Intraoperative Indocyanine Green Angiography for Assessing Flap Perfusion in Skull Base Reconstruction: A Systematic Review

Abstract

Objective This study was aimed to study the current use of intraoperative indocyanine green (ICG) angiography during skull base reconstruction and understand its efficacy in predicting postoperative magnetic resonance imaging (MRI) enhancement and flap.

Study Design The Embase, the Cochrane Central Register of Controlled Trials (CENTRAL), Web of Science, and Google Scholar databases were searched from the date of inception until August 2020 for studies of ICG flap perfusion assessment during skull base reconstruction. The primary outcome of interest was the development of cerebrospinal fluid (CSF) leak after skull base reconstruction. Secondary outcomes of interest included postoperative meningitis, flap MRI enhancement, flap necrosis, flap perfusion measurements, and total complications.

Results Search results yielded 189 studies, from which seven studies with a total of 104 patients were included in the final analysis. There were 44 nasoseptal flaps (NSF), two lateral nasal wall flaps (LNWF), 14 pericranial flaps (PCF), and 44 microvascular free flaps. The rates of CSF leak and postoperative MRI enhancement were 11 and 94%, respectively. There was one case of postoperative meningitis. Pooled analysis of the available data showed that intraoperative ICG flap perfusion was associated with flap enhancement on postoperative MRI (p = 0.008) and CSF leak (p = 0.315) by Fisher's exact test.

Conclusion The available literature suggests intraoperative ICG enhancement is associated with postoperative MRI enhancement. Given the small sample sizes in the literature and the rarity of complications associated with skull base reconstruction, intraoperative ICG enhancement has not been predictive of flap necrosis or postoperative complications such as CSF leak or meningitis.

Level of Evidence This study presents level 3 evidence as a systematic review of case studies, case reports, and retrospective and prospective trials with no blinding, controls, and inconsistently applied reference standards.

Keywords

indocyanine green angiography - skull base reconstruction - nasal flap - MRI - endoscopic surgery

