Abstract
Background
Perisellar infiltration may be responsible for incomplete removal of pituitary tumors. Since intraoperative visualization of parasellar structures is difficult during transsphenoidal surgery, we are describing the use of intraoperative direct contact ultrasound (IOUS).
Methods
Within 5 years, in 113 transsphenoidal operations (58 male, 55 female, age 14–81 years, 110 pituitary adenomas (mean diameter 26.6 mm, 69 non-secreting adenomas, 41 secreting adenomas), and 1 of each Rathke’s cleft cyst, craniopharyngioma, and xanthogranuloma), IOUS was applied. After wide opening of the sellar floor and removal of the intrasellar tumor portions, a commercially available side fire ultrasound probe is introduced, and in direct contact to the sellar envelope, the perisellar space is scanned perpendicular to the axis of the working channel. We compared the results of IOUS to postoperative MRI after 3–6 months.
Results
Identification of the intracavernous ICA, the anterior optic pathway, and the ACA, was possible, it was safe to operate close to them. In 65 operations (58%), further resection of tumor remnants was performed after IOUS. In this selected series, complete resection of tumors (stated by postoperative MRI after 3–6 months) was achieved in 75 operations (66%) and remission was achieved in 18 operations of secreting adenomas (44%). Compared to MRI after 3 to 6 months, the sensitivity of IOUS was 0.568 and the specificity was 0.907. No complications related to IOUS were seen.
Conclusions
Visualization of the perisellar compartments by IOUS is easy and fast to perform. It allows the surgeon to identify resectable tumor remnants intraoperatively, which otherwise could be missed.
Similar content being viewed by others
Abbreviations
- ACA:
-
Anterior cerebral artery
- ACTH:
-
Adrenocorticotropic hormone
- ADH:
-
Antidiuretic hormone
- A1:
-
A1-segment of ACA
- CS:
-
Cavernous sinus
- CSF:
-
Cerebrospinal fluid
- CT:
-
Computed tomography
- GH:
-
Growth hormone
- ICA:
-
Internal carotid artery
- IGF-1:
-
Insulin-like growth factor 1
- IOUS:
-
Intraoperative ultrasound
- MRI:
-
Magnetic resonance imaging
- OC:
-
Optic chiasm
- ON:
-
Optic nerve
- PRL:
-
Prolactin
- SIADH:
-
Syndrome of inappropriate ADH secretion
- TSH:
-
Thyroid-stimulating hormone
References
Ammirati M, Wei L, Ciric I (2013) Short-term outcome of endoscopic versus microscopic pituitary adenoma surgery: a systematic review and meta-analysis. J Neurol Neurosurg Psychiatry 84:843–849
Anand VK, Schwartz TH, Hiltzik DH, Kacker A (2006) Endoscopic transphenoidal pituitary surgery with real-time intraoperative magnetic resonance imaging. Am J Rhinol 20:401–405
Arita K, Kurisu K, Tominaga A, Kawamoto H, Iida K, Mizoue T, Pant B, Uozumi T (1998) Trans-sellar color Doppler ultrasonography during transsphenoidal surgery. Neurosurgery 42:81–85
Atkinson JL, Kasperbauer JL, James EM, Lane JI, Nippoldt TB (2000) Transcranial-transdural real-time ultrasonography during transsphenoidal resection of a large pituitary tumor. Case report. J Neurosurg 93:129–131
Barzaghi LR, Losa M, Giovanelli M, Mortini P (2007) Complications of transsphenoidal surgery in patients with pituitary adenoma: experience at a single Centre. Acta Neurochir 149:877–885
Bohinski RJ, Warnick RE, Gaskill-Shipley MF, Zuccarello M, van Loveren HR, Kormos DW, Tew JM Jr (2001) Intraoperative magnetic resonance imaging to determine the extent of resection of pituitary macroadenomas during transsphenoidal microsurgery. Neurosurgery 49:1133–1143
Cappabianca P, Cavallo LM, Colao A, Del Basso De Caro M, Esposito F, Cirillo S, Lombardi G, de Divitiis E (2002) Endoscopic endonasal transsphenoidal approach: outcome analysis of 100 consecutive procedures. Minim Invasive Neurosurg 45:193–200
Cappabianca P, Cavallo LM, de Divitiis O, Solari D, Esposito F, Colao A (2008) Endoscopic pituitary surgery. Pituitary 11:385–390
Dehdashti AR, Ganna A, Karabatsou K, Gentili F (2008) Pure endoscopic endonasal approach for pituitary adenomas: early surgical results in 200 patients and comparison with previous microsurgical series. Neurosurgery 62:1006–1015
Elias WJ, Chadduck JB, Alden TD, Laws ER Jr (1999) Frameless stereotaxy for transsphenoidal surgery. Neurosurgery 45:271–275
