Skip to main content

Advertisement

Log in

Application of indocyanine green fluorescence endoscopic system in transsphenoidal surgery for pituitary tumors

  • Original Article - Pituitaries
  • Published:
Acta Neurochirurgica Aims and scope Submit manuscript

Abstract

Background

For the precise removal of pituitary tumors, preserving the surrounding normal structures, we need real-time intraoperative information on tumor location, margins, and surrounding structures. The aim of this study was to evaluate the benefits of a new intraoperative real-time imaging modality using indocyanine green (ICG) fluorescence through an endoscopic system during transsphenoidal surgery (TSS) for pituitary tumors.

Methods

Between August 2013 and October 2014, 20 patients with pituitary and parasellar region tumors underwent TSS using the ICG fluorescence endoscopic system. We used a peripheral vein bolus dose of 6.25 mg/injection of ICG, started with a time counter, and examined how each tissue type increased and decreased in fluorescence through time.

Results

A total of 33 investigations were performed for 20 patients: 9 had growth hormone secreting adenomas, 6 non-functioning pituitary adenomas, 3 Rathke’s cleft cysts, 1 meningioma, and 1 pituicytoma. After the injection of ICG, the intensity of fluorescence of tumor and normal tissues under near-infrared light showed clear differences. We could differentiate tumor margins from adjacent normal tissues and define clearly the surrounding normal structures using the different fluorescent intensities time changes and tissue-specific fluorescence patterns.

Conclusions

The ICG endoscopic system is simple, user-friendly, quick, cost-effective, and reliable. The method offered real-time information during TSS to delimit pituitary and parasellar region tumor tissue from surrounding normal structures. This method can contribute to the improvement of total removal rates of tumors, reduction of complications after TSS, saving surgical time, and preserving endocrinological functions.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7
Fig. 8
Fig. 9

Similar content being viewed by others

Abbreviations

CS:

Cavernous sinus

CT:

Computed tomography

GHoma:

Growth hormone-producing pituitary adenoma

ICG:

Indocyanine green

ICS:

Intercavernous sinus

MRI:

Magnetic resonance image

NFoma:

Non-functioning pituitary adenoma

RCC:

Rathke’s cleft cysts

TSS:

Transsphenoidal surgery

T1WIGd:

T1-weighted image with gadolinium enhancement

References

  1. Amano K, Hori T, Kawamata T, Okada Y (2016) Repair and prevention of cerebrospinal fluid leakage in transsphenoidal surgery: a sphenoid sinus mucosa technique. Neurosurg Rev 39:123–131; discussion 131. https://doi.org/10.1007/s10143-015-0667-6

    Article  PubMed  Google Scholar 

  2. Bonneville JF, Cattin F, Gorczyca W, Hardy J (1993) Pituitary microadenomas: early enhancement with dynamic CT—implications of arterial blood supply and potential importance. Radiology 187:857–861. https://doi.org/10.1148/radiology.187.3.8497646

    Article  CAS  PubMed  Google Scholar 

  3. Campbell PG, Teo KS, Worthley SG, Kearney MT, Tarique A, Natarajan A, Zaman AG (2009) Non-invasive assessment of saphenous vein graft patency in asymptomatic patients. Br J Radiol 82:291–295. https://doi.org/10.1259/bjr/19829466

    Article  CAS  PubMed  Google Scholar 

  4. Ceylan S, Koc K, Anik I (2010) Endoscopic endonasal transsphenoidal approach for pituitary adenomas invading the cavernous sinus. J Neurosurg 112:99–107. https://doi.org/10.3171/2009.4.JNS09182

    Article  PubMed  Google Scholar 

  5. Ciric I, Ragin A, Baumgartner C, Pierce D (1997) Complications of transsphenoidal surgery: results of a national survey, review of the literature, and personal experience. Neurosurgery 40:225–236 discussion 236-227

    Article  CAS  PubMed  Google Scholar 

  6. Cusimano MD, Fenton RS (1996) The technique for endoscopic pituitary tumor removal. Neurosurg Focus 1:e1 discussion 1p following e3

    Article  CAS  PubMed  Google Scholar 

  7. d'Avella E, Volpin F, Manara R, Scienza R, Della Puppa A (2013) Indocyanine green videoangiography (ICGV)-guided surgery of parasagittal meningiomas occluding the superior sagittal sinus (SSS). Acta Neurochir 155:415–420. https://doi.org/10.1007/s00701-012-1617-5

