Accepted Manuscript The expanding spectrum of disease treated by the transnasal, transsphenoidal microscopic and endoscopic anterior skull base approach: single-center experience 2008-2015 David J. Cote, BS, Robert Wiemann, BA, Timothy R. Smith, MD, PhD, MPH, Ian F. Dunn, MD, Ossama Al-Mefty, MD, Edward R. Laws, MD PII:

S1878-8750(15)00582-3

DOI:

10.1016/j.wneu.2015.05.019

Reference:

WNEU 2907

To appear in:

World Neurosurgery

Received Date: 25 March 2015 Revised Date:

15 May 2015

Accepted Date: 16 May 2015

Please cite this article as: Cote DJ, Wiemann R, Smith TR, Dunn IF, Al-Mefty O, Laws ER, The expanding spectrum of disease treated by the transnasal, transsphenoidal microscopic and endoscopic anterior skull base approach: single-center experience 2008-2015, World Neurosurgery (2015), doi: 10.1016/j.wneu.2015.05.019. This is a PDF file of an unedited manuscript that has been accepted for publication. As a service to our customers we are providing this early version of the manuscript. The manuscript will undergo copyediting, typesetting, and review of the resulting proof before it is published in its final form. Please note that during the production process errors may be discovered which could affect the content, and all legal disclaimers that apply to the journal pertain.

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Title: The expanding spectrum of disease treated by the transnasal, transsphenoidal microscopic and endoscopic anterior skull base approach: single-center experience 2008-2015 Authors: 1David J. Cote, BS, 1Robert Wiemann, BA, 1Timothy R. Smith, MD, PhD, MPH, 1Ian F. Dunn, MD, 1Ossama Al-Mefty, MD, 1Edward R. Laws, MD

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Corresponding Author: Edward R. Laws, MD Professor of Neurosurgery Harvard Medical School Department of Neurosurgery Brigham and Women’s Hospital 15 Francis Street-PBB3 Boston, MA 02115 P: 617 525 8371 F: 617 734 8342 E: [email protected]

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Affiliations: 1Department of Neurosurgery, Brigham and Women’s Hospital, 15 Francis Street, Boston, MA 02115, United States of America

Key Words: craniopharyngioma; endoscopic surgery; meningioma; pituitary adenoma; skull base; transsphenoidal surgery

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Abbreviations: cerebrospinal fluid (CSF), adrenocorticotropic hormone (ACTH), thyroidstimulating hormone (TSH), insulin-like growth factor (IGF-1) Running Title: Expanding utility of the transsphenoidal approach to the anterior skull base

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Disclosures: The authors have nothing to disclose.

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Abstract Introduction The transsphenoidal approach was initially developed in neurosurgical practice as an operative

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approach to the pituitary gland. The introduction of the operating endoscope has improved the versatility of the transsphenoidal approach, broadening the spectrum of lesions effectively treated

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with this operative strategy.

Methods

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We performed a retrospective review of all patients who underwent transnasal, transsphenoidal operations at Brigham and Women’s Hospital from April 2008 through February 2015 and categorized each case by pathological diagnosis.

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Results

792 transnasal, transsphenoidal operations (512 endoscopic) were performed by nine neurosurgeons for 33 pathologies over a 7-year period. Pituitary adenomas (535, 67.55%) were

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the most common impetus for transsphenoidal operation. Others included Rathke’s cleft cysts (86, 10.86%), craniopharyngiomas (25, 3.16%), lympocytic hypophysitis/pituitary inflammation

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(21, 2.65%), arachnoid cysts (8, 1.01%), spindle cell oncocytoma (4, 0.51%), colloid cysts (4, 0.51%), and pituicytoma (2, 0.25%). Pituitary hyperplasia was treated in nine cases (1.14%), and pituitary apoplexy in seven (0.88%). 19 operations were undertaken for post-operative repairs (2.40%), and three for abscesses (0.38%).

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Other diseases treated transsphenoidally included chordomas (12, 1.52%), metastases (9, 1.14%), meningiomas (5, 0.63%), clival lesions (4, 0.51%), germinomas (3, 0.38%), granulomas (2, 0.25%), dermoid tumors (2, 0.25%), and one (0.13%) each of esthesioneuroblastoma, granular

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cell tumor, Wegener’s granulomatosis, olfactory neuroblastoma, glioneuronal tumor,

chondromyxoid fibroma, epidermoid, meningoencephalocele, aneurysm, neuroendocrine

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carcinoma, chondrosarcoma, and lymphoma.