Fahlbusch R, Ganslandt O, Buchfelder M, Schott W, Nimsky C (2001) Intraoperative magnetic resonance imaging during transsphenoidal surgery. J Neurosurg 95:381–390
Furtado SV, Thakar S, Hegde AS (2012) The use of image guidance in avoiding vascular injury during trans-sphenoidal access and decompression of recurrent pituitary adenomas. J Craniomaxillofac Surg 40:680–684
Gerlach R, du Mesnil de Rochemont R, Gasser T, Marquardt G, Reusch J, Imoehl L, Seifert V (2008) Feasibility of Polestar N20, an ultra-low-field intraoperative magnetic resonance imaging system in resection control of pituitary macroadenomas: lessons learned from the first 40 cases. Neurosurgery 63:272–284
Greenman Y, Ouaknine G, Veshchev I, Reider G II, Segev Y, Stern N (2003) Postoperative surveillance of clinically nonfunctioning pituitary macroadenomas: markers of tumour quiescence and regrowth. Clin Endocrinol 58:763–769
Hazer DB, Isik S, Berker D, Guler S, Gurlek A, Yucel T, Berker M (2013) Treatment of acromegaly by endoscopic transsphenoidal surgery: surgical experience in 214 cases and cure rates according to current consensus criteria. J Neurosurg 119:1467–1477
Honegger J, Ernemann U, Psaras T, Will B (2007) Objective criteria for successful transsphenoidal removal of suprasellar nonfunctioning pituitary adenomas. A prospective study. Acta Neurochir 149:21–29
Ishikawa M, Ota Y, Yoshida N, Iino Y, Tanaka Y, Watanabe E (2015) Endonasal ultrasonography-assisted neuroendoscopic transsphenoidal surgery. Acta Neurochir 157:863–868
Ito M, Kuge A, Matsuda KI, Sato S, Kayama T, Sonoda Y (2017) The likelihood of remnant nonfunctioning pituitary adenomas shrinking is associated with the lesion’s blood supply pattern. World Neurosurg 107:137–141
Jane JA, Jr L, Laws ER (2001) The surgical management of pituitary adenomas in a series of 3,093 patients. J Am Coll Surg 193:651–659
Jho HD, Park IS, Alfieri A (2000) The future of pituitary surgery. Clin Neurosurg 47:83–98
Knappe UJ, Engelbach M, Konz K, Lakomek HJ, Saeger W, Schonmayr R, Mann WA (2011) Ultrasound-assisted microsurgery for Cushing’s disease. Exp Clin Endocrinol Diabetes 119:191–200
Knosp E, Steiner E, Kitz K, Matula C (1993) Pituitary adenomas with invasion of the cavernous sinus space: a magnetic resonance imaging classification compared with surgical findings. Neurosurgery 33:610–617
Losa M, Mortini P, Barzaghi R, Ribotto P, Terreni MR, Marzoli SB, Pieralli S, Giovanelli M (2008) Early results of surgery in patients with nonfunctioning pituitary adenoma and analysis of the risk of tumor recurrence. J Neurosurgery 108:525–532
Marcus HJ, Vercauteren T, Ourselin S, Dorward NL (2017) Intraoperative ultrasound in patients undergoing transsphenoidal surgery for pituitary adenoma: systematic review [corrected]. World Neurosurg 106:680–685
Mattozo CA, Dusick JR, Esposito F, Mora H, Cohan P, Malkasian D, Kelly DF (2006) Suboptimal sphenoid and sellar exposure: a consistent finding in patients treated with repeat transsphenoidal surgery for residual endocrine-inactive macroadenomas. Neurosurgery 58:857–865
McLaughlin N, Eisenberg AA, Cohan P, Chaloner CB, Kelly DF (2013) Value of endoscopy for maximizing tumor removal in endonasal transsphenoidal pituitary adenoma surgery. J Neurosurg 118:613–620
Micko AS, Wohrer A, Wolfsberger S, Knosp E (2015) Invasion of the cavernous sinus space in pituitary adenomas: endoscopic verification and its correlation with an MRI-based classification. J Neurosurg 122:803–811
Mortini P, Losa M, Barzaghi R, Boari N, Giovanelli M (2005) Results of transsphenoidal surgery in a large series of patients with pituitary adenoma. Neurosurgery 56:1222–1233
Nimsky C, Rachinger J, Iro H, Fahlbusch R (2004) Adaptation of a hexapod-based robotic system for extended endoscope-assisted transsphenoidal skull base surgery. Minim Invasive Neurosurg 47:41–46
Nimsky C, von Keller B, Ganslandt O, Fahlbusch R (2006) Intraoperative high-field magnetic resonance imaging in transsphenoidal surgery of hormonally inactive pituitary macroadenomas. Neurosurgery 59:105–114
Ota Y, Mami I (2013) Ultrasonography imaging during nasal endoscopic transsphenoidal surgery. J Otorhinolaryngol Relat Spec 75:27–31
Otori N, Haruna S, Kamio M, Ohashi G, Moriyama H (2001) Endoscopic transethmosphenoidal approach for pituitary tumors with image guidance. Am J Rhinol 15:381–386
Ram Z, Shawker TH, Bradford MH, Doppman JL, Oldfield EH (1995) Intraoperative ultrasound-directed resection of pituitary tumors. J Neurosurg 83:225–230
Ram Z, Bruck B, Hadani M (1999) Ultrasound in pituitary tumor surgery. Pituitary 2:133–138
Schwartz TH, Stieg PE, Anand VK (2006) Endoscopic transsphenoidal pituitary surgery with intraoperative magnetic resonance imaging. Neurosurgery 58:ONS44–ONS51
Solheim O, Selbekk T, Lovstakken L, Tangen GA, Solberg OV, Johansen TF, Cappelen J, Unsgard G (2010) Intrasellar ultrasound in transsphenoidal surgery: a novel technique. Neurosurgery 66:173–185
Solheim O, Johansen TF, Cappelen J, Unsgard G, Selbekk T (2016) Transsellar ultrasound in pituitary surgery with a designated probe: early experiences. Oper Neurosurg (Hagerstown) 12:128–134
Suzuki R, Asai J, Nagashima G, Itokawa H, Chang CW, Noda M, Fujimoto M, Fujimoto T (2004) Transcranial echo-guided transsphenoidal surgical approach for the removal of large macroadenomas. J Neurosurg 100:68–72
Thomale UW, Stover JF, Unterberg AW (2005) The use of neuronavigation in transnasal transsphenoidal pituitary surgery. Zentralbl Neurochir 66:126–132
Uhl E, Zausinger S, Morhard D, Heigl T, Scheder B, Rachinger W, Schichor C, Tonn JC (2009) Intraoperative computed tomography with integrated navigation system in a multidisciplinary operating suite. Neurosurgery 64:231–239
van Lindert EJ, Grotenhuis JA (2005) New endoscope shaft for endoscopic transsphenoidal pituitary surgery. Neurosurgery 57:203–206
Wagenmakers MA, Boogaarts HD, Roerink SH, Timmers HJ, Stikkelbroeck NM, Smit JW, van Lindert EJ, Netea-Maier RT, Grotenhuis JA, Hermus AR (2013) Endoscopic transsphenoidal pituitary surgery: a good and safe primary treatment option for Cushing’s disease, even in case of macroadenomas or invasive adenomas. Eur J Endocrinol 169:329–337
Watson JC, Shawker TH, Nieman LK, DeVroom HL, Doppman JL, Oldfield EH (1998) Localization of pituitary adenomas by using intraoperative ultrasound in patients with Cushing’s disease and no demonstrable pituitary tumor on magnetic resonance imaging. J Neurosurg 89:927–932
Wolfsberger S, Ba-Ssalamah A, Pinker K, Mlynarik V, Czech T, Knosp E, Trattnig S (2004) Application of three-tesla magnetic resonance imaging for diagnosis and surgery of sellar lesions. J Neurosurg 100:278–286
Yamasaki T, Moritake K, Hatta J, Nagai H (1996) Intraoperative monitoring with pulse Doppler ultrasonography in transsphenoidal surgery: technique application. Neurosurgery 38:95–97
Acknowledgements
This manuscript contains essential parts of the thesis of Dr. Med. Ali Alomari.
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Conflict of interest
All authors certify that they have no affiliations with or involvement in any organization or entity with any financial interest (such as honoraria; educational grants; participation in speaker’s bureaus; membership, employment, consultancies, stock ownership, or other equity interest; and expert testimony or patient-licensing arrangements), or non-financial interest (such as personal or professional relationships, affiliations, knowledge or beliefs) in the subject matter or materials discussed in this manuscript.
Ethical approval
All procedures performed in studies involving human participants were in accordance with the ethical standards of the institutional and/or national research committee (Ethikkommission der Ärztekammer Westfalen-Lippe, Universität Muenster) and with the 1964 Helsinki declaration and its later amendments or comparable ethical standards.
For this type of study formal consent is not required.
Additional information
This article is part of the Topical Collection on Pituitaries
Rights and permissions
About this article
Cite this article
Alomari, A., Jaspers, C., Reinbold, WD. et al. Use of intraoperative intracavitary (direct-contact) ultrasound for resection control in transsphenoidal surgery for pituitary tumors: evaluation of a microsurgical series. Acta Neurochir 161, 109–117 (2019). https://doi.org/10.1007/s00701-018-3747-x
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00701-018-3747-x