TRANSSPHENOIDAL APPROACHES IN PITUITARY TUMOR SURGERY . A REVIEW 
.ivko Gnjidiæ1, Tomislav Sajko1, Nenad Kudeliæ1 and Ma.a Malenica2 
1University Department of Neurosurgery, 2University Department of Pediatrics, Sestre milosrdnice University Hospital, Zagreb, Croatia 
SUMMARY . Transsphenoidal approach to pituitary tumors was for a long time reserved for sellar region tumors, whereas tumors expanding into extrasellar region were treated by transcranial approach. With the development of surgical equipment and gaining surgical experience, indications for the transsphenoidal approach and its modifications have become wider and ever more frequently used for pituitary tumors with extrasellar expansion. During the twenty-five years of performing pituitary surgery, we have operated on more than 1400 tumors of the sellar region using the transsphenoidal approach and its modifications. The novel transsphenoidal endoscopic approach is strongly taking more place in pituitary surgery, advancing the possibilities of the standard transsphenoidal approach. A review is presented of surgical approaches to pituitary tumors. 
Key words: Pituitary neoplasms . surgery; Skull base neoplasms . surgery; Neurosurgical procedures 
Since Sir Victor Horsley, a famous British neurosur-95% of pituitary tumors are treated via transsphenoidal geon, had performed the first surgery of pituitary tumor approach, whereas the rest of 5% are treated transcranitranscranially in 1904 in London, many surgeons accept-ally4. ed this approach1. After the Viennese surgeon Schloffer Very few surgical approaches remained unchanged demonstrated the great practical value of the sphenoid almost throughout the 20th century as the transsphenoibone sinus as the easiest way to reach the pituitary gland dal approach to pituitary tumors did. This fact speaks in 1906, he performed the first transnasal transsphenoi-for itself and for the brilliant idea of Schloffer to use the dal surgery of a pituitary tumor in 1907 in Innsbruck2,3. natural cavities of the nose and the sphenoid bone to After the initial success, a great number of surgeons and approach the pituitary gland5,6. otorhinolaryngologists accepted this approach with some Transsphenoidal approach was for a long time used modifications depending on the surgical equipment and for the tumors located in the sellar region, whereas the skills of the surgeon. From the beginning, this approach extrasellarly expanding lesions were treated transcraniwas in accordance with the minimally invasive concept ally. In the last 25 years, due to the development of sur-and should be regarded as its ancestor. This approach gical equipment and operative techniques, indications 
experienced a great number of technical ameliorations for the transsphenoidal approach have grown larger, ex-through which its use overwhelmed surgical treatment panding to lesions of the clivus, cavernous sinus and suof not only pituitary tumors but also of other pathology prasellar region7,8. of the sellar and parasellar region. Nowadays, more than Widening of the transsphenoidal approach to treat 
pathological lesions of the clivus and parasellar region Correspondence to: Head Doctor .ivko Gnjidiæ, MD, PhD, University have been described in detail by Couldwell and Weis9. Department of Neurosurgery, Sestre milosrdnice University Hospital, 
Using a combination of various speculum positions and 
Vinogradska c. 29, HR-10000 Zagreb, Croatia 
asymmetrical retractors, visualization of different parts 
E-mail: zgnjidic@kbsm.hr of the skull base has been achieved and bone resections 
Received September 26, 2005, accepted in revised form February 23, can be enlarged in the superior, inferior and lateral way 
Fig. 1. The width of viewing possibilities to the medial part of the skull base provided by modified transsphenoidal approach. 
