Abstract
Differentiating tumor from normal pituitary gland is very important for achieving complete resection without complications in endoscopic endonasal transsphenoidal surgery (ETSS) for pituitary adenoma. To facilitate such surgery, we investigated the utility of indocyanine green (ICG) fluorescence endoscopy as a tool in ETSS. Twenty-four patients with pituitary adenoma were enrolled in the study and underwent ETSS using ICG endoscopy. After administering 12.5 mg of ICG twice an operation with an interval > 30 min, times from ICG administration to appearance of fluorescence on vital structures besides the tumor were measured. ICG endoscopy identified vital structures by the phasic appearance of fluorescent signals emitted at specific consecutive elapsed times. Elapsed times for internal carotid arteries did not differ according to tumor size. Conversely, as tumor size increased, elapsed times for normal pituitary gland were prolonged but those for the tumor were reduced. ICG endoscopy revealed a clear boundary between tumors and normal pituitary gland and enabled confirmation of no more tumor. ICG endoscopy could provide a useful tool for differentiating tumor from normal pituitary gland by evaluating elapsed times to fluorescence in each structure. This method enabled identification of the boundary between tumor and normal pituitary gland under conditions of a low-fluorescence background, resulting in complete tumor resection with ETSS. ICG endoscopy will contribute to improve the resection rate while preserving endocrinological functions in ETSS for pituitary adenoma.
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Amano K, Aihara Y, Tsuzuki S, Okada Y, Kawamata T (2019) Application of indocyanine green fluorescence endoscopic system in transsphenoidal surgery for pituitary tumors. Acta Neurochir 161(4):695–706
Bruneau M, Appelboom G, Rynkowski M, Van Cutsem N, Mine B, De Witte O (2013) Endoscope-integrated ICG technology: first application during intracranial aneurysm surgery. Neurosurg Rev 36(1):77–85
Cappabianca P, Alfieri A, Thermes S, Buonamassa S, de Divitiis E (1999) Instruments for endoscopic endonasal transsphenoidal surgery. Neurosurgery 45(2):392–395
Catapano D, Sloffer CA, Frank G, Pasquini E, D’Angelo VA, Lanzino G (2006) Comparison between the microscope and endoscope in the direct endonasal extended transsphenoidal approach: anatomical study. J Neurosurg 104(3):419–425
Della Puppa A, Rustemi O, Gioffrè G, Causin F, Scienza R (2014) Transdural indocyanine green video-angiography of vascular malformations. Acta Neurochir 156(9):1761–1767
Della Puppa A, Rustemi O, Rossetto M, Gioffrè G, Munari M, Charbel FT, Scienza R (2014) The “squeezing maneuver” in microsurgical clipping of intracranial aneurysms assisted by indocyanine green videoangiography. Neurosurgery 10(Suppl 2):208–213
Della Puppa A, Rustemi O, Scienza R (2016) Intraoperative flow measurement by microflow probe during spinal dural arteriovenous fistula surgery. World Neurosurg 89:413–419
Della Puppa A, Rossetto M, Volpin F, Rustemi O, Grego A, Gerardi A, Ortolan R, Causin F, Munari M, Scienza R (2018) Microsurgical clipping of intracranial aneurysms assisted by neurophysiological monitoring, microvascular flow probe, and ICG-VA: outcomes and intraoperative data on a multimodal strategy. World Neurosurg 113:e336–e344
Frank G, Pasquini E, Farneti G, Mazzatenta D, Sciarretta V, Grasso V, Faustini Fustini M (2006) The endoscopic versus the traditional approach in pituitary surgery. Neuroendocrinology 83(3–4):240–248
