997; Jho and Ha, 2004; Stippler et al., 2009; Fraser et al., 2010; Komotar et al., 2011). A multistaged transsphenoidal approach, for the removal of intrasuprasellar adenomas, as an intentionally two-stage transsphenoidal operation, in order to favor the descent of a suprasellar remnant of the adenoma and limit the risks of a brisk decompression of huge lesions (Saito et al., 1995).

Nevertheless, there are conditions that limit and sometimes contraindicate the choice of the transsphenoidal approach in favor of the transcranial, either related to the anatomy of the surgical route or to the inner features of the lesion itself (Zada et al., 2011). The size of the sella, its degree of ossification, the size and the pneumatization of the sphenoid sinus and/or carotid arteries, position and shape can increase the difficulty of the transsphenoidal procedure. Indications for transcranial surgery include the following (Wilson, 1990; Yasargil, 1996; Thapar and Laws, 2001; Powell and Pollock, 2003): ●

● ●

Tumors with extensive intracranial invasion, with asymmetric lateral development, into the anterior cranial fossa or lateral or posterior extension into the middle and posterior cranial fossa, particularly if major vessel involvement is present Suprasellar tumors not completely resectable through the transsphenoidal route Recurrent or residual pituitary tumors in patients who have already had unsuccessful transsphenoidal surgery.

TRANSSPHENOIDAL APPROACHES The transsphenoidal approach represents a minimally traumatic corridor of surgical access to the sella, providing direct and superior visualization of the pituitary gland and adjacent pathology (Laws, 1993b; Perneczky et al., 1999; Elias and Laws, 2000; Leonhard et al., 2003; Cappabianca and de Divitiis, 2004; Doglietto et al., 2005; Kanter et al., 2005). It has been performed since the 1960s by means of the operating microscope, through transnasal transseptal, sublabial transseptal, or endonasal procedures (microsurgical transsphenoidal procedures) (Kanter et al., 2005). Recently, the endoscope has been introduced in transsphenoidal surgery

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as the sole visualizing tool during the entire surgical procedure, defining the “pure” endoscopic endonasal transsphenoidal approach (Doglietto et al., 2005). The combined use of the microscope and the endoscope during the same approach defines the procedure of endoscope-assisted microsurgery.

Microsurgical transsphenoidal approaches There are three basic microsurgical transsphenoidal approaches to pituitary tumors: (1) the transnasal transseptal transsphenoidal approach, (2) the sublabial transseptal transsphenoidal approach, and (3) the endonasal transsphenoidal approach, performed with an operating microscope for visualization, illumination, and magnification of the surgical field.

MICROSURGICAL TRANSNASAL TRANSSEPTAL TRANSSPHENOIDAL APPROACH

In the right nostril, the columella is retracted to expose the anterior edge of the septal cartilage; the cartilaginous septum is then dissected and freed from the bony septum. Posterior submucosal tunnels are created along both sides of the bony septum, which is partially removed to facilitate the introduction of a self-retaining transsphenoidal retractor. Care must be taken to avoid mucosal perforation during these maneuvers.

MICROSURGICAL SUBLABIAL TRANSSEPTAL TRANSSPHENOIDAL APPROACH

The upper lip is retracted, and an incision is made along the buccogingival junction, between the two canine fossae; the upper lip and the periosteum are elevated to expose the anterior nasal spine and the inferior border of the pyriform aperture of the nasal cavities. The mucosa of the floor of the nose is elevated first on both sides; the inferior and posterior portion of the cartilaginous septum is dissected from the bony nasal septum and is deflected laterally. The self-retaining nasal speculum is introduced and widely opened; indeed, a more anterior trajectory is provided as compared to the transnasal option.

MICROSURGICAL ENDONASAL TRANSSPHENOIDAL APPROACH

A hand-held speculum is inserted into the nostril along the middle turbinate, and a vertical mucosal incision is performed at the junction of the keel of the sphenoid bone and the posterior nasal septum; the septum, with its intact mucosa, is pushed off the midline by the medial blade of the speculum (Griffith and Veerapen, 1987). Bilateral mucosal flaps over the keel of the sphenoid bone are reflected laterally.

When the anterior wall of the sphenoid sinus has been reached by one of the aforementioned three routes, microdrill and/or bone punches are used to make a large opening. One or more septa can be identified, dividing the sphenoid sinus into concamerations; the removal or the flattening of septa allows the exposure of all the useful anatomic keypoints inside the sphenoid cavity, especially on the posterior wall. When those landmarks are not clearly visible, C-arm fluoroscopy or, more recently, a neuronavigation system could be helpful to provide surgical orientation. It is crucial to realize an adequate bony exposure of the sellar floor for the success of the approach. This latter is opened with a microdrill or bone punches or both; then the dura is incised in a midline position, in a linear or cross fashion, taking care, especially in the case of microadenomas, to avoid damaging a possibly ectopic carotid artery within the sella, which is very likely in acromegalic patients. For removal of a microadenoma, if it is visible on the surface of the gland, a cleavage plane between the microadenoma and the residual anterior pituitary should be found; when the microadenoma is not superficial a small incision can be made in the normal pituitary gland on the same side of the lesion, which can be removed with the help of small ring curettes. For removal of macroadenomas, the inferior and lateral components of the lesion are removed before the superior aspect. Indeed, the removal of the superior part first will prematurely allow the suprasellar cistern and the redundant diaphragma to fall into the operative field, thus reducing the ability to expose and remove the lateral portions of the lesion. Nevertheless, if the descent of the suprasellar portion of the lesion is not observed, a Valsalva maneuver can be useful, causing the protrusion of the suprasellar cistern into the sellar cavity. At the end of the procedure, the speculum is retracted and nasal structures are placed back in their primitive position. Nasal packing is placed for 24 hours in selected cases, but is not routinely employed.