    Article  PubMed  Google Scholar 

  8. Dashti R, Laakso A, Niemela M, Porras M, Hernesniemi J (2009) Microscope-integrated near-infrared indocyanine green videoangiography during surgery of intracranial aneurysms: the Helsinki experience. Surg Neurol 71:543–550; discussion 550. https://doi.org/10.1016/j.surneu.2009.01.027

    Article  PubMed  Google Scholar 

  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 62:1006–1015; discussion 1015-1007. https://doi.org/10.1227/01.neu.0000325862.83961.12

    Article  Google Scholar 

  10. Ferroli P, Acerbi F, Albanese E, Tringali G, Broggi M, Franzini A, Broggi G (2011) Application of intraoperative indocyanine green angiography for CNS tumors: results on the first 100 cases. Acta Neurochir Suppl 109:251–257. https://doi.org/10.1007/978-3-211-99651-5_40

    Article  CAS  PubMed  Google Scholar 

  11. Ferroli P, Acerbi F, Broggi M, Broggi G (2013) The role of indocyanine green videoangiography (ICGV) in surgery of parasagittal meningiomas. Acta Neurochir 155:1035. https://doi.org/10.1007/s00701-013-1722-0

    Article  PubMed  Google Scholar 

  12. Ferroli P, Acerbi F, Tringali G, Albanese E, Broggi M, Franzini A, Broggi G (2011) Venous sacrifice in neurosurgery: new insights from venous indocyanine green videoangiography. J Neurosurg 115:18–23. https://doi.org/10.3171/2011.3.JNS10620

    Article  PubMed  Google Scholar 

  13. Fujisawa I, Asato R, Kawata M, Sano Y, Nakao K, Yamada T, Imura H, Naito Y, Hoshino K, Noma S et al (1989) Hyperintense signal of the posterior pituitary on T1-weighted MR images: an experimental study. J Comput Assist Tomogr 13:371–377

    Article  CAS  PubMed  Google Scholar 

  14. Gorczyca W, Hardy J (1988) Microadenomas of the human pituitary and their vascularization. Neurosurgery 22:1–6

    Article  CAS  PubMed  Google Scholar 

  15. Hide T, Yano S, Kuratsu J (2014) Indocyanine green fluorescence endoscopy at endonasal transsphenoidal surgery for an intracavernous sinus dermoid cyst: case report. Neurol Med Chir (Tokyo) 54:999–1003

    Article  Google Scholar 

  16. Hide T, Yano S, Shinojima N, Kuratsu J (2015) Usefulness of the indocyanine green fluorescence endoscope in endonasal transsphenoidal surgery. J Neurosurg 122:1185–1192. https://doi.org/10.3171/2014.9.JNS14599

    Article  PubMed  Google Scholar 

  17. Hofstetter CP, Shin BJ, Mubita L, Huang C, Anand VK, Boockvar JA, Schwartz TH (2011) Endoscopic endonasal transsphenoidal surgery for functional pituitary adenomas. Neurosurg Focus 30:E10. https://doi.org/10.3171/2011.1.FOCUS10317

    Article  PubMed  Google Scholar 

  18. Holm C, Dornseifer U, Sturtz G, Ninkovic M (2010) Sensitivity and specificity of ICG angiography in free flap reexploration. J Reconstr Microsurg 26:311–316. https://doi.org/10.1055/s-0030-1249314

    Article  PubMed  Google Scholar 

  19. Holm C, Tegeler J, Mayr M, Becker A, Pfeiffer UJ, Muhlbauer W (2002) Monitoring free flaps using laser-induced fluorescence of indocyanine green: a preliminary experience. Microsurgery 22:278–287. https://doi.org/10.1002/micr.10052

    Article  CAS  PubMed  Google Scholar 

  20. Ito S, Muguruma N, Kimura T, Yano H, Imoto Y, Okamoto K, Kaji M, Sano S, Nagao Y (2006) Principle and clinical usefulness of the infrared fluorescence endoscopy. J Med Investig 53:1–8

    Article  Google Scholar 

  21. Kawamata T, Amano K, Hori T (2008) Novel flexible forceps for endoscopic transsphenoidal resection of pituitary tumors: technical report. Neurosurg Rev 31:65–68; discussion 68. https://doi.org/10.1007/s10143-007-0108-2