• References

• 1 Slakter JS, Yannuzzi LA, Guyer DR, Sorenson JA, Orlock DA. Indocyanine-green angiography. Curr Opin Ophthalmol 1995; 6 (03) 25-32
• 2 Landsman ML, Kwant G, Mook GA, Zijlstra WG. Light-absorbing properties, stability, and spectral stabilization of indocyanine green. J Appl Physiol 1976; 40 (04) 575-583
• 3 Burke M. Indocyanine green dye for choroidal angiography. J Ophthalmic Nurs Technol 1996; 15 (05) 186-189
• 4 Cherrick GR, Stein SW, Leevy CM, Davidson CS. Indocyanine green: observations on its physical properties, plasma decay, and hepatic extraction. J Clin Invest 1960; 39: 592-600
• 5 Alander JT, Kaartinen I, Laakso A. et al. A review of indocyanine green fluorescent imaging in surgery. Int J Biomed Imaging 2012; 2012: 940585
• 6 Levesque E, Hoti E, Azoulay D. et al. Non-invasive ICG-clearance: a useful tool for the management of hepatic artery thrombosis following liver transplantation. Clin Transplant 2011; 25 (02) 297-301
• 7 Bell OH, Carreño E, Williams EL. et al. Intravenous indocyanine green dye is insufficient for robust immune cell labelling in the human retina. PLoS One 2020; 15 (02) e0226311
• 8 Boyle NS, Chang EL. Intraoperative use of indocyanine green and trypan blue mixed with fibrin glue in the excision of periocular cystic lesions. Am J Ophthalmol Case Rep 2020; 20: 100990
• 9 Cho WS, Kim JE, Kang HS. et al. Dual-channel endoscopic indocyanine green fluorescence angiography for clipping of cerebral aneurysms. World Neurosurg 2017; 100: 316-324
• 10 Cho SS, Salinas R, Lee JYK. Indocyanine-green for fluorescence-guided surgery of brain tumors: evidence, techniques, and practical experience. Front Surg 2019; 6: 11
• 11 Scott-Wittenborn N, Jackson RS. Intraoperative imaging during minimally invasive transoral robotic surgery using near-infrared light. Am J Otolaryngol 2018; 39 (02) 220-222
• 12 Klatt-Cromwell CN, Thorp BD, Del Signore AG, Ebert CS, Ewend MG, Zanation AM. Reconstruction of skull base defects. Otolaryngol Clin North Am 2016; 49 (01) 107-117
• 13 Hanasono MM, Silva A, Skoracki RJ. et al. Skull base reconstruction: an updated approach. Plast Reconstr Surg 2011; 128 (03) 675-686
• 14 Moy JD, Gardner PA, Sridharan S, Wang EW. Radial forearm free tissue transfer to clival defect. J Neurol Surg B Skull Base 2019; 80 (Suppl. 04) S380-S381
• 15 Kassam AB, Thomas A, Carrau RL. et al. Endoscopic reconstruction of the cranial base using a pedicled nasoseptal flap. Neurosurgery 2008;63(1, suppl 1)ONS44–ONS52, discussion ONS52–ONS53
• 16 de Weerd L, Mercer JB, Setså LB. Intraoperative dynamic infrared thermography and free-flap surgery. Ann Plast Surg 2006; 57 (03) 279-284
• 17 Erdmann D, Sweis R, Wong MS. et al. [Current perspectives of orthogonal polarization spectral imaging in plastic surgery] (in German). Chirurg 2002; 73 (08) 827-832
• 18 Hölzle F, Loeffelbein DJ, Nolte D, Wolff KD. Free flap monitoring using simultaneous non-invasive laser Doppler flowmetry and tissue spectrophotometry. J Craniomaxillofac Surg 2006; 34 (01) 25-33
• 19 Geltzeiler M, Nakassa ACI, Turner M. et al. Evaluation of intranasal flap perfusion by intraoperative indocyanine green fluorescence angiography. Oper Neurosurg (Hagerstown) 2018; 15 (06) 672-676
• 20 Shahein M, Prevedello DM, Beaumont TL. et al. The role of indocyanine green fluorescence in endoscopic endonasal skull base surgery and its imaging correlations. J Neurosurg 2020; (e-pub ahead of print)
• 21 Shahein M, Montaser AS, Todeschini AB. et al. Endoscopic endonasal resection of tuberculum sellae meningioma with utilization of indocyanine green. J Neurol Surg B Skull Base 2018; 79 (Suppl. 03) S269-S270
• 22 Kerr EE, Jamshidi A, Carrau RL. et al. Indocyanine green fluorescence to evaluate nasoseptal flap viability in endoscopic endonasal cranial base surgery. J Neurol Surg B Skull Base 2017; 78 (05) 408-412
• 23 Pestana IA, Coan B, Erdmann D, Marcus J, Levin LS, Zenn MR. Early experience with fluorescent angiography in free-tissue transfer reconstruction. Plast Reconstr Surg 2009; 123 (04) 1239-1244