Endoscopic endonasal transsphenoidal approach The endoscopic endonasal approach is performed by means of the endoscope as a stand-alone visualizing instrument, without the need for the transsphenoidal retractor; it has the same indications as the conventional microsurgical technique. It requires specific endoscopic skills and is based on a different concept because the endoscopic view that the surgeon receives on the video monitor is not the transposition of the real image, as it would be looking through the eyepiece of a microscope, but is the result of a microprocessor’s elaboration

SURGICAL APPROACH TO PITUITARY TUMORS 295 (Jho, 2000; de Divitiis and Cappabianca, 2002; microadenoma, it is easier to dissect tumor pseudocapCappabianca et al., 2004; Cappabianca et al., 2008a; sule from pituitary gland tissue, in order to achieve an Shahlaie et al., 2010). “en bloc” removal. Finally, after lesion removal, an The procedure consists of three main aspects: expoendoscopic exploration of the tumor cavity, by means sure of the lesion, management of the relevant patholof a 0-degree and/or angled scope, is performed to ogy, and reconstruction of the sella, that go through assess for the presence of any tumor remnants. three different steps, the nasal, the sphenoid, and the It should be noted that some pituitary adenomas presellar phases. In the first two steps, the corridor to the sent some features (e.g., dumb-bell shape, supra- or lesion and the room to work comfortably are identified parasellar extension, and/or fibrous or rubbery consisand adapted to the need of each single case, while in the tency, which is high likely in the case of a recurrent sellar phase the lesion is removed and the tailored recontumor) that may hinder such a route. In these cases an struction of the sellar area is realized. extended, purely endoscopic endonasal technique When the endoscope (18 cm in length, 4 mm in diam(Cavallo et al., 2005b; Kassam et al., 2005; de Divitiis eter) is introduced, it is possible to identify the main anaet al., 2007; Cappabianca et al., 2008b), as described tomic landmarks, such as the inferior turbinate laterally for suprasellar lesions, may be suitable for the removal and the nasal septum medially. Cottonoid pledgets of these selected pituitary adenomas. This technique soaked with diluted adrenaline (2:100 000) or with xyloallows the use of two surgical corridors, the conventional metazoline hydrochloride are positioned between the endosellar extra-arachnoidal and a suprasellar transarmiddle turbinate and the nasal septum; then, the middle achnoidal (Di Maio et al., 2011). The suprasellar aspect turbinate is gently pushed laterally. If more space is of the lesion is debulked and its capsule is dissected from required, middle turbinectomy on one side as well as a the surrounding neurovascular structures through an posterior bilateral ethmoidectomy can be carried out. arachnoid plane, using microscissors and sharp dissecCoagulation of the sphenoethmoid recess and the tion, as in a conventional open microsurgical technique. area around the sphenoid ostium is performed in order In cases where an adenoma extends into the cavernto avoid arterial bleeding from septal branches of the ous sinus, it should be noted that two different surgical sphenopalatine artery. The nasal septum is detached corridors have been described to gain access to different from the sphenoid rostrum by means of a microdrill areas of the cavernous sinus, according to the relationand the anterior wall of the sphenoid sinus is opened ship with the intracavernous carotid artery (ICA); one wide; the posterior nasal septum is then removed with corridor permits access to a compartment medial to a retrograde bone punch. The removal of all the sphenoid the ICA, while the other allows access to a cavernous septa is required to expose the anatomic landmarks sinus compartment lateral to it (Frank and Pasquini, inside the sphenoid cavity. After such a maneuver, the 2002; Cavallo et al., 2005a). posterior and lateral walls of the sphenoid sinus, with The first approach is indicated for pituitary adenothe sellar floor at the center, the sphenoethmoid planum mas projecting through the medial wall of the cavernous above it, and the clival indentation below, become sinus, without extension into the lateral compartment. visible. The tumor itself enlarges the C-shaped parasellar segFrom this point on, the surgeon performs a bimanual ment of the internal carotid artery, thus making easier dissection while a coworker holds the endoscope dynamthe suctioning and the curettage through this corridor. ically, allowing the comfortable introduction of two Conversely the approach to the lateral compartment of instruments through one or both nostrils, without comthe cavernous sinus is indicated in the case of tumors ing into conflict with it – the so-called “3-4 hands techinvolving the entire cavernous sinus. nique” (Castelnuovo et al., 2006); this requires a high The tumor removal proceeds from the extracaverlevel of collaboration between two surgeons. nous to the intracavernous portion. In the case of tumors The endoscope is held by the assistant in the patient’s occupying mainly the lateral compartment of the cavernright nostril; this is stretched upward (at 12 o’clock) by ous sinus, the growth of the lesion usually displaces the means of another instrument, usually a suction tube held ICA medially and pushes the cranial nerves laterally. by the first surgeon, in the most inferior position in the Delicate maneuvers of curettage and suction usually same nostril (at 6 o’clock). The main instrument is held in allow the removal of the parasellar portion of the lesion, the left nostril by the primary surgeon, using his or her in the same way as the intrasellar portion. dominant hand. After lesion removal, closure of the sellar floor is The sellar phase of the procedure follows the same required. Various techniques could be adopted for sellar rules as the microsurgical transsphenoidal approach. repair (intra- and/or extradural closure of the sella and Lesions involving the medial wall of the cavernous sinus packing of the sella with or without packing of the sphecan also be removed under endoscopic control; in case of noid sinus), depending on the size of osteodural defect

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and of the “dead space” inside the sella. Usually autologous or heterologous materials, either resorbable or not, if necessary, are used, taking care to avoid overpacking to prevent compression of the optic apparatus (Cappabianca et al., 2002b). If an extended approach has been used, especially in the suprasellar area, a consistent intraoperative CSF leakage occurs, due to intentional arachnoid opening, and thus an accurate reconstruction of the skull base defect is mandatory (Cavallo et al., 2007, Esposito et al., 2007). At the end of the procedure, hemostasis is obtained and the middle turbinate is gently restored in position. Packing of the nasal cavity is not commonly considered necessary.