Conclusions

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Although initially devised in neurosurgical practice for tumors of the pituitary gland, developments in technology now make the transsphenoidal approach an effective operative strategy for a wide range of anterior skull base lesions.

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Key Words

Craniopharyngioma; endoscopic surgery; meningioma; pituitary adenoma; skull base;

Introduction

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transsphenoidal surgery

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The transnasal, transsphenoidal approach to the skull base and brain has a history dating to the time of the Ancient Egyptians. Upon death, royal Egyptians of ancient times would undergo extensive burial rites, part of which involved removal of organs and mummification. Using a metal or wood rod, Egyptian embalmers would perform a transnasal craniotomy, breaking through the bones at the base of the skull to access the brain from below. The embalmers would

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then remove some brain matter through the nose, liquefying the rest and allowing it to drain through the nose by gravity.36

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In modern times, the first successful transsphenoidal approach was described by Hermann

Schloffer, who reported the resection of a pituitary tumor by the transsphenoidal approach in March 1907.31-33 Transcranial approaches to the pituitary had been attempted by pioneering

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neurosurgeons such as Victor Horsley, Fedor Krause, Charles Frazier, Harvey Cushing, and Walter Dandy, but high complication rates encouraged the development of extracranial

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approaches that could spare the vital anatomy of the region.8 In 1909, Theodor Kocher modified Schloffer’s approach to the sella, resecting the nasal septum submucosally to improve visualization.23 In 1910, Oskar Hirsch used an endonasal transsphenoidal approach for a pituitary

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tumor, and later introduced the nasal speculum for the operation.14

Following this rapid expansion in use, the transsphenoidal approach entered a period of relative dormancy in 1929, when Harvey Cushing, then the world’s most admired neurosurgeon,

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abandoned the transsphenoidal approach to the sella in favor of various transcranial approaches.8 Nevertheless, some neurosurgeons resisted Cushing’s lead and continued to innovate the

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transsphenoidal method, including Norman Dott, one of Cushing’s trainees, who introduced a nasal speculum with attached lighting apparatus.7 Later, Gerard Guiot introduced intraoperative fluoroscopic guidance and Jules Hardy adopted the operative microscope for pituitary surgery.7,10,13 More recent improvements came with the introduction of advanced imaging, hormone isolation and radioimmunoassays, and selective microsurgical operations for hyperfunctioning microadenomas.8

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More modern innovations of the transsphenoidal approach involve extensions beyond the sella for more diverse midline lesions of the skull base. Craniopharyngiomas—cystic tumors that arise

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in the sellar and suprasellar region—had been treated by the transsphenoidal approach as early as 1909.25 In the years after, transcranial routes were favored by Cushing and others because of the high morbidity and incomplete resection often accomplished by the transsphenoidal approach.

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During the second half of the 20th century, however, advances in technology made the

transsphenoidal approach to craniopharyngiomas attractive yet again. In 1980, the senior author

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reported a series of patients with craniopharyngiomas who were treated transsphenoidally, arguing that in certain cases of patients with an enlarged sella turcica, the transsphenoidal approach could match or exceed the effectiveness of transcranial routes.25

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The introduction of the operating endoscope further improved the ability of the transsphenoidal approach to rival the visualization obtained by transcranial routes for midline skull base lesions. Around the turn of the century, numerous reports by endoscopic pioneers including Hae Dong

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Jho, Paolo Cappabianca, Amin Kassam, Theodore Schwartz, and the senior author demonstrated the efficacy of the endoscope in treating a range of midline lesions, including pituitary

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adenomas, meningiomas, craniopharyngiomas, chordomas, and Rathke’s cleft cysts.2-4,16-20,22,27,38 Recent adoption of the three-dimensional endoscope has improved visualization during transsphenoidal operations even further, although studies have yet to demonstrate a significant difference in post-operative outcomes between patients undergoing operations with twodimensional versus three-dimensional endoscopes.1,15,21

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Today, most diseases treated transsphenoidally fall into four main categories (Table 1). First are congenital lesions, including arachnoid, colloid, pars intermedia, and Rathke’s cleft cysts, craniopharyngiomas, epidermoid and dermoid tumors, hamartomas, and germ cell tumors.

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Second are infectious and inflammatory lesions, including bacterial and fungal abscesses, mucocele and mucopyocele, Wegener’s granulomatosis, lymphocytic and granulomatous

hypophysitis, tuberculosis, and sarcoidosis. Third are vascular lesions, the least commonly

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treated transsphenoidally, including carotid and anterior communicating artery aneurysms, cavernomas, and carotid-cavernous fistulae. Fourth and most commonly are neoplasms,

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including pituitary adenomas and hyperplasia, astrocytomas, gangiogliomas, fibrosarcomas, pituicytomas, granular cell tumors, meningiomas, lymphomas, plasmacytomas, and metastatic cancer.

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Methods

We performed a retrospective review of all patients who underwent transnasal, transsphenoidal operations in the Department of Neurosurgery at Brigham and Women’s Hospital from April

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2008 through February 2015. We categorized each case based on pre-operative characteristics, intraoperative findings, and conclusive pathological diagnosis. No cases were excluded. Data

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were tabulated using IBM® SPSS® version 22 (IBM Inc., 2013).

Results

During the study period, 792 transnasal, transsphenoidal operations were performed by nine neurosurgeons at Brigham and Women’s Hospital over a 7-year period. Each case was categorized based on pre-operative characteristics, intraoperative findings, and conclusive

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pathological diagnosis (Table 2). Endoscopy was the primary surgical method in 512 cases, and microscopy or a combination of endoscopic-assisted microscopy was used in the remainder.

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These operations were undertaken for 33 different pathologies, including tumors, cysts, and postoperative complication repairs (Figure 1). Pituitary adenomas were the most common impetus for transsphenoidal operation, representing 535 (67.55%) of the assembled cases. Other

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pathologies of the sellar region that were operated on transsphenoidally included Rathke’s cleft cysts (86, 10.86%), craniopharyngiomas (25, 3.16%), lympocytic hypophysitis/pituitary

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inflammation (20, 2.53%), arachnoid cysts (8, 1.01%), spindle cell oncocytoma (4, 0.51%), colloid cysts (4, 0.51%), and pituicytoma (2, 0.25%). Pituitary apoplexy was treated in seven cases (0.88%), 19 operations were undertaken for post-operative cerebrospinal fluid (CSF) leak

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repairs or reoperations (2.40%), and three were undertaken for abscesses (0.38%).

Other tumors treated transsphenoidally included chordomas (12, 1.52%), metastases (9, 1.14%), meningiomas (5, 0.63%), clival lesions (4, 0.51%), germinomas (3, 0.38%), granulomas (2,

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0.25%), and dermoid tumors (2, 0.25%).

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The rarest cases treated transsphenoidally included one (0.13%) each of esthesioneuroblastoma, granular cell tumor, Wegener’s granulomatosis, olfactory neuroblastoma, glioneuronal tumor, chondromyxoid fibroma, epidermoid tumor, meningoencephalocele, aneurysm, neuroendocrine carcinoma, chondrosarcoma, and lymphoma.

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The pituitary tumors resected transsphenoidally were diverse (Table 3). Of the 535 patients who underwent resection of a pituitary adenoma during the eight year time period, 88 had acromegaly (16.45%), 69 harbored prolactinomas (12.90%), and 55 had Cushing’s disease (10.28%). 19 were

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found to have silent ACTH-secreting tumors (3.55%), and 12 were found to have

mammosomatotroph tumors (2.24%). Five patients harbored functioning gonadotroph adenomas (0.93%) and four had tumors that were TSH-secreting (0.75%). The remainder of the

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pathologically confirmed pituitary adenomas were non-functioning (283, 52.90%).

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Eighteen cases resulted in pathologically non-diagnostic pituitary tissue (2.27%). All of these patients had clinically-diagnosed pituitary microadenomas (Table 4). Of the clinical diagnoses, four patients were suspected to have acromegaly (13%), eight were suspected to have Cushing’s disease (26%), three were suspected to have prolactinomas (10%), and three were suspected to

(1.14%) (Table 5).