    Article  PubMed  Google Scholar 

  22. Kim DL, Cohen-Gadol AA (2013) Indocyanine-green videoangiogram to assess collateral circulation before arterial sacrifice for management of complex vascular and neoplastic lesions: technical note. World Neurosurg 79(404):e401–e406. https://doi.org/10.1016/j.wneu.2012.07.028

    Article  Google Scholar 

  23. Kim EH, Cho JM, Chang JH, Kim SH, Lee KS (2011) Application of intraoperative indocyanine green videoangiography to brain tumor surgery. Acta Neurochir 153:1487–1495; discussion 1494-1485. https://doi.org/10.1007/s00701-011-1046-x

    Article  PubMed  Google Scholar 

  24. Kimura T, Muguruma N, Ito S, Okamura S, Imoto Y, Miyamoto H, Kaji M, Kudo E (2007) Infrared fluorescence endoscopy for the diagnosis of superficial gastric tumors. Gastrointest Endosc 66:37–43. https://doi.org/10.1016/j.gie.2007.01.009

    Article  PubMed  Google Scholar 

  25. Kuroda K, Kinouchi H, Kanemaru K, Wakai T, Senbokuya N, Horikoshi T (2011) Indocyanine green videoangiography to detect aneurysm and related vascular structures buried in subarachnoid clots. J Neurosurg 114:1054–1056. https://doi.org/10.3171/2010.11.JNS1036

    Article  PubMed  Google Scholar 

  26. Kurokawa H, Fujisawa I, Nakano Y, Kimura H, Akagi K, Ikeda K, Uokawa K, Tanaka Y (1998) Posterior lobe of the pituitary gland: correlation between signal intensity on T1-weighted MR images and vasopressin concentration. Radiology 207:79–83. https://doi.org/10.1148/radiology.207.1.9530302

    Article  CAS  PubMed  Google Scholar 

  27. Litvack ZN, Zada G, Laws ER Jr (2012) Indocyanine green fluorescence endoscopy for visual differentiation of pituitary tumor from surrounding structures. J Neurosurg 116:935–941. https://doi.org/10.3171/2012.1.JNS11601

    Article  PubMed  Google Scholar 

  28. 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. https://doi.org/10.3171/2012.11.JNS112020

    Article  PubMed  Google Scholar 

  29. Mielke D, Malinova V, Rohde V (2014) Comparison of intraoperative microscopic and endoscopic ICG angiography in aneurysm surgery. Neurosurgery 10(Suppl 3):418–425; discussion 425. https://doi.org/10.1227/NEU.0000000000000345

    Article  PubMed  Google Scholar 

  30. Miki Y, Matsuo M, Nishizawa S, Kuroda Y, Keyaki A, Makita Y, Kawamura J (1990) Pituitary adenomas and normal pituitary tissue: enhancement patterns on gadopentetate-enhanced MR imaging. Radiology 177:35–38. https://doi.org/10.1148/radiology.177.1.2399335

    Article  CAS  PubMed  Google Scholar 

  31. Murakami K, Endo T, Tominaga T (2012) An analysis of flow dynamics in cerebral cavernous malformation and orbital cavernous angioma using indocyanine green videoangiography. Acta Neurochir 154:1169–1175. https://doi.org/10.1007/s00701-012-1354-9

    Article  PubMed  Google Scholar 

  32. 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 117:302–308. https://doi.org/10.3171/2012.5.JNS112300

    Article  PubMed  Google Scholar 

  33. Noura S, Ohue M, Seki Y, Tanaka K, Motoori M, Kishi K, Miyashiro I, Ohigashi H, Yano M, Ishikawa O, Miyamoto Y (2010) Feasibility of a lateral region sentinel node biopsy of lower rectal cancer guided by indocyanine green using a near-infrared camera system. Ann Surg Oncol 17:144–151. https://doi.org/10.1245/s10434-009-0711-2

    Article  PubMed  Google Scholar 

  34. Otani R, Fukuhara N, Ochi T, Oyama K, Yamada S (2012) Rapid growth hormone measurement during transsphenoidal surgery: analysis of 252 acromegalic patients. Neurol Med Chir (Tokyo) 52:558–562

    Article  Google Scholar 

  35. Raabe A, Beck J, Gerlach R, Zimmermann M, Seifert V (2003) Near-infrared indocyanine green video angiography: a new method for intraoperative assessment of vascular flow. Neurosurgery 52:132–139 discussion 139