TRANSCRANIAL APPROACHES There are different standard transcranial or alternative skull base approaches routinely used for the resection of pituitary tumors with extensive suprasellar and parasellar extension, depending on the direction of the extrasellar growth of the lesion: the unilateral subfrontal approach, the pterional approach, and the bilateral subfrontal interhemispheric approach. Depending on the particular compartment where the tumor is located, the size of the opening must be commensurate with the best and the safest removal of the tumor – “as small as possible, as large as necessary, but cosmetically optimal” (Yasargil, 1984, 1996). The unilateral subfrontal approach is indicated mainly for large suprasellar adenomas with an asymmetric supraparasellar extension and when the tumor has expanded into the upper prepontine cistern. It gives excellent bilateral access to the optic nerves and the chiasm (Powell and Pollock, 2003). Usually a bicoronal skin incision is adopted and craniotomy has a quadrangular shape, with the basal cut as low as possible. Preoperatively, the surgeon should have a clear idea of the size of the frontal sinuses: when opened, it should be stripped of mucosa and packed, then covered with galea capitis, temporalis fascia, or dural substitute. After the dural opening, the olfactory nerve is microscopically freed and the frontal lobe is retracted gently. Once the lesion has been identified, bipolar coagulation and incision of the capsule permit debulking and removal of the adenoma, between the optic nerves, preserving the pituitary stalk. During retrochiasmatic removal, care must be taken to minimize the manipulations, avoiding damage to the optic pathways. The frontolateral craniotomy, also known as the pterional approach, is a versatile craniotomy that gives good exposure of the inferolateral portion of the frontal lobe and the anterior temporal lobe. The pterional approach provides a short distance to the suprasellar region and

is the craniotomy of choice for adenomas with unilateral extrasellar parasellar extension, when there is the need to expose the compartment between the optic nerve and the ICA or the ICA and the third cranial nerve. It may be useful when cavernous sinus area invasion or a significant retrochiasmatic component is present (Dolenc, 1997). The skin incision designs a large radius arc to terminate at the midline, posterior to the hairline; the bone flap resembles a relatively circular shape, centered on the pterion. The dura is opened in a curvilinear fashion and the sylvian fissure is opened to ease frontal lobe retraction in order to realize an adequate corridor. The carotid cistern is completely opened, revealing the carotid artery and its branches. The tumor can be found in the optochiasmatic cistern, the interpeduncular cistern, and the cistern of lamina terminalis. In the case of intraventricular extension, the adenoma can be reached through the translamina terminalis corridor (King, 1979; Maira et al., 2000). The optimal technique is to decompress the tumor between the optic nerves and to mobilize it from the opticocarotid space to the interoptic space. When a large pituitary tumor invades the parasellar-cavernous sinus area and the adjacent central skull base regions, Dolenc’s variations (Dolenc et al., 1987; Dolenc, 1997) of this technique could be adopted. The bilateral interhemispheric subfrontal approach is not used today as frequently as the other two options, being mostly indicated for the treatment of large lesions, above all cranioparyngiomas, with retrochiasmatic extension. It offers a wide exposure – the craniotomy and dural opening are extended bilaterally – of the anterior cranial base with a good overview of the sellar, suprasellar, and parasellar areas. It affords an excellent midline orientation and may be used for the treatment of huge pituitary adenomas with large bilateral suprasellar extension.

COMPLICATIONS Complications of pituitary surgery depend on the surgical route employed to reach the sella; microsurgical transsphenoidal surgery offers a lower mortality and morbidity rate, and furthermore does not leave visible scars, when compared with the conventional transcranial approaches, resulting in it being more appealing to both patients and physicians. Serious complications of transsphenoidal surgery are uncommon and seem to be mainly related to the size of the tumor and the experience of the surgeon. Nevertheless, even if the mortality rate is low (usually < 1%), complications still occur (Ciric et al., 1997; Laws and Kern, 1982; Black et al., 1987; Cappabianca et al., 2002a; Kassam et al., 2011). Major morbidity (CSF leak, meningitis, stroke, intracranial hemorrhage, visual loss) occurs in 3.4% of cases,