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Discussion

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have non-functioning adenomas (10%). Pituitary hyperplastic tissue was removed in 9 cases

The transnasal, transsphenoidal approach to the skull base has an ancient history, but its

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expansion as an operative technique for a variety of lesions is a relatively recent one. In the early days of neurosurgery, the transsphenoidal approach was used almost exclusively for access to tumors of the pituitary, the purpose for which it was originally designed.8,31,32

As technology advanced throughout the 20th century, however, the transsphenoidal approach was steadily expanded as an operative strategy for a more diverse selection of midline skull base

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lesions. With the introduction of the operative microscope to the transsphenoidal approach in the 1960s and the more recent introduction of the endoscope, visualization of the skull base via the transsphenoidal approach has improved dramatically, with a related expansion in case diversity.

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The aim of this report is to illustrate this operative diversity with a large series of transsphenoidal operations for a variety of pathologies.

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Nuances

The endoscope has gradually begun to replace the microscope as the primary instrument for

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neurosurgical transsphenoidal operations. Use of the endoscope yields superior visualization of the operative field, allowing the surgeon more reliably to identify and avoid damage to vital structures in the sellar region such as the carotid arteries and the optic nerve. It also provides better visualization of the suprasellar and parasellar spaces, which is of particular importance in

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many of the pathologies treated here that are not typical pituitary adenomas (e.g., meningiomas, craniopharyngiomas). Even in the case of typical adenomas, however, use of the endoscope allows for more effective preservation of the normal pituitary gland and more complete tumor

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resection, which in turn may lead to higher rates of endocrine remission and lower rates of recurrence, although this has not been shown conclusively.6,9,24,26 The disadvantages of

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endoscopic assistance during transsphenoidal surgery are few, but they include longer mean operative durations and occasional technical problems.1,4,19,26 Many surgeons, including most of our colleagues, are enthusiastic about 3D endoscopy.1,21,22,26

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In this contemporary series, pituitary adenomas, the third most common primary brain tumor, still make up the majority (67.55%) of cases treated transsphenoidally. These tumors are diverse

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among themselves, varying greatly in size, texture, and hormone secretion.

Prolactinomas comprised 12.9% of all of our resected pituitary tumors, despite being a pathology that can be usually be treated successfully with medical therapy in the form of dopamine agonists

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(DA).37 The indications for surgical resection of prolactinomas are two-fold: DA intolerance and/or DA resistance. DA intolerance is estimated to occur in 3 to 14% of patients, and presents

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as a constellation of symptoms including nausea, vomiting, insomnia, headache, mood changes, fatigue, and orthostatic hypertension.11,35,37 In these patients, surgical resection has the potential to normalize serum prolactin levels and ameliorate mass effect without the side effects associated

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with DA therapy.

DA resistance occurs when patients undergoing DA therapy do not experience normalization of serum prolactin levels or decrease in tumor size.28,29 DA resistance is estimated to occur in 11 to

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24% of patients, depending on the specific DA used.28 DA resistance causes significant morbidity both as a result of persistently elevated levels of serum prolactin and due to continued

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mass effect from the prolactinoma itself. Surgical resection in the case of DA resistance can achieve normalization of prolactin levels and reduction of mass effect.

Transsphenoidal surgery should not be considered a first-line treatment options for patients harboring prolactinomas, as medical therapy poses lower risks and a relatively high rate of success. All non-emergent patients with prolactinomas should initiate DA therapy, with regular

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serum prolactin tests and MRIs to assess tumor size. In the event that a patient develops DA intolerance and/or resistance, however, transsphenoidal resection can resolve hyperprolactinemia and symptoms of mass effect with relatively low risk of complication. Our referral practice

intolerant patients as a result of an extensive referral network.

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includes an abnormally high number of medically-resistant prolactinomas and medically-

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An interesting aspect of the case series reported here is the notorious difficulty in pre-operatively diagnosing pathologies of the sellar region. Often, imaging and laboratory results indicate a

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certain pathologic diagnosis, but the tissue returned after the operation provides a different diagnosis entirely.

For example, pituitary hyperplasia was reported in nine (1.14%) of the patients in this report

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based on pathological tissue analysis. Eight of these patients underwent transsphenoidal resection for clinically suspected Cushing’s disease, and were instead found to have ACTH hyperplasia on

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pathology. The ninth underwent resection of a suspected non-functioning microadenoma.