Hide T, Yano S, Shinojima N, Kuratsu J (2015) Usefulness of the indocyanine green fluorescence endoscope in endonasal transsphenoidal surgery. J Neurosurg 122(5):1185–1192
Inoue A, Ohnishi T, Kohno S, Harada H, Nishikawa M, Ozaki S, Matsumoto S, Ohue S (2015) Utility of three-dimensional computed tomography for anatomical assistance in endoscopic endonasal transsphenoidal surgery. Neurosurg Rev 38(3):559–565
Inoue A, Ohnishi T, Kohno S, Nishida N, Nakamura Y, Ohtsuka Y, Matsumoto S, Ohue S (2015) Usefulness of an image fusion model using three-dimensional CT and MRI with indocyanine green fluorescence endoscopy as a multimodal assistant system in endoscopic transsphenoidal surgery. Int J Endocrinol 694273
Jankowski R, Auque J, Simon C, Marchal JC, Hepner H, Wayoff M (1992) Endoscopic pituitary tumor surgery. Laryngoscope 102(2):198–202
Jho HD, Alfieri A (2001) Endoscopic endonasal pituitary surgery: evolution of surgical technique and equipment in 150 operations. Minim Invasive Neurosurg 44(1):1–12
Litvack ZN, Zada G, Laws ER Jr (2012) Indocyanine green fluorescence endoscopy for visual differentiation of pituitary tumor from surrounding structures. J Neurosurg 116(5):935–941
Nishiyama Y, Kinouchi H, Senbokuya N, Kato T, Kanemaru K, Yoshioka H, Horikoshi T (2012) Endoscopic indocyanine green video angiography in aneurysm surgery: an innovative method for intraoperative assessment of blood flow in vasculature hidden from microscopic view. J Neurosurg 117(2):302–308
Raabe A, Nakaji P, Beck J, Kim LJ, Hsu FP, Kamerman JD, Seifert V, Spetzler RF (2005) Prospective evaluation of surgical microscope integrated intraoperative near-infrared indocyanine green videoangiography during aneurysm surgery. J Neurosurg 103(6):982–989
Sandow N, Klene W, Elbelt U, Strasburger CJ, Vajkoczy P (2015) Intraoperative indocyanine green videoangiography for identification of pituitary adenomas using a microscopic transsphenoidal approach. Pituitary 18(5):613–620
Schuette AJ, Cawley CM, Barrow DL (2010) Indocyanine green videoangiography in the management of dural arteriovenous fistulae. Neurosurgery 67(3):658–662
Suzuki K, Kodama N, Sasaki T, Matsumoto M, Ichikawa T, Munakata R, Muramatsu H, Kasuya H (2007) Confirmation of blood flow in perforating arteries using fluorescein cerebral angiography during aneurysm surgery. J Neurosurg 107(1):68–73
van Cauwenberge P, Calliauw L (1983) The transethmoidal-transsphenoidal route to the pituitary gland. Technique, advantages, limitations and possible complications. Acta Otorhinolaryngol Belg 37(6):883–891
Verstegen MJT, Tummers QRJG, Schutte PJ, Pereira AM, van Furth WR, van de Velde CJH, Malessy MJA, Vahrmeijer AL (2016) Intraoperative identification of a normal pituitary gland and an adenoma using near-infrared fluorescence imaging and low-dose indocyanine green. Oper Neurosurg (Hagerstown) 12(3):260–268
Yaniv E, Rappaport ZH (1997) Endoscopic transseptal transsphenoidal surgery for pituitary tumors. Neurosurgery 40(5):944–946
Acknowledgments
We would like to express our gratitude to Taichi Furumochi and Yasuhiro Shiraishi of the Department of Neurology, Ehime University Hospital, Japan; and Satsuki Myoga of the Department of Pathology, Ehime University Hospital, Japan, for their help in obtaining pathological and radiological findings.
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Inoue, A., Kohno, S., Ohnishi, T. et al. Tricks and traps of ICG endoscopy for effectively applying endoscopic transsphenoidal surgery to pituitary adenoma. Neurosurg Rev 44, 2133–2143 (2021). https://doi.org/10.1007/s10143-020-01382-4
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DOI: https://doi.org/10.1007/s10143-020-01382-4