Acta Neurochirurgica

, Volume 161, Issue 1, pp 109–117 | Cite as

Use of intraoperative intracavitary (direct-contact) ultrasound for resection control in transsphenoidal surgery for pituitary tumors: evaluation of a microsurgical series

  • Ali Alomari
  • Christian Jaspers
  • Wolf-Dieter Reinbold
  • Joachim Feldkamp
  • Ulrich J. KnappeEmail author
Original Article - Pituitaries
Part of the following topical collections:
  1. Pituitaries



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).


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.


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.


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.


Intraoperative ultrasound Pituitary surgery Transsphenoidal surgery Pituitary tumor 



Anterior cerebral artery


Adrenocorticotropic hormone


Antidiuretic hormone


A1-segment of ACA


Cavernous sinus


Cerebrospinal fluid


Computed tomography


Growth hormone


Internal carotid artery


Insulin-like growth factor 1


Intraoperative ultrasound


Magnetic resonance imaging


Optic chiasm


Optic nerve




Syndrome of inappropriate ADH secretion


Thyroid-stimulating hormone



This manuscript contains essential parts of the thesis of Dr. Med. Ali Alomari.

Compliance with ethical standards

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.


  1. 1.
    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 84:843–849CrossRefGoogle Scholar
  2. 2.
    Anand VK, Schwartz TH, Hiltzik DH, Kacker A (2006) Endoscopic transphenoidal pituitary surgery with real-time intraoperative magnetic resonance imaging. Am J Rhinol 20:401–405CrossRefGoogle Scholar
  3. 3.
    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 42:81–85CrossRefGoogle Scholar
  4. 4.
    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 93:129–131CrossRefGoogle Scholar
  5. 5.
    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 149:877–885CrossRefGoogle Scholar
  6. 6.
    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 49:1133–1143Google Scholar
  7. 7.
    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 45:193–200CrossRefGoogle Scholar
  8. 8.
    Cappabianca P, Cavallo LM, de Divitiis O, Solari D, Esposito F, Colao A (2008) Endoscopic pituitary surgery. Pituitary 11:385–390CrossRefGoogle Scholar
  9. 9.
    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 62:1006–1015CrossRefGoogle Scholar
  10. 10.
    Elias WJ, Chadduck JB, Alden TD, Laws ER Jr (1999) Frameless stereotaxy for transsphenoidal surgery. Neurosurgery 45:271–275CrossRefGoogle Scholar
  11. 11.
    Fahlbusch R, Ganslandt O, Buchfelder M, Schott W, Nimsky C (2001) Intraoperative magnetic resonance imaging during transsphenoidal surgery. J Neurosurg 95:381–390CrossRefGoogle Scholar
  12. 12.
    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 40:680–684CrossRefGoogle Scholar
  13. 13.
    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 63:272–284CrossRefGoogle Scholar
  14. 14.
    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 58:763–769CrossRefGoogle Scholar
  15. 15.
    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 119:1467–1477CrossRefGoogle Scholar
  16. 16.
    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 149:21–29CrossRefGoogle Scholar
  17. 17.
    Ishikawa M, Ota Y, Yoshida N, Iino Y, Tanaka Y, Watanabe E (2015) Endonasal ultrasonography-assisted neuroendoscopic transsphenoidal surgery. Acta Neurochir 157:863–868CrossRefGoogle Scholar
  18. 18.
    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 107:137–141CrossRefGoogle Scholar
  19. 19.
    Jane JA, Jr L, Laws ER (2001) The surgical management of pituitary adenomas in a series of 3,093 patients. J Am Coll Surg 193:651–659CrossRefGoogle Scholar
  20. 20.
    Jho HD, Park IS, Alfieri A (2000) The future of pituitary surgery. Clin Neurosurg 47:83–98Google Scholar
  21. 21.
    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 119:191–200CrossRefGoogle Scholar
  22. 22.
    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 33:610–617Google Scholar
  23. 23.
    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 108:525–532CrossRefGoogle Scholar
  24. 24.
    Marcus HJ, Vercauteren T, Ourselin S, Dorward NL (2017) Intraoperative ultrasound in patients undergoing transsphenoidal surgery for pituitary adenoma: systematic review [corrected]. World Neurosurg 106:680–685CrossRefGoogle Scholar
  25. 25.
    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 58:857–865CrossRefGoogle Scholar
  26. 26.
    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 118:613–620CrossRefGoogle Scholar
  27. 27.
    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 122:803–811CrossRefGoogle Scholar
  28. 28.
    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 56:1222–1233CrossRefGoogle Scholar
  29. 29.
    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 47:41–46CrossRefGoogle Scholar
  30. 30.
    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 59:105–114CrossRefGoogle Scholar
  31. 31.
    Ota Y, Mami I (2013) Ultrasonography imaging during nasal endoscopic transsphenoidal surgery. J Otorhinolaryngol Relat Spec 75:27–31CrossRefGoogle Scholar
  32. 32.
    Otori N, Haruna S, Kamio M, Ohashi G, Moriyama H (2001) Endoscopic transethmosphenoidal approach for pituitary tumors with image guidance. Am J Rhinol 15:381–386CrossRefGoogle Scholar
  33. 33.
    Ram Z, Shawker TH, Bradford MH, Doppman JL, Oldfield EH (1995) Intraoperative ultrasound-directed resection of pituitary tumors. J Neurosurg 83:225–230CrossRefGoogle Scholar
  34. 34.
    Ram Z, Bruck B, Hadani M (1999) Ultrasound in pituitary tumor surgery. Pituitary 2:133–138CrossRefGoogle Scholar
  35. 35.
    Schwartz TH, Stieg PE, Anand VK (2006) Endoscopic transsphenoidal pituitary surgery with intraoperative magnetic resonance imaging. Neurosurgery 58:ONS44–ONS51Google Scholar
  36. 36.
    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 66:173–185CrossRefGoogle Scholar
  37. 37.
    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) 12:128–134Google Scholar
  38. 38.
    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 100:68–72CrossRefGoogle Scholar
  39. 39.
    Thomale UW, Stover JF, Unterberg AW (2005) The use of neuronavigation in transnasal transsphenoidal pituitary surgery. Zentralbl Neurochir 66:126–132CrossRefGoogle Scholar
  40. 40.
    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 64:231–239CrossRefGoogle Scholar
  41. 41.
    van Lindert EJ, Grotenhuis JA (2005) New endoscope shaft for endoscopic transsphenoidal pituitary surgery. Neurosurgery 57:203–206Google Scholar
  42. 42.
    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 169:329–337CrossRefGoogle Scholar
  43. 43.
    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 89:927–932CrossRefGoogle Scholar
  44. 44.
    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 100:278–286CrossRefGoogle Scholar
  45. 45.
    Yamasaki T, Moritake K, Hatta J, Nagai H (1996) Intraoperative monitoring with pulse Doppler ultrasonography in transsphenoidal surgery: technique application. Neurosurgery 38:95–97CrossRefGoogle Scholar

Copyright information

© Springer-Verlag GmbH Austria, ein Teil von Springer Nature 2018

Authors and Affiliations

  1. 1.Department of Neurosurgery, Johannes Wesling KlinikumUniversity Hospital of Ruhr-Universität BochumMindenGermany
  2. 2.Department of Endocrinology, Johannes Wesling KlinikumUniversity Hospital of Ruhr-Universität BochumMindenGermany
  3. 3.Institute of Radiology and Neuroradiology, Johannes Wesling KlinikumUniversity Hospital of Ruhr-Universität BochumMindenGermany
  4. 4.Department of EndocrinologyKlinikum BielefeldBielefeldGermany

Personalised recommendations