(Fig. 1). With this modified, widened transsphenoidal approach it is possible to remove the lesions expanding toward the parasellar and suprasellar region. Using this modification of the transsphenoidal approach we removed 17 clivus tumors, predominantly chordomas. Suprasellar tumors, without enlargement of the sella turcica (craniopharyngeomas and ectopic suprasellar adenomas attached to the infundibulum), were successfully removed by Kuory and Mason using the modified transsphenoidal approach10,11. The same modification is described by Kato, naming it the transsphenoido-transtuberculum sellae approach, emphasizing its use in dealing with small lesions located above the diaphragma sellae and attached to the infundibulum with the possibility to keep the adenohypophysis intact12. The possibility of total removal of lesions located medially in the suprasellar region using the modified transsphenoidal approach has been described by Kaptain et al., who emphasize that it carries more complications than the standard transsphenoidal approach13. Being aware of the potential hazards of this approach, we used it in only two cases. 
Pituitary tumors frequently infiltrate cavernous sinuses and, in this case, they represent a great problem and challenge to many neurosurgeons. Neither stand
ard transsphenoidal approach nor transcranial approach allows for good visualization of the cavernous sinus. Fraioli et al. have described the transmaxillosphenoidal approach to lesions located at the medial border of the cavernous sinus. This approach allows for direct visualization of the intracavernous portion of the internal carotid artery during tumor removal14. Arita et al. report on the oblique transsphenoidal approach for removal of pituitary tumors expanding into the medial part of the cavernous sinus using a modified speculum which allows for good visualization of the lateral border of the sphenoid sinus and the medial part of the cavernous sinus15. Kitano and Tanada reach the tumors located in the parasellar region by opening the sphenoid sinus and the posterior ethmoid sinus on the tumor side16. Analyzing all the above mentioned modalities, we have performed the so-called .oblique transsphenoethmoidal approach. in 23 cases since 1996. Two different modalities in expanding the pituitary tumor into the cavernous sinus have been recognized: indentation and infiltration. Using the standard trans-sphenoidal approach it is possible to remove tumors reaching the cavernous sinus borders but not invading it. Invasion of the cavernous sinus by tumorous tissue is a complicated problem, especially in cases of hormonally active tumors. It is often possible to reduce tumors invading the cavernous sinus using the standard trans-sphenoidal approach, although it does not allow for good visualization of the cavernous sinus structures. Transcranial intradural or extradural approaches did not yield better results but enlarged the intraoperative trauma and complications19-22. On using the oblique transsphenoethmoidal approach the surgical corridor is almost the same as in the Fig. 2. Asymmetrical speculum.

Fig. 3. Oblique transsphenoethmoidal approach: (A) minimal osteotomy of the maxilla on the tumor opposite side; (B) the longer part of the speculum is placed in the sphenoid sinus. The shorter part is in the posterior ethmoidal sinus. In the middle of the operative field is the medial part of the cavernous sinus and intracavernous portion of the internal carotid 
artery. 
standard transsphenoidal approach. After the sphenoidal sinus is wide open, minimal osteotomy of the maxilla is done in the inferior lateral angle of the apertura piriformis, on the tumor-opposite side, removing the nasal process of the maxilla. The asymmetrical speculum is brought in the operative field and placed so that the longer part is in the sphenoidal sinus on the tumor-opposite side, and the shorter part of the speculum on the tumor side, reaching the posterior ethmoidal sinus which is wide open (Fig. 2). By doing so, the sphenoidal and ethmoidal sinuses are connected in a single cavity, and the posterior and lateral border of the sphenoidal sinus is located in the middle of the operative field17 (Fig. 3A,B). 
The bone prominence of the internal carotid artery and the optical nerve are completely visualized. Opening the dura in this region, the medial anterior and inferior part of the cavernous sinus is approached. There is more bleeding, especially after the tumor has been removed, but it can be easily controlled with the use of hemostatic material. 
Using the above mentioned approach it is possible to totally remove the intrasellar and intracavernous part of the tumor and to visualize the intracavernous portion of the internal carotid artery. Cranial nerves are pushed toward the lateral border of the cavernous sinus and are not exposed to intraoperative manipulations. 
Closing is done as in the standard transsphenoidal approach. Tumorous cavity is filled with fatty tissue followed by reconstruction of the anterior wall of the sella turcica (Fig. 4A,B,C,D). 