    PubMed  Google Scholar 

  36. 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 103:982–989. https://doi.org/10.3171/jns.2005.103.6.0982

    Article  PubMed  Google Scholar 

  37. 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 18:613–620. https://doi.org/10.1007/s11102-014-0620-7

    Article  CAS  PubMed  Google Scholar 

  38. Takagi Y, Kikuta K, Nozaki K, Sawamura K, Hashimoto N (2007) Detection of a residual nidus by surgical microscope-integrated intraoperative near-infrared indocyanine green videoangiography in a child with a cerebral arteriovenous malformation. J Neurosurg 107:416–418. https://doi.org/10.3171/PED-07/11/416

    Article  PubMed  Google Scholar 

  39. Tamura Y, Hirota Y, Miyata S, Yamada Y, Tucker A, Kuroiwa T (2012) The use of intraoperative near-infrared indocyanine green videoangiography in the microscopic resection of hemangioblastomas. Acta Neurochir 154:1407–1412; discussion 1412. https://doi.org/10.1007/s00701-012-1421-2

    Article  PubMed  Google Scholar 

  40. Tsuzuki S, Aihara Y, Eguchi S, Amano K, Kawamata T, Okada Y (2014) Application of indocyanine green (ICG) fluorescence for endoscopic biopsy of intraventricular tumors. Childs Nerv Syst 30:723–726. https://doi.org/10.1007/s00381-013-2266-6

    Article  PubMed  Google Scholar 

  41. Ueba T, Abe H, Matsumoto J, Higashi T, Inoue T (2012) Efficacy of indocyanine green videography and real-time evaluation by FLOW 800 in the resection of a spinal cord hemangioblastoma in a child: case report. J Neurosurg Pediatr 9:428–431. https://doi.org/10.3171/2011.12.PEDS11286

    Article  PubMed  Google Scholar 

  42. Ueba T, Okawa M, Abe H, Nonaka M, Iwaasa M, Higashi T, Inoue T, Takano K (2013) Identification of venous sinus, tumor location, and pial supply during meningioma surgery by transdural indocyanine green videography. J Neurosurg 118:632–636. https://doi.org/10.3171/2012.11.JNS121113

    Article  PubMed  Google Scholar 

  43. Woitzik J, Horn P, Vajkoczy P, Schmiedek P (2005) Intraoperative control of extracranial-intracranial bypass patency by near-infrared indocyanine green videoangiography. J Neurosurg 102:692–698. https://doi.org/10.3171/jns.2005.102.4.0692

    Article  PubMed  Google Scholar 

  44. Yamada S, Takada K (2003) Angiogenesis in pituitary adenomas. Microsc Res Tech 60:236–243. https://doi.org/10.1002/jemt.10262

    Article  CAS  PubMed  Google Scholar 

  45. Yamamoto Y, Shibuya H, Okunaka T, Aizawa K, Kato H (1999) Fibrin plugging as a cause of microcirculatory occlusion during photodynamic therapy. Lasers Med Sci 14:129–135. https://doi.org/10.1007/s101030050034

    Article  CAS  PubMed  Google Scholar 

  46. Zada G, Cavallo LM, Esposito F, Fernandez-Jimenez JC, Tasiou A, De Angelis M, Cafiero T, Cappabianca P, Laws ER (2010) Transsphenoidal surgery in patients with acromegaly: operative strategies for overcoming technically challenging anatomical variations. Neurosurg Focus 29:E8. https://doi.org/10.3171/2010.8.FOCUS10156

Download references

Acknowledgements

We would like to thank Kostadin L. Karagiozov, MD, PhD, for his review of this manuscript and Ichiro Fujisawa, radiologist, for the advice on MRI of pituitary adenoma.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Kosaku Amano.

Ethics declarations

Conflict of interest

The authors declare that they have no competing interests.

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 and with the 1964 Helsinki declaration and its later amendments or comparable ethical standards.

Informed consent

Informed consent was obtained from all individual participants included in the study.

Additional information

Publisher’s note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

This article is part of the Topical Collection on Pituitaries

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Amano, K., Aihara, Y., Tsuzuki, S. et al. Application of indocyanine green fluorescence endoscopic system in transsphenoidal surgery for pituitary tumors. Acta Neurochir 161, 695–706 (2019). https://doi.org/10.1007/s00701-018-03778-0

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00701-018-03778-0

Keywords

Navigation