SURGICAL APPROACH TO PITUITARY TUMORS 297 whereas minor complications (sinus disease, nasal septal microadenomas, while in macroadenomas it occurs in perforations) are present in approximately 4.6% of proabout 5% of cases. Permanent diabetes insipidus occurs cedures. Therefore, according to the anatomic compartin 3% of cases (Laws and Kern, 1982; Thapar and ments and relative structures involved during the Laws, 2001). different steps of the procedure, the possible complicaThe endoscopic approach is endonasal, so that rare tions can be divided into the following categories: (1) oronasal phase complications such as anesthesia of the nasofacial (mostly related to the approach itself ); (2) upper lip and of the anterior maxillary teeth, nasal septal sphenoid sinus (bleeding from the sphenopalatine artery, perforations, and saddle nose are almost absent. The sinusitis); (3) sellar (CSF leak); (4) parasellar and supralack of the nasal speculum avoids the development of sellar (including central nervous system injuries, cranial other rare complications, such as diastasis of the maxilla nerve damage – optic, olphactory, abducens, etc., vascuor fracture of the hard palate due to overspreading of the lar problems – carotid artery, basilar artery, cavernous speculum, fracture of the orbit, and injury or fracture of sinus, etc.); and (5) endocrine complications (Laws and the cribriform plate and subsequent CSF leak. Kern, 1982; Cappabianca et al., 2002a). Nevertheless, even though the corridor is completely Nasofacial complications, including nasal septal perendonasal and no incision of nasal mucosa is required, forations, bleeding from the mucosal branches of the the insertion and movement of the endoscope and blunt sphenopalatine artery, injury or fracture of the cribriand/or, above all, sharp instruments could cause a direct form plate with subsequent CSF leak, anesthesia of mucosal tearing. In addition, during the nasal step of an the upper lip and of the anterior maxillary teeth, saddle extended endonasal approach, it should be remembered nose, anosmia caused by undue superior nasal septum that the extensive manipulations necessary when perdissection, diastasis of the maxilla, or fracture of the forming maneuvers such as middle turbinectomy, postehard palate due to overspreading of the speculum, have rior septectomy, ethmoidectomy and/or the harvesting been reported. The occurrence of postoperative disorof the mucosal nasoseptal flap could increase the risk ders such as numbness of the upper lip and/or the anteof bleeding from sphenopalatine artery branches. rior maxillary teeth, nasal septum perforations, diastasis Series of endoscopic operations show an overall of the maxilla or fracture of the hard palate caused by decreased incidence of complications compared with overspreading of the speculum, fracture of the orbit historical microsurgical transsphenoidal series (Ciric and, moreover, injury or fracture of the cribriform plate et al., 1997). and subsequent CSF leak, could be definitely addressed The morbidity and mortality of transcranial to the microsurgical transsphendoidal technique. approaches have consistently decreased in the microsurSphenoid sinus complications more frequently occurgical era. A direct comparison of the complications ring are sinusitis and mucocele, a rare and usually latebetween the two groups is not possible because the onset disorder, caused by obstruction of the airflow at respective inclusion criteria have changed over the years. the osteomeatal complex. Fracture of the sphenoid body One aspect that should not be underestimated is that with injury to the optic nerves and the carotid arteries, nowadays transcranial surgery is usually employed for mostly related to the use of a transsphenoidal retractor giant and invasive pituitary adenomas or adenomas and/or to its overspread, sometimes due to thin or absent invading the parasellar compartment or the central skull bone, is exceptional, but must be kept in mind. base, representing a cohort of subjects with the most difComplications reported for the sellar phase of the ficult surgical management and intricate surgical probprocedure account essentially for the CSF leak, due to lems. Despite these considerations, a surprisingly high violation of the arachnoid membrane, subarachnoid total tumor resection rate (63–96%) has been reported hemorrhage, vasospasm, and tension pneumocephalus. more recently. A wide but infrequent range of suprasesllar and paraselSpecific complications are those events common to lar complications have been reported: hypothalamic any supratentorial craniotomy and related to traction injury, visual damage, hemorrhage or ischemia, vascular on the frontal and temporal lobes, dissection of major injury to one of the vessels of the circle of Willis, menor perforating vessels, and manipulation of the optic ingitis related to a CSF leak or to contamination; cavernor oculomotor nerves. The most common postoperative ous sinus injury (ICA; sixth, thirth, and fourth cranial complication is diabetes insipidus, which can be immedinerve injury), when dealing with lesions extending into ate, delayed (4–5 days), or triphasic, and either transient the parasellar area, and, finally, brainstem injury due (31.8%) or permanent (21.1%); the next most common is to a misdirected approach toward the clivus. Conversely, hemiparesis, either transient (33.3%), or permanent the endocrine sequelae are the most frequent complica(9.1%). Loss of vision can occur, most commonly due tions, namely loss of one or more anterior pituitary to disruption of the blood supply to the chiasm or the functional axes occurs in approximately 3% of optic nerves. Other complications, such as worsening

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of anterior pituitary function, epilepsy, infection, and CSF leak, can also occur. The strict operative mortality (5%) or mortality from disease-related complications (11.3%) is not negligible (Yasargil, 1996).

FINAL REMARKS Surgery, either transsphenoidal or transcranial, should accomplish the goal of a total removal of the lesion during the first operation, if possible, for the patient’s best chance of “cure”. Only a reasonable risk can be borne by the patient in terms of complications and postoperative morbidity; the surgeon must always attempt a complete and radical result, but at the same time should remember that a wide variety of different options – medical, surgical, and radiotherapeutic – are now effective treatment in terms of long-term results. What is crucial, regardless of the surgical option selected for a single case, whether transsphenoidal or transcranial, is to relate the goal of surgery to the patient’s needs, selecting the best option for the actual condition of the patient from among all the options available, surgical or otherwise.