• 24 Stubbs VC, Kuan EC, Kohanski MA. et al. Indocyanine green endoscopic video angiography to assess nasoseptal flap vascular perfusion in skull base reconstruction. J Neurol Surg B Skull Base 2018; 79 (01) 113
• 25 Iida T, Mihara M, Asakage T, Koshima I, Kawai K, Nakagawa M. Selection of free flaps in skull base reconstruction: versatility of perforator flaps and new diagnostic imaging devices. J Neurol Surg B Skull Base 2012; 73 (02) A500
• 26 National Heart, Lung, and Blood Institute. Study quality assessment tools. Accessed June 24, 2021 at: https://www.nhlbi.nih.gov/health-topics/study-quality-assessment-tools
• 27 A language and environment for statistical computing. R Foundation for Statistical Computing [computer program]. Accessed June 24, 2021 at: https://www.gbif.org/tool/81287/r-a-language-and-environment-for-statistical-computing
• 28 Nakassa ACI, Geltzeiler MN, Valappil B. et al. Use of intraoperative indocyanine green endoscopy in the assessment of vascularity of intranasal flaps. J Neurol Surg B Skull Base 2018; 79 (01) A124
• 29 Yano T, Okazaki M, Tanaka K, Tsunoda A, Aoyagi M, Kishimoto S. Use of intraoperative fluorescent indocyanine green angiography for real-time vascular evaluation of pericranial flaps. Ann Plast Surg 2016; 76 (02) 198-204
• 30 Komatsu F, Imai M, Hirayama A. et al. Endoscopic middle cranial fossa reconstruction with a subtemporal keyhole. World Neurosurg 2017; 108: 157-162
• 31 Harvey RJ, Parmar P, Sacks R, Zanation AM. Endoscopic skull base reconstruction of large dural defects: a systematic review of published evidence. Laryngoscope 2012; 122 (02) 452-459
• 32 Soudry E, Turner JH, Nayak JV, Hwang PH. Endoscopic reconstruction of surgically created skull base defects: a systematic review. Otolaryngol Head Neck Surg 2014; 150 (05) 730-738
• 33 Abiri A, Abiri P, Goshtasbi K. et al. Endoscopic anterior skull base reconstruction: a meta-analysis and systematic review of graft type. World Neurosurg 2020; 139: 460-470
• 34 Chabot JD, Patel CR, Hughes MA. et al. Nasoseptal flap necrosis: a rare complication of endoscopic endonasal surgery. J Neurosurg 2018; 128 (05) 1463-1472
• 35 Suzuki Y, Shimizu Y, Kasai S. et al. Indocyanine green fluorescence videoangiography for reliable variations of supraclavicular artery flaps. Arch Plast Surg 2019; 46 (04) 318-323
• 36 Hitier M, Cracowski JL, Hamou C, Righini C, Bettega G. Indocyanine green fluorescence angiography for free flap monitoring: a pilot study. J Craniomaxillofac Surg 2016; 44 (11) 1833-1841
• 37 Fu TS, Monteiro E, Witterick I. et al. Costs and perioperative outcomes associated with open versus endoscopic resection of sinonasal malignancies with skull base involvement. J Neurol Surg B Skull Base 2017; 78 (05) 430-440
• 38 Shahangian A, Soler ZM, Baker A. et al. Successful repair of intraoperative cerebrospinal fluid leaks improves outcomes in endoscopic skull base surgery. Int Forum Allergy Rhinol 2017; 7 (01) 80-86
• 39 Turri-Zanoni M, Zocchi J, Lambertoni A. et al. Endoscopic endonasal reconstruction of anterior skull base defects: what factors really affect the outcomes?. World Neurosurg 2018; 116: e436-e443
• 40 Gruss CL, Al Komser M, Aghi MK. et al. Risk factors for cerebrospinal leak after endoscopic skull base reconstruction with nasoseptal flap. Otolaryngol Head Neck Surg 2014; 151 (03) 516-521
• 41 Zanation AM, Carrau RL, Snyderman CH. et al. Nasoseptal flap reconstruction of high flow intraoperative cerebral spinal fluid leaks during endoscopic skull base surgery. Am J Rhinol Allergy 2009; 23 (05) 518-521
• 42 Tien DA, Stokken JK, Recinos PF, Woodard TD, Sindwani R. Cerebrospinal fluid diversion in endoscopic skull base reconstruction: an evidence-based approach to the use of lumbar drains. Otolaryngol Clin North Am 2016; 49 (01) 119-129
• 43 Garcia-Navarro V, Anand VK, Schwartz TH. Gasket seal closure for extended endonasal endoscopic skull base surgery: efficacy in a large case series. World Neurosurg 2013; 80 (05) 563-568