In addition, eighteen operations for pituitary microadenomas resulted in pathologically non-

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diagnostic tissue. In all cases, pituitary microadenomas were diagnosed based on elevated serum hormones (prolactin, ACTH, or IGF-1 for prolactinomas, Cushing’s disease, and acromegaly, respectively) and/or magnetic resonance imaging demonstrating an intrasellar lesion. It is likely that many of these microadenomas were too small to yield pathologically conclusive tissue, a relatively common occurrence during transsphenoidal surgery for Cushing’s disease. In the cases of suspected acromegaly and prolactinoma reported here, tumor was thought to be discovered

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intra-operatively, but the tissue samples procured were too scarce for a proper pathological analysis. In our patients with Cushing’s Disease, 66% with no pathologic tissue experienced

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endocrine remission.34

Twenty cases were reported as either lymphocytic hypophysitis or pituitary inflammation. Many of the cases of lymphocytic hypophysitis were diagnosed pre-operatively by radiographic

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imaging and clinical evaluation. Characteristic presentation of lymphocytic hypophysitis

typically includes severe, intractable headache, diabetes insipidus, and hypopituitarism.5,12 On

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MRI, the pituitary and pituitary stalk often appear enlarged, with a pear-shaped appearance.5,30 Patients diagnosed with lymphocytic hypophysitis in this case series received first-line treatment with high-dose corticosteroids and other pituitary hormone replacement as needed. Transsphenoidal operations were undertaken only when patients did not respond to medical

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treatment, or had persistent or relentlessly recurrent symptoms including vision loss, headache, diabetes insipidus, or hypopituitarism. During these operations, between one third to one half of the mass was resected to provide relief of pressure on the optic chiasm and the normal,

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uninvolved gland, which was left undisturbed as much as possible.

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The series reported here illuminates the modern operative diversity of the transnasal, transsphenoidal approach. It includes not only pathologies of the pituitary and sellar region in addition to adenomas (e.g., Rathke’s cleft cysts, pituicytoma, craniopharyngiomas) but also tumors that are often treated via more invasive transcranial approaches (e.g., meningiomas, germinomas). Many of the tumors treated transsphenoidally in this series are quite rare (e.g., spindle cell oncocytoma, olfactory neuroblastoma).

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Without the technological expansion that occurred during the last 50 years of the 20th century, it is likely that many of these patients would have been treated transcranially, as they were prior to

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the advent of the transsphenoidal approach in the early 1900s. The morbidity associated with the transcranial approach to anterior skull base lesions is often much higher than that of the transsphenoidal approach.8 Therefore, the latter is favored when feasible. Although the

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transsphenoidal approach is not appropriate for all skull base lesions, its versatility has improved

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greatly since its inception.

Conclusions

Although initially devised in neurosurgical practice as a route to tumors of the pituitary gland, the transnasal, transsphenoidal approach is now employed as an effective operative strategy for a

Acknowledgements

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wide range of midline anterior skull base lesions.

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The authors would like to acknowledge the contributions of Gabriel Zada, MD, Sherry Iuliano, NP, Peter Black, MD, PhD, Alexandra Golby, MD, Elizabeth Claus, MD, PhD, Arthur Day, MD,

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Mark Johnson, MD, PhD, and Robert Friedlander, MD.

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Barkhoudarian G, Del Carmen Becerra Romero A, Laws ER: Evaluation of the 3dimensional endoscope in transsphenoidal surgery. Neurosurgery 73:ons74-78; discussion ons78-79, 2013 Cappabianca P, Buonamassa S, Cavallo LM, Mariniello G, de Divitiis O: Neuroendoscopy: present and future applications. Clin Neurosurg 51:186-190, 2004

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Table 1: The modern diversity of diseases treated transsphenoidally.

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Neoplasms Pituitary adenoma Pituitary hyperplasia Granular cell tumor Pituicytoma Neuroendocrine carcinoma Astrocytoma Ganglioglioma Gangliocytoma Fibrosarcoma Meningioma Hemangiopericytoma Chordoma Chondrosarcoma Hemangioblastoma Plasmacytoma Lymphoma Metastatic carcinoma Chondromyxoid fibroma Pituitary carcinoma Neuroendocrine carcinoma

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Congenital Arachnoid cyst Rathke’s cleft cyst Craniopharyngioma Epidermoid tumor Dermoid tumor Teratoma Encephalocele Germ cell tumor Hamartoma Pars intermedia cyst Colloid cyst McCune-Albright syndrome Cholesteatoma Empty sella

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Inflammatory/Infectious Tuberculosis Sarcoidosis Lymphocytic hypophysitis Granulomatous hypophysitis Wegener’s granulomatosis Rosai-Dorfman disease Bacterial abscess Fungal abscess Cysticercosis Langerhans cell histiocytosis Mucocele Mucopyocele Tolosa-Hunt syndrome Grave’s disease Giant reparative granuloma

Vascular Carotid aneurysm A. comm. artery aneurysm Carotid-cavernous fistula Other Fibrous dysplasia Esthesioneuroblastoma Juvenile angiofibrosarcoma Sinu-nasal sarcinoma Acinic cell tumor Sphenoid cyst Salivary cyst Basilar impression

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Table 2: Transsphenoidal operations by Brigham and Women’s Department of Neurosurgery 4/2008 through 2/2015 (by pathology).

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*see Table 3, see Table 4

% 67.55 10.86 3.16 2.53 2.40 2.27 1.52 1.14 1.14 1.01 0.88 0.63 0.51 0.51 0.51 0.38 0.38 0.25 0.25 0.25 0.25 0.13 0.13 0.13 0.13 0.13 0.13 0.13 0.13 0.13 0.13 0.13 0.13

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Pituitary adenoma* Rathke’s cleft cyst Craniopharyngioma Lymphocytic hypophysitis/pituitary inflammation Post-operative repair/reoperation (CSF leak) Non-diagnostic pituitary tissue † Chordoma Pituitary hyperplasia Metastasis Arachnoid cyst Pituitary apoplexy Meningioma Clival lesion Spindle cell oncocytoma Colloid cyst Abscess Germinoma Granuloma Pituicytoma Dermoid tumor Fibrous dysplasia Granular cell tumor Esthesioneuroblastoma Wegener’s granulomatosis Olfactory neuroblastoma Glioneuronal tumor (ganglioglioma) Chondromyxoid fibroma Epidermoid tumor Meningoencephalocele Aneurysm Neuroendocrine carcinoma Chondrosarcoma Lymphoma Total

Number 535 86 25 20 19 18 12 9 9 8 7 5 4 4 4 3 3 2 2 2 2 1 1 1 1 1 1 1 1 1 1 1 1 792

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Table 3: Pituitary adenomas resected via transsphenoidal operations at Brigham and Women’s Hospital Department of Neurosurgery 4/2008 through 2/2015.

TE D EP AC C

RI PT

% 52.90 16.45 2.24 12.90 10.28 3.55 0.93 0.75

SC

Number 283 88 12 69 55 19 5 4 535

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Type Non functioning adenoma GH-secreting (acromegaly) Mammosomatotroph Prolactinoma ACTH-secreting (Cushing's disease) Silent ACTH FSH-secreting TSH-secreting Total

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Table 4: Clinical diagnoses for non-diagnostic pituitary tissue obtained during transsphenoidal operations at Brigham and Women’s Hospital Department of Neurosurgery 4/2008 through 2/2015. Type Number % Acromegaly 4 22 Cushing’s disease 8 44 Non-functioning adenoma 3 17 Prolactinoma 3 17 Total 18

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Figure 1. Some of the diverse lesions treated by the transsphenoidal approach to the anterior skull base: a) abscess, b) arachnoid cyst, c) chordoma, d) craniopharyngioma, e) dermoid tumor, f) epidermoid tumor, g) esthesioneuroblastoma, h) germ cell tumor, i) germinoma, j) Langerhan’s cell histiocytosis k) lymphocytic hypophysitis, l) meningioma, m) metastatic breast cancer, n) pituicytoma, o) spindle cell oncocytoma, p) sarcoidosis.

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Highlights

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The transsphenoidal approach was initially devised as a route to the pituitary With improved technology, the role of this approach has expanded A variety of lesions can now be effectively treated by transsphenoidal operation We report 792 transsphenoidal operations for 31 different pathologies

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Abbreviation List

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Cerebrospinal fluid (CSF) Adrenocorticotropic hormone (ACTH) Thyroid-stimulating hormone (TSH) Insulin-like growth factor (IGF-1)

The Expanding Spectrum of Disease Treated by the Transnasal, Transsphenoidal Microscopic and Endoscopic Anterior Skull Base Approach: A Single-Center Experience 2008-2015.

The transsphenoidal approach was initially developed in neurosurgical practice as an operative approach to the pituitary gland. The introduction of th...
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