REFERENCES Abe T, Ludecke DK (1999). Transnasal surgery for infradiaphragmatic craniopharyngiomas in pediatric patients. Neurosurgery 44: 957–964, discussion 964–966. Abosch A, Tyrrell JB, Lamborn KR et al. (1998). Transsphenoidal microsurgery for growth hormonesecreting pituitary adenomas: initial outcome and longterm results. J Clin Endocrinol Metab 83: 3411–3418. Alfieri A, Jho HD (2001). Endoscopic endonasal approaches to the cavernous sinus: surgical approaches. Neurosurgery 49: 354–360, discussion 360–362. Artico M, Pastore FS, Fraioli B et al. (1998). The contribution of Davide Giordano (1864–1954) to pituitary surgery: the transglabellar-nasal approach. Neurosurgery 42: 909–911, discussion 911–912. Baskin DS, Wilson CB (1984). Transsphenoidal treatment of non-neoplastic intrasellar cysts. A report of 38 cases. J Neurosurg 60: 8–13. Bevan JS, Webster J, Burke CW et al. (1992). Dopamine agonists and pituitary tumor shrinkage. Endocr Rev 13: 220–240. Bills DC, Meyer FB, Laws Jr ER et al. (1993). A retrospective analysis of pituitary apoplexy. Neurosurgery 33: 602–608, discussion 608–609. Black PM, Zervas NT, Candia GL (1987). Incidence and management of complications of transsphenoidal operation for pituitary adenomas. Neurosurgery 20: 920–924. Brisman MH, Katz G, Post KD (1996). Symptoms of pituitary apoplexy rapidly reversed with bromocriptine. Case report. J Neurosurg 85: 1153–1155. Cappabianca P, de Divitiis E (2004). Endoscopy and transsphenoidal surgery. Neurosurgery 54: 1043–1048, discussion 1048–1050.

Cappabianca P, Alfieri A, de Divitiis E (1998). Endoscopic endonasal transsphenoidal approach to the sella: towards functional endoscopic pituitary surgery (FEPS). Minim Invasive Neurosurg 41: 66–73. Cappabianca P, Cavallo LM, Colao A et al. (2002a). Surgical complications associated with the endoscopic endonasal transsphenoidal approach for pituitary adenomas. J Neurosurg 97: 293–298. Cappabianca P, Cavallo LM, Esposito F et al. (2002b). Sellar repair in endoscopic endonasal transsphenoidal surgery: results of 170 cases. Neurosurgery 51: 1365–1371, discussion 1371–1372. Cappabianca P, de Divitiis O, Maiuri F (2003). Evolution of transsphenoidal surgery. In: E de Divitiis, P Cappabianca (Eds.), Endoscopic Endonasal Transsphenoidal Surgery, Springer, Vienna and New York, pp. 1–7. Cappabianca P, Cavallo LM, de Divitiis E (2004). Endoscopic endonasal transsphenoidal surgery. Neurosurgery 55: 933–940, discussion 940–941. Cappabianca P, Cavallo LM, de Divitiis O et al. (2008a). Endoscopic pituitary surgery. Pituitary 11: 385–390. Cappabianca P, Cavallo LM, Esposito F et al. (2008b). Extended endoscopic endonasal approach to the midline skull base: the evolving role of transsphenoidal surgery. In: JD Pickard, N Akalan, C Di Rocco et al. (Eds.), Advances and Technical Standards in Neurosurgery, Springer, Vienna and New York, pp. 152–199. Cappabianca P, Cavallo LM, de Divitiis O et al. (2010). Pituitary surgery. In: LJ DeGroot, JL Jameson (Eds.), Endocrinology, 6th edn. Saunders Elsevier, Philadelphia, pp. 358–376. Cardoso ER, Peterson EW (1984). Pituitary apoplexy: a review. Neurosurgery 14: 363–373. Carrau RL, Jho HD, Ko Y (1996). Transnasal-transsphenoidal endoscopic surgery of the pituitary gland. Laryngoscope 106: 914–918. Casanueva FF, Molitch ME, Schlechte JA et al. (2006). Guidelines of the Pituitary Society for the diagnosis and management of prolactinomas. Clin Endocrinol (Oxf) 65: 265–273. Castelnuovo P, Pistochini A, Locatelli D (2006). Different surgical approaches to the sellar region: focusing on the “two nostrils four hands technique”. Rhinology 44: 2–7. Castelnuovo P, Dallan I, Pistochini A et al. (2007). Endonasal endoscopic repair of Sternberg’s canal cerebrospinal fluid leaks. Laryngoscope 117: 345–349. Caton R (1893). Notes of a case of acromegaly treated by operation. Br Med J 2: 1421–1423. Cavallo LM, Cappabianca P, Galzio R et al. (2005a). Endoscopic transnasal approach to the cavernous sinus versus transcranial route: anatomic study. Neurosurgery 56: ONS379–ONS389. Cavallo LM, Messina A, Cappabianca P et al. (2005b). Endoscopic endonasal surgery of the midline skull base: anatomical study and clinical considerations. Neurosurg Focus 19: E2. Cavallo LM, Messina A, Esposito F et al. (2007). Skull base reconstruction in the extended endoscopic transsphenoidal approach for suprasellar lesions. J Neurosurg 107: 713–720.

SURGICAL APPROACH TO PITUITARY TUMORS Cavallo LM, Prevedello D, Esposito F et al. (2008). The role of the endoscope in the transsphenoidal management of cystic lesions of the sellar region. Neurosurg Rev 31: 55–64, discussion 64. Chen JC, Amar AP, Choi S et al. (2003). Transsphenoidal microsurgical treatment of Cushing disease: postoperative assessment of surgical efficacy by application of an overnight low-dose dexamethasone suppression test. J Neurosurg 98: 967–973. Ciric I, Ragin A, Baumgartner C et al. (1997). Complications of transsphenoidal surgery: results of a national survey review of the literature and personal experience. Neurosurgery 40: 225–236, discussion 236–237. Colao A, Ferone D, Cappabianca P et al. (1997). Effect of octreotide pretreatment on surgical outcome in acromegaly. J Clin Endocrinol Metab 82: 3308–3314. Colao A, Di Sarno A, Cappabianca P et al. (2003). Withdrawal of long-term cabergoline therapy for tumoral and nontumoral hyperprolactinemia. N Engl J Med 349: 2023–2033. Cushing H (1909). III. Partial hypophysectomy for acromegaly: with remarks on the function of the hypophysis. Ann Surg 50: 1002–1017. Cushing H (1932). Intracranial tumors. Note upon a series of two thousands verified cases with surgical-mortality percentages pertaining thereto, Charles C, Thomas, Springfield, MA. Cushing H (1981). Medical Classic. The functions of the pituitary body: Harvey Cushing. Am J Med Sci 281: 70–78. Dallan I, Seccia V, Muscatello L et al. (2011). Transoral endoscopic anatomy of the parapharyngeal space: a step-by-step logical approach with surgical considerations. Head Neck 33: 557–561. Dandy WE (1934). The brain. In: D Lewis (Ed.), Practice of Surgery, WF Prior, Hagerstown, pp. 556–605. Davis DH, Laws Jr ER, Ilstrup DM et al. (1993). Results of surgical treatment for growth hormone-secreting pituitary adenomas. J Neurosurg 79: 70–75. de Divitiis E, Cappabianca P (2002). Endoscopic endonasal transsphenoidal surgery. In: JD Pickard (Ed.), Advances and Technical Standards in Neurosurgery, SpringerVerlag, Vienna and New York, pp. 173–177. de Divitiis E, Cappabianca P, Cavallo LM (2003). Endoscopic endonasal transsphenoidal approach to the sellar region. In: E de Divitiis, P Cappabianca (Eds.), Endoscopic Endonasal Transsphenoidal Surgery, Springer, Vienna and New York, pp. 91–130. de Divitiis E, Cavallo LM, Cappabianca P et al. (2007). Extended endoscopic endonasal transsphenoidal approach for the removal of suprasellar tumors: Part 2. Neurosurgery 60: 46–58, discussion 58–59. Di Maio S, Cavallo LM, Esposito F et al. (2011). Extended endoscopic endonasal approach for selected pituitary adenomas: early experience. J Neurosurg 114: 345–353. Doglietto F, Prevedello DM, Jane Jr JA et al. (2005). Brief history of endoscopic transsphenoidal surgery – from Philipp Bozzini to the First World Congress of Endoscopic Skull Base Surgery. Neurosurg Focus 19: E3. Dolenc VV (1997). Transcranial epidural approach to pituitary tumors extending beyond the sella. Neurosurgery 41: 542–550, discussion 551–552.

299

Dolenc VV, Kregar T, Ferluga M et al. (1987). Treatment of tumors invading the cavernous sinus. In: VV Dolenc (Ed.), The Cavernous Sinus, Springer-Verlag, New York, pp. 377–391. Elias WJ, Laws ER (2000). Transsphenoidal approach to lesion of the sella. In: HH Schmideck (Ed.), Schmideck and Sweet, 4th edn, WB Saunders, Philadelphia, Operative Neurosurgical Technique. Indications Methods and Results, pp 373–384. el-Mahdy W, Powell M (1998). Transsphenoidal management of 28 symptomatic Rathke’s cleft cysts with special reference to visual and hormonal recovery. Neurosurgery 42: 7–16, discussion 16–17. Esposito F, Dusick JR, Cohan P et al. (2006). Clinical review. Early morning cortisol levels as a predictor of remission after transsphenoidal surgery for Cushing’s disease. J Clin Endocrinol Metab 91: 7–13. Esposito F, Dusick JR, Fatemi N et al. (2007). Graded repair of cranial base defects and cerebrospinal fluid leaks in transsphenoidal surgery. Neurosurgery 60: 295–303, discussion 303–304. Fahlbusch R, Honegger J, Buchfelder M (1996). Acromegaly – the place of the neurosurgeon. Metabolism 45: 65–66. Fraioli B, Esposito V, Santoro A et al. (1995). Transmaxillosphenoidal approach to tumors invading the medial compartment of the cavernous sinus. J Neurosurg 82: 63–69. Frank G, Pasquini E (2002). Endoscopic endonasal approaches to the cavernous sinus: surgical approaches. Neurosurgery 50: 675. Fraser JF, Nyquist GG, Moore N et al. (2010). Endoscopic endonasal transclival resection of chordomas: operative technique clinical outcome and review of the literature. J Neurosurg 112: 1061–1069. Giordano D (1911). Compendio di chirurgia operativa italiana, UTET, Turin. Griffith HB, Veerapen R (1987). A direct transnasal approach to the sphenoid sinus. Technical note. J Neurosurg 66: 140–142. Guiot G (1973). Transsphenoidal approach in surgical treatment of pituitary adenomas: general principles and indications in non-functioning adenomas. In: PO Kohler, GT Ross (Eds.), Diagnosis and Treatment of Pituitary Adenomas, Excerpta Medica, Amsterdam, pp. 159–178. Guiot G, Derome P (1972). Indications for trans-sphenoid approach in neurosurgery. 521 cases. Ann Med Interne (Paris) 123: 703–712. Guiot G, Rougerie J, Fourestier M et al. (1963). Intracranial endoscopic explorations [in French]. Presse Med 71: 1225–1228. Handelsmann Horsley V (1911). Preliminary note on experimental investigations on the pituitary body. Br Med J 2: 1150–1151. Hardy J (1969). Transphenoidal microsurgery of the normal and pathological pituitary. Clin Neurosurg 16: 185–217. Hardy J (1971). Transsphenoidal hypophysectomy. J Neurosurg 34: 582–594. Hardy J, Vezina JL (1976). Transsphenoidal neurosurgery of intracranial neoplasm. Adv Neurol 15: 261–273.

300

D. SOLARI ET AL.

Hirsch O (1910). Endonasal method of removal of hypofiseal tumors. With a report of two successful cases. JAMA 55: 772–774. Jane Jr JA, Thapar K, Laws Jr ER (2001). Acromegaly: historical perspectives and current therapy. J Neurooncol 54: 129–137. Jankowski R, Auque J, Simon C et al. (1992). Endoscopic pituitary tumor surgery. Laryngoscope 102: 198–202. Jho HD (2000). Endoscopic transsphenoidal surgery. In: HH Schmidek (Ed.), Schmidek and Sweet, Operative Neurosurgical Techniques. WB Saunders, Philadelphia, pp. 385–397. Jho HD, Ha HG (2004). Endoscopic endonasal skull base surgery. Part 3. The clivus and posterior fossa. Minim Invasive Neurosurg 47: 16–23. Jho HD, Carrau RL, Ko Y (1996a). Endoscopic pituitary surgery. In: H Wilkins, S Rengachary (Eds.), Neurosurgical Operative Atlas, American Association of Neurological Surgeons, Park Ridge, IL, pp. 1–12. Jho HD, Carrau RL, McLaughlin ML et al. (1996b). Endoscopic transsphenoidal resection of a large chordoma in the posterior fossa. Case report. Neurosurg Focus 1: e3, discussion one page following e3. Jho HD, Carrau RL, McLaughlin MR et al. (1997). Endoscopic transsphenoidal resection of a large chordoma in the posterior fossa. Acta Neurochir (Wien) 139: 343–347, discussion 347–348. Kanter AS, Dumont AS, Asthagiri AR et al. (2005). The transsphenoidal approach. A historical perspective. Neurosurg Focus 18: e6. Kassam A, Snyderman CH, Mintz A et al. (2005). Expanded endonasal approach: the rostrocaudal axis. Part I. Crista galli to the sella turcica. Neurosurg Focus 19: 1–12, E3. Kassam AB, Prevedello DM, Carrau RL et al. (2011). Endoscopic endonasal skull base surgery: analysis of complications in the authors’ initial 800 patients. J Neurosurg 114: 1544–1568. Kato T, Sawamura Y, Abe H et al. (1998). Transsphenoidaltranstuberculum sellae approach for supradiaphragmatic tumours: technical note. Acta Neurochir (Wien) 140: 715–719. Kelley TF, Stankiewicz JA, Chow JM et al. (1996). Endoscopic closure of postsurgical anterior cranial fossa cerebrospinal fluid leaks. Neurosurgery 39: 743–746. Kennedy DW (1985). Functional endoscopic sinus surgery. Technique Arch Otolaryngol 111: 643–649. Kim J, Choe I, Bak K et al. (2000). Transsphenoidal supradiaphragmatic intradural approach: technical note. Minim Invasive Neurosurg 43: 33–37. King TT (1979). Removal of intraventricular craniopharyngiomas through the lamina terminalis. Acta Neurochir (Wien) 45: 277–286. Kitano M, Taneda M (2009). Extended transsphenoidal surgery for suprasellar craniopharyngiomas: infrachiasmatic radical resection combined with or without a suprachiasmatic trans-lamina terminalis approach. Surg Neurol 71: 290–298. Kitano M, Taneda M, Shimono T et al. (2008). Extended transsphenoidal approach for surgical management of pituitary

adenomas invading the cavernous sinus. J Neurosurg 108: 26–36. Komotar RJ, Starke RM, Raper DM et al. (2011). The endoscope-assisted ventral approach compared with open microscope-assisted surgery for clival chordomas. World Neurosurg 76: 318–327, discussion 259–262. Kouri JG, Chen MY, Watson JC et al. (2000). Resection of suprasellar tumors by using a modified transsphenoidal approach. Report of four cases. J Neurosurg 92: 1028–1035. Lanzino G, Laws Jr ER (2001). Pioneers in the development of transsphenoidal surgery: Theodor Kocher Oskar Hirsch and Norman Dott. J Neurosurg 95: 1097–1103. Laws Jr ER (1980). Transsphenoidal microsurgery in the management of craniopharyngioma. J Neurosurg 52: 661–666. Laws E (1993a). Clivus chordomas. In: LN Sekhar, IP Janecka (Eds.), Surgery of Cranial Base Tumors, Raven Press, New York, pp. 679–685. Laws ERJ (1993b). Transsphenoidal surgery. In: MLJ Apuzzo (Ed.), Brain Surgery: Complications, Avoidance and Management, Churchill Livingstone, New York, pp. 357–362. Laws Jr ER, Ebersold MJ (1982). Pituitary apoplexy – an endocrine emergency. World J Surg 6: 686–688. Laws ER, Kern EB (1982). Complications of transsphenoidal surgery. In: ER Laws, RV Randall, EB Kern et al. (Eds.), Management of Pituitary Adenomas and Related Lesions with Emphasis on Transsphenoidal Microsurgery, Appleton-Century-Crofts, New York, pp. 329–346. Laws ER, Lanzino G (Eds.), (2010). Transsphenoidal Surgery, Saunders Elsevier, Philadelphia. Laws ER, Kanter AS, Jane Jr JA et al. (2005). Extended transsphenoidal approach. J Neurosurg 102: 825–827, discussion 827–828. Leonhard M, Cappabianca P, de Divitiis E (2003). The endoscope, endoscopic equipment and instrumentation. In: E de Divitiis, P Cappabianca (Eds.), Endoscopic Endonasal Transsphenoidal Surgery, Springer-Verlag, Vienna and New York, pp. 9–19. Liu JK, Das K, Weiss MH et al. (2001). The history and evolution of transsphenoidal surgery. J Neurosurg 95: 1083–1096. Locatelli D, Rampa F, Acchiardi I et al. (2006). Endoscopic endonasal approaches for repair of cerebrospinal fluid leaks: nine-year experience. Neurosurgery 58: ONS246–256, discussion ONS-256–257.. Lohmann T, Trantakis C, Biesold M et al. (2001). Minor tumour shrinkage in nonfunctioning pituitary adenomas by long-term treatment with the dopamine agonist cabergoline. Pituitary 4: 173–178. Losa M, Mortini P, Urbaz L et al. (2006). Presurgical treatment with somatostatin analogs in patients with acromegaly: effects on the remission and complication rates. J Neurosurg 104: 899–906. Maira G, Pallini R, Anile C et al. (1996). Surgical treatment of clival chordomas: the transsphenoidal approach revisited. J Neurosurg 85: 784–792. Maira G, Anile C, Colosimo C et al. (2000). Craniopharyngiomas of the third ventricle: trans-lamina terminalis approach. Neurosurgery 47: 857–863, discussion 863–865.

SURGICAL APPROACH TO PITUITARY TUMORS Maira G, Anile C, Albanese A et al. (2004). The role of transsphenoidal surgery in the treatment of craniopharyngiomas. J Neurosurg 100: 445–451. McLaughlin N, Laws ER, Oyesiku NM et al. (2012). Pituitary centers of excellence. Neurosurgery 71: 916–924, discussion 924–926. Molitch ME, Elton RL, Blackwell RE et al. (1985). Bromocriptine as primary therapy for prolactin-secreting macroadenomas: results of a prospective multicenter study. J Clin Endocrinol Metab 60: 698–705. Perneczky A, Muller-Forell W, van Lindert E et al. (1999). Keyhole Concept in Neurosurgery, Thieme, Stuttgart and New York. Powell MP, Pollock JR (2003). Transcranial surgery. In: MP Powell, SL Lightman, ERJ Laws (Eds.), Management of Pituitary Tumors, Humana Press, Totowa, NJ, pp. 147–159. Rosegay H (1981). Cushing’s legacy to transsphenoidal surgery. J Neurosurg 54: 448–454. Ross DA, Norman D, Wilson CB (1992). Radiologic characteristics and results of surgical management of Rathke’s cysts in 43 patients. Neurosurgery 30: 173–178, discussion 178–179. Saito K, Kuwayama A, Yamamoto N et al. (1995). The transsphenoidal removal of nonfunctioning pituitary adenomas with suprasellar extensions: the open sella method and intentionally staged operation. Neurosurgery 36: 668–675, discussion 675–676. Schloffer H (1907). Erforgleiche operationen eines hypophysentumors auf nasalem wege. Wien Klin Wochenschr 20: 621–624. Shahlaie K, McLaughlin N, Kassam AB et al. (2010). The role of outcomes data for assessing the expertise of a pituitary surgeon. Curr Opin Endocrinol Diabetes Obes 17: 369–376. Shomali ME, Katznelson L (1999). Medical therapy for gonadotroph and thyrotroph tumors. Endocrinol Metab Clin North Am 28: 223–240, viii.

301

Simmons NE, Alden TD, Thorner MO et al. (2001). Serum cortisol response to transsphenoidal surgery for Cushing disease. J Neurosurg 95: 1–8. Stammberger H, Posawetz W (1990). Functional endoscopic sinus surgery. Concept indications and results of the Messerklinger technique. Eur Arch Otorhinolaryngol 247: 63–76. Stippler M, Gardner PA, Snyderman CH et al. (2009). Endoscopic endonasal approach for clival chordomas. Neurosurgery 64: 268–277, discussion 277–278. Swearingen B, Barker 2nd FG, Katznelson L et al. (1998). Long-term mortality after transsphenoidal surgery and adjunctive therapy for acromegaly. J Clin Endocrinol Metab 83: 3419–3426. Thapar K, Laws ERJ (2001). Pituitary tumors. In: AH Kaye, ER Laws Jr (Eds.), Brain Tumors, Churchill Livingstone, London, pp. 804–854. Weiss MH (1987). The transnasal transsphenoidal approach. In: MLJ Apuzzo (Ed.), Surgery of the Third Ventricle, Williams and Wilkins, Baltimore, pp. 476–494. Wilson CB (1990). Role of surgery in the management of pituitary tumors. Neurosurg Clin N Am 1: 139–159. Yasargil MG (1984). General operative techniques. In: MG Yasargil (Ed.), Microsurgical Anatomy of the Basal Cisterns and Vessels of the Brain, Diagnostic Studies, General Operative Techniques and Pathological Considerations of the Intracranial Aneurysms, Georg Thieme Verlag, New York, pp. 215–233. Yasargil MG (1996). Transcranial surgery for large pituitary adenomas. In: MG Yasargil (Ed.), Microneurosurgery: Microneurosurgery of CNS Tumors, Georg Thieme Verlag, Stuttgart, pp. 200–204. Zada G, Cappabianca P (2010). Raising the bar in transsphenoidal pituitary surgery. World Neurosurg 74: 452–454. Zada G, Du R, Laws Jr ER (2011). Defining the “edge of the envelope”: patient selection in treating complex sellarbased neoplasms via transsphenoidal versus open craniotomy. J Neurosurg 114: 286–300.