Our experience in using the oblique transsphenoethmoidal approach is favorable. It represents a logical pathway, especially in pituitary tumors invading the cavernous sinus. By this approach the cavernous sinus is reached completely extradurally and from the medial side, i.e. the side of the tumor growth, minimizing the risk of lesion of intracavernous cranial nerves. Also, the oblique transseptal approach and opening of the posterior ethmoidal sinus allows for keeping the nasal mucosa intact and preventing direct communication between the nasal bacterial flora and the operative field23. There 

Fig. 4. Preoperative MRI scans showing invasive pituitary adenoma infiltrating the right cavernous sinus (A, B, C). The early postoperative CT scan showing fatty tissue in the place of the removed adenoma (D). 
are few neurosurgeons skilled to reach this delicate field the logical pathway. It enables, with better visualizausing the transcranial approach. Even so, there is a high tion and minimal intraoperative trauma, to completely risk of leaving residual tumor behind that requires fur-remove the tumor or to reduce it to a size that can be ther surgical, medicamentous treatment or irradiation. further treated radiosurgically. Modifications of the transsphenoidal approach such as Superior visualization and excellent surgical results the oblique transsphenoethmoidal approach represent in endoscopic sinus surgery have stimulated neurosur
geons to explore the use of endoscope in transsphenoidal surgery24. The first use of an endoscope in pituitary surgery was reported by Bushe and Halvers in 1978, but this work remained almost unnoticed25. At first, rigid endoscopes or sinus scopes were used to verify any residual part of the tumor following the standard trans-sphenoidal approach, enabling the so-called .behind the corner look.. In 1982 we used such a rigid endoscope (sinus scope for straight view and 30 and 70 degree sinus scope) in pituitary surgery without knowing that Bushe and Havers were doing the same26,27. 
Because of the lack of video camera and often operating field desterilization we used that technique only for visualization the tumor cavity after removal of large extrasellarly extending tumors. Thanks to data obtained with other forms of intraoperative control (x-ray, urgent intraoperative histopathology, 45° mirror examination and intraoperative hormone level monitoring), we had good intraoperative control in cases of hormone secreting adenomas with good postoperative functional results27-29. 
With technological advancement of endoscopic surgery, novel systems of rigid and flexible endoscopes for use in neurosurgery and pituitary surgery were developed. Nowadays, endoscope is mostly being used as an ancillary instrument during transsphenoidal microsurgery. Yanniv and Rappaport have described the combined 
approach during which the endoscope was used in the initial transseptal phase and afterwards converted into a standard transsphenoidal approach. This resulted in a reduced postoperative morbidity, also taking the advantage of stereoscopic visualization by using the operative microscope28. Further technological development allowed for the whole transsphenoidal surgery to be performed endoscopically, even more reducing postoperative morbidity. 
The main advantages of endoscopic approach are better visualization, the so-called .panoramic view., better illumination and magnification. There is no need of nostril tampons, and the patient could be released from the hospital at 24 hours postoperatively28. The endoscope is usually introduced into the left nostril. The use of the endoscope is facilitated by the placement of a table-mounted endoscope holder on the left-hand side of the operative table to free both hands of the surgeon29. Despite the opinion that endoscopic approach allows for quicker postoperative recovery and reduces hospital stay, some experienced pituitary surgeons question this statement30,31. There are no large series reporting results accomplished by using either this method or a long-time follow up of patients submitted to this type of surgery32. 
The main disadvantages of the transsphenoidal endoscopic approach are the lack of stereoscopic view and the lack of instrumentation. Also, it lacks control in cas

Fig. 5. Giant craniopharyngeoma successfully removed by endoscopy-assisted transsphenoidal approach: (A) preoperative MRI scan; (B) postoperative MRI scan. 
es of serious intraoperative bleeding24. On the other hand, the transsphenoidal endoscopic approach provides many advantages of a minimally invasive method with satisfactory results. 
Worldwide, the transseptal, transsphenoidal approach is the method of choice in treating most of the sellar region tumors33,34. This approach has been developed and modified throughout the 20th century. The endoscopic approach has been developed over the last decade35-37. Better efficacy and minimal invasiveness of the transsphenoidal technique flourish in the hand of a skilled neurosurgeon38-40. 
Nowadays, two different surgical approaches play a dominant role in pituitary surgery: microsurgical and endoscopic, each with its own philosophy. In-between, there is an endoscopic assisted transsphenoidal surgery, as a golden compromise (Fig. 5A,B). The operative microscope allows for an excellent three-dimensional view and comfortable surgical manipulation, while the endoscope provides a closer look and reduces the postoperative recovery period41. 
A neurosurgeon skilled in the standard transsphenoidal approach could also be trained for the endoscope use. An inexperienced neurosurgeon should be trained to be able to perform pituitary surgery with both modalities. 
The objective differences between the two above mentioned approaches should become clear after large series of patients treated endoscopically are reported. Both of these methods are efficient if: the pathological lesion is successfully identified and removed; the neurosurgeon works with highly sophisticated equipment; and the neurosurgeon is skilled in various operative techniques. 
Edward Laws, an experienced pituitary neurosurgeon and President of the International Association of the Pituitary Surgeons, has stated: .It is important to remember that the goal of pituitary surgery is not releasing the patient from the hospital on the first or second postoperative day, but to successfully remove the tumor.33. 
At this moment, it remains unclear whether an experienced neurosurgeon can achieve the same results using either the standard or the endoscopic transsphenoidal approach. Until now, there is a small amount of data to make a straight conclusion, but according to the results published so far, one can only be impressed with the possibilities the endoscopic transssphenoidal approach is offering. 
In our opinion, the advantages of the endoscopic transsphenoidal approach are very remarkable and every young neurosurgeon has to be trained to perform such a surgery. Yet, it has to be emphasized that the standard microsurgical transsphenoidal approach still remains the number one procedure in pituitary tumor surgery worldwide. The future lies in the complementary use of these two great operative techniques. 
Because of various typical and recognizable anatomic and topographic markers, the new and sophisticated method of neuronavigation has a negligible role in pituitary surgery44,45. 
Rarely, the suprasellar and parasellar extending tumors are primarily or after transsphenoidal reduction operated by transcranial approach. In these cases we insist on minimally invasive methods4,46,47. The radio-surgical method has the leading place in treating tumor residua in the cavernous sinus. In the last two years, we successfully used gamma knife in the treatment of 30 patients48-51. 
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Sa.etak 
SMJEROVI RAZVOJA KIRUR.KOG LIJEÈENJA TUMORA HIPOFIZE 
.. Gnjidiæ, T. Sajko, N. Kudeliæ i M. Malenica 
Transsfenoidni pristup tumorima hipofize dugo je bio rezerviran za intraselarne neoplazme, dok se ekstraselarno pro.irene tumore rje.avalo transkranijskim pristupom. Zahvaljujuæi razvoju kirur.ke opreme i instrumentarija te veæem iskustvu operatera indikacije za ovaj pristup i njegove modalitete postale su .ire pa se èe.æe rabe i za ekstraselarno pro.irene tumore. Tijekom 25 godina bavljenja kirurgijom hipofize operirali smo preko 1400 tumora selarne regije rabeæi transsfenoidni pristup i njegove modalitete. Novi endoskopski transsfenoidni pristup zauzima sve vi.e mjesta u kirur.kom lijeèenju hipofize te tako poveæava lepezu moguænosti pro.irenog transsfenoidnog pristupa. Prikazani su kirur.ki pristupi lijeèenju tumora hipofize. 
Kljuène rijeèi: Neoplazme hipofize . kirurgija; Neoplazme baze lubanje . kirurgija; Neurokirur.ki zahvati 
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