Advertisement

Acta Neurochirurgica

, Volume 160, Issue 2, pp 317–324 | Cite as

Investigation of the usefulness of fluorescein sodium fluorescence in stereotactic brain biopsy

  • Ady Thien
  • Julian Xinguang Han
  • Krishan Kumar
  • Yew Poh Ng
  • Jai Prashanth Rao
  • Wai Hoe Ng
  • Nicolas Kon Kam King
Original Article - Neurosurgical Techniques

Abstract

Background

Intraoperative frozen section assessment, to confirm acquisition of pathological tissues, is used in stereotactic brain biopsy to minimise sampling errors. Limitations include the dependence on dedicated neuro-oncology pathologists and an increase in operative duration. We investigated the use of intraoperative fluorescein sodium, and compared it to frozen section assessment, for confirming pathological tissue samples in the stereotactic biopsy of gadolinium-contrast-enhancing brain lesions.

Methods

This prospective observational study consisted of 18 consecutive patients (12 men; median age, 63 years) who underwent stereotactic biopsy of gadolinium-contrast-enhancing brain lesions with intravenous fluorescein sodium administration. Twenty-three specimens were obtained and examined for the presence of fluorescence using a microscope with fluorescence visualisation capability. Positive and negative predictive values were calculated based on the fluorescence status of the biopsy samples with its corresponding intraoperative frozen section and definitive histopathological diagnosis.

Results

Nineteen specimens (83%) were fluorescent and four (17%) were non-fluorescent. All 19 fluorescent specimens were confirmed to be lesional on intraoperative frozen section assessment and were suitable for histopathological diagnosis. Three of the non-fluorescent specimens were confirmed to be lesional on intraoperative frozen section assessment. One non-fluorescent specimen was non-diagnostic on frozen section and histological assessments. The positive predictive value was 100% and the negative predictive value was 25%.

Conclusions

Fluorescein sodium fluorescence is as accurate as frozen section assessment in confirming sampling of pathological tissue in the stereotactic biopsy of gadolinium-contrast-enhancing brain lesions. Fluorescein sodium fluorescence-guided stereotactic biopsy is a useful addition to the neurosurgical armamentarium.

Keywords

Brain tumour Fluorescein sodium Fluorescence Stereotactic brain biopsy 

Notes

Funding

This research is supported by the Singapore Ministry of Health’s National Medical Research Council under its Translational and Clinical Research Flagship Programme—Tier 1 (Project number: NMRC/TCR/016-NNI/2016). They have no role in the design and conduct of this research.

Compliance with ethical standards

Conflict of interest

Dr King has received travel grant from Carl Zeiss Pte Ltd. The other authors have no personal financial or institutional interests in any of the devices, materials, or methods described in this article.

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.

References

  1. 1.
    Acerbi F, Broggi M, Eoli M, Anghileri E, Cuppini L, Pollo B, Schiariti M, Visintini S, Orsi C, Franzini A, Broggi G, Ferroli P (2013) Fluorescein-guided surgery for grade IV gliomas with a dedicated filter on the surgical microscope: preliminary results in 12 cases. Acta Neurochir 155:1277–1286CrossRefPubMedGoogle Scholar
  2. 2.
    Acerbi F, Broggi M, Eoli M, Anghileri E, Cavallo C, Boffano C, Cordella R, Cuppini L, Pollo B, Schiariti M, Visintini S, Orsi C, La Corte E, Broggi G, Ferroli P (2014) Is fluorescein-guided technique able to help in resection of high-grade gliomas? Neurosurg Focus 36:E5CrossRefPubMedGoogle Scholar
  3. 3.
    Acerbi F, Cavallo C, Broggi M, Cordella R, Anghileri E, Eoli M, Schiariti M, Broggi G, Ferroli P (2014) Fluorescein-guided surgery for malignant gliomas: a review. Neurosurg Rev 37:547–557CrossRefPubMedGoogle Scholar
  4. 4.
    Aker FV, Hakan T, Karadereler S, Erkan M (2005) Accuracy and diagnostic yield of stereotactic biopsy in the diagnosis of brain masses: comparison of results of biopsy and resected surgical specimens. Neuropathology 25:207–213CrossRefPubMedGoogle Scholar
  5. 5.
    Appin CL, Brat DJ (2014) Molecular genetics of gliomas. Cancer J 20:66–72CrossRefPubMedGoogle Scholar
  6. 6.
    Bauchet L, Zouaoui S, Darlix A, Menjot de Champfleur N, Ferreira E, Fabbro M, Kerr C, Taillandier L (2014) Assessment and treatment relevance in elderly glioblastoma patients. Neuro-Oncology 16:1459–1468CrossRefPubMedPubMedCentralGoogle Scholar
  7. 7.
    Bongetta D, Zoia C, Pugliese R, Adinolfi D, Silvani V, Gaetani P (2016) Low-cost Fluorescein detection system for high-grade Glioma surgery. World Neurosurg 88:54–58CrossRefPubMedGoogle Scholar
  8. 8.
    Catapano G, Sgulo FG, Seneca V, Lepore G, Columbano L, di Nuzzo G (2017) Fluorescein-guided surgery for high grade glioma resection: an intraoperative “contrast-enhancer”. World Neurosurg 104:239–247CrossRefPubMedGoogle Scholar
  9. 9.
    Chen B, Wang H, Ge P, Zhao J, Li W, Gu H, Wang G, Luo Y, Chen D (2012) Gross total resection of glioma with the intraoperative fluorescence-guidance of fluorescein sodium. Int J Med Sci 9:708–714CrossRefPubMedPubMedCentralGoogle Scholar
  10. 10.
    Choi YL, Suh YL, Kim D, Ko YH, Sung CO, Lee JI (2006) Malignant lymphoma of the central nervous system: difficult histologic diagnosis after glucocorticoid therapy prior to biopsy. Clin Neuropathol 25:29–36PubMedGoogle Scholar
  11. 11.
    Dammers R, Haitsma IK, Schouten JW, Kros JM, Avezaat CJ, Vincent AJ (2008) Safety and efficacy of frameless and frame-based intracranial biopsy techniques. Acta Neurochir 150:23–29CrossRefPubMedGoogle Scholar
  12. 12.
    Dammers R, Schouten JW, Haitsma IK, Vincent AJ, Kros JM, Dirven CM (2010) Towards improving the safety and diagnostic yield of stereotactic biopsy in a single centre. Acta Neurochir 152:1915–1921CrossRefPubMedPubMedCentralGoogle Scholar
  13. 13.
    Diaz RJ, Dios RR, Hattab EM, Burrell K, Rakopoulos P, Sabha N, Hawkins C, Zadeh G, Rutka JT, Cohen-Gadol AA (2015) Study of the biodistribution of fluorescein in glioma-infiltrated mouse brain and histopathological correlation of intraoperative findings in high-grade gliomas resected under fluorescein fluorescence guidance. J Neurosurg 122:1360–1369CrossRefPubMedGoogle Scholar
  14. 14.
    Dickerman RD, Mittler MA, Morgan JT (2005) Stereotactic brain biopsies and operative complications: technique to further decrease risks. Acta Neurochir 147:911–912CrossRefPubMedGoogle Scholar
  15. 15.
    Eckel-Passow JE, Lachance DH, Molinaro AM, Walsh KM, Decker PA, Sicotte H, Pekmezci M, Rice T, Kosel ML, Smirnov IV, Sarkar G, Caron AA, Kollmeyer TM, Praska CE, Chada AR, Halder C, Hansen HM, McCoy LS, Bracci PM, Marshall R, Zheng S, Reis GF, Pico AR, O’Neill BP, Buckner JC, Giannini C, Huse JT, Perry A, Tihan T, Berger MS, Chang SM, Prados MD, Wiemels J, Wiencke JK, Wrensch MR, Jenkins RB (2015) Glioma groups based on 1p/19q, IDH, and TERT promoter mutations in tumors. N Engl J Med 372:2499–2508CrossRefPubMedPubMedCentralGoogle Scholar
  16. 16.
    Hakan T, Aker FV (2016) Evaluation of 126 consecutive stereotactic procedures: brain biopsy, diagnostic yield, accuracy, non-diagnostic results, complications and follow-up. Turk Neurosurg 26:890–899PubMedGoogle Scholar
  17. 17.
    Hamamcioglu MK, Akcakaya MO, Goker B, Kasimcan MO, Kiris T (2016) The use of the YELLOW 560 nm surgical microscope filter for sodium fluorescein-guided resection of brain tumors: our preliminary results in a series of 28 patients. Clin Neurol Neurosurg 143:39–45CrossRefPubMedGoogle Scholar
  18. 18.
    Heper AO, Erden E, Savas A, Ceyhan K, Erden I, Akyar S, Kanpolat Y (2005) An analysis of stereotactic biopsy of brain tumors and nonneoplastic lesions: a prospective clinicopathologic study. Surg Neurol 64(Suppl 2):S82–S88CrossRefPubMedGoogle Scholar
  19. 19.
    Hohne J, Brawanski A, Schebesch KM (2017) Fluorescence-guided surgery of brain abscesses. Clin Neurol Neurosurg 155:36–39CrossRefPubMedGoogle Scholar
  20. 20.
    Hohne J, Hohenberger C, Proescholdt M, Riemenschneider MJ, Wendl C, Brawanski A, Schebesch KM (2017) Fluorescein sodium-guided resection of cerebral metastases-an update. Acta Neurochir 159:363–367CrossRefPubMedGoogle Scholar
  21. 21.
    Ichikawa T, Suzuki K, Watanabe Y, Sato T, Sakuma J, Saito K (2016) Development of and clinical experience with a simple device for performing intraoperative fluorescein fluorescence cerebral angiography: technical notes. Neurol Med Chir (Tokyo) 56:141–149CrossRefGoogle Scholar
  22. 22.
    Jackson RJ, Fuller GN, Abi-Said D, Lang FF, Gokaslan ZL, Shi WM, Wildrick DM, Sawaya R (2001) Limitations of stereotactic biopsy in the initial management of gliomas. Neuro-Oncology 3:193–200CrossRefPubMedPubMedCentralGoogle Scholar
  23. 23.
    Jain D, Sharma MC, Sarkar C, Deb P, Gupta D, Mahapatra AK (2006) Correlation of diagnostic yield of stereotactic brain biopsy with number of biopsy bits and site of the lesion. Brain Tumor Pathol 23:71–75CrossRefPubMedGoogle Scholar
  24. 24.
    Kellermann SG, Hamisch CA, Hafkemeyer V, Rueß D, Grau SJ, Ruge MI (2016) Stereotactic biopsy in elderly patients: risk assessment and impact on treatment decision. Neuro Oncol 18:iv83Google Scholar
  25. 25.
    Kickingereder P, Willeit P, Simon T, Ruge MI (2013) Diagnostic value and safety of stereotactic biopsy for brainstem tumors: a systematic review and meta-analysis of 1480 cases. Neurosurgery 72:873–881 discussion 882; quiz 882 CrossRefPubMedGoogle Scholar
  26. 26.
    Kim JE, Kim DG, Paek SH, Jung HW (2003) Stereotactic biopsy for intracranial lesions: reliability and its impact on the planning of treatment. Acta Neurochir 145:547–554 discussion 554-545 CrossRefPubMedGoogle Scholar
  27. 27.
    Koc K, Anik I, Cabuk B, Ceylan S (2008) Fluorescein sodium-guided surgery in glioblastoma multiforme: a prospective evaluation. Br J Neurosurg 22:99–103CrossRefPubMedGoogle Scholar
  28. 28.
    Kondziolka D, Firlik A, Lunsford L (1998) Complications of stereotactic brain surgery. Neurol Clin 16:35–54CrossRefPubMedGoogle Scholar
  29. 29.
    Kulkarni AV, Guha A, Lozano A, Bernstein M (1998) Incidence of silent hemorrhage and delayed deterioration after stereotactic brain biopsy. J Neurosurg 89:31–35CrossRefPubMedGoogle Scholar
  30. 30.
    Li Y, Rey-Dios R, Roberts DW, Valdes PA, Cohen-Gadol AA (2014) Intraoperative fluorescence-guided resection of high-grade gliomas: a comparison of the present techniques and evolution of future strategies. World Neurosurg 82:175–185CrossRefPubMedGoogle Scholar
  31. 31.
    Lovato RM, Vitorino Araujo JL, Esteves Veiga JC (2017) Low-cost device for fluorescein guided surgery in malignant brain tumor. World Neurosurg 104:61–67CrossRefPubMedGoogle Scholar
  32. 32.
    Murray KJ (1982) Improved surgical resection of human brain tumors: part I. A preliminary study. Surg Neurol 17:316–319CrossRefPubMedGoogle Scholar
  33. 33.
    Neira JA, Ung TH, Sims JS, Malone HR, Chow DS, Samanamud JL, Zanazzi GJ, Guo X, Bowden SG, Zhao B, Sheth SA, McKhann GM 2nd, Sisti MB, Canoll P, D’Amico RS, Bruce JN (2016) Aggressive resection at the infiltrative margins of glioblastoma facilitated by intraoperative fluorescein guidance. J Neurosurg 127:111–122CrossRefPubMedGoogle Scholar
  34. 34.
    Onder E, Arikok AT, Onder S, Han U, Sorar M, Kertmen H, Yilmaz ED, Fesli R, Alper M (2015) Corticosteroid pre-treated primary CNS lymphoma: a detailed analysis of stereotactic biopsy findings and consideration of interobserver variability. Int J Clin Exp Pathol 8:7798–7808PubMedPubMedCentralGoogle Scholar
  35. 35.
    Pulhorn H, Quigley DG, Bosma JJ, Kirollos R, du Plessis DG, Jenkinson MD (2008) Impact of brain biopsy on the management of patients with nonneoplastic undiagnosed neurological disorders. Neurosurgery 62:833–837 discussion 837-838 CrossRefPubMedGoogle Scholar
  36. 36.
    Quick-Weller J, Tichy J, Dinc N, Tritt S, Won SY, Behmanesh B, Bruder M, Seifert V, Weise LM, Marquardt G (2017) Benefit and complications of frame-based stereotactic biopsy in old and very old patients. World Neurosurg 102:442–448CrossRefPubMedGoogle Scholar
  37. 37.
    Rey-Dios R, Cohen-Gadol AA (2013) Technical principles and neurosurgical applications of fluorescein fluorescence using a microscope-integrated fluorescence module. Acta Neurochir 155:701–706CrossRefPubMedGoogle Scholar
  38. 38.
    Rey-Dios R, Hattab EM, Cohen-Gadol AA (2014) Use of intraoperative fluorescein sodium fluorescence to improve the accuracy of tissue diagnosis during stereotactic needle biopsy of high-grade gliomas. Acta Neurochir 156:1071–1075 discussion 1075 CrossRefPubMedGoogle Scholar
  39. 39.
    Schebesch KM, Proescholdt M, Hohne J, Hohenberger C, Hansen E, Riemenschneider MJ, Ullrich W, Doenitz C, Schlaier J, Lange M, Brawanski A (2013) Sodium fluorescein-guided resection under the YELLOW 560 nm surgical microscope filter in malignant brain tumor surgery—a feasibility study. Acta Neurochir 155:693–699CrossRefPubMedGoogle Scholar
  40. 40.
    Schebesch KM, Hoehne J, Hohenberger C, Acerbi F, Broggi M, Proescholdt M, Wendl C, Riemenschneider MJ, Brawanski A (2015) Fluorescein sodium-guided surgery in cerebral lymphoma. Clin Neurol Neurosurg 139:125–128CrossRefPubMedGoogle Scholar
  41. 41.
    Schebesch KM, Hoehne J, Hohenberger C, Proescholdt M, Riemenschneider MJ, Wendl C, Brawanski A (2015) Fluorescein sodium-guided resection of cerebral metastases-experience with the first 30 patients. Acta Neurochir 157:899–904CrossRefPubMedGoogle Scholar
  42. 42.
    Schebesch KM, Brawanski A, Hohenberger C, Hohne J (2016) Fluorescein sodium-guided surgery of malignant brain Tumors: history, current concepts, and future project. Turk Neurosurg 26:185–194PubMedGoogle Scholar
  43. 43.
    Shastri-Hurst N, Tsegaye M, Robson DK, Lowe JS, Macarthur DC (2006) Stereotactic brain biopsy: an audit of sampling reliability in a clinical case series. Br J Neurosurg 20:222–226CrossRefPubMedGoogle Scholar
  44. 44.
    Shooman D, Belli A, Grundy PL (2010) Image-guided frameless stereotactic biopsy without intraoperative neuropathological examination. J Neurosurg 113:170–178CrossRefPubMedGoogle Scholar
  45. 45.
    Theeler BJ, Yung WK, Fuller GN, De Groot JF (2012) Moving toward molecular classification of diffuse gliomas in adults. Neurology 79:1917–1926CrossRefPubMedPubMedCentralGoogle Scholar
  46. 46.
    Thien A, Rao JP, Ng WH, King NK (2017) The Fluoropen: a simple low-cost device to detect intraoperative fluorescein fluorescence in stereotactic needle biopsy of brain tumors. Acta Neurochir 159:371–375CrossRefPubMedGoogle Scholar
  47. 47.
    Tilgner J, Herr M, Ostertag C, Volk B (2005) Validation of intraoperative diagnoses using smear preparations from stereotactic brain biopsies: intraoperative versus final diagnosis--influence of clinical factors. Neurosurgery 56:257–265CrossRefPubMedGoogle Scholar
  48. 48.
    von Campe G, Moschopulos M, Hefti M (2012) 5-Aminolevulinic acid-induced protoporphyrin IX fluorescence as immediate intraoperative indicator to improve the safety of malignant or high-grade brain tumor diagnosis in frameless stereotactic biopsies. Acta Neurochir 154:585–588 discussion 588 CrossRefGoogle Scholar
  49. 49.
    Weller M, Stupp R, Hegi ME, van den Bent M, Tonn JC, Sanson M, Wick W, Reifenberger G (2012) Personalized care in neuro-oncology coming of age: why we need MGMT and 1p/19q testing for malignant glioma patients in clinical practice. Neuro Oncol 14(Suppl 4):iv100-iv108Google Scholar
  50. 50.
    Widhalm G, Minchev G, Woehrer A, Preusser M, Kiesel B, Furtner J, Mert A, Di Ieva A, Tomanek B, Prayer D, Marosi C, Hainfellner JA, Knosp E, Wolfsberger S (2012) Strong 5-aminolevulinic acid-induced fluorescence is a novel intraoperative marker for representative tissue samples in stereotactic brain tumor biopsies. Neurosurg Rev 35:381–391 discussion 391 CrossRefPubMedGoogle Scholar
  51. 51.
    Zaki HS, Jenkinson MD, Du Plessis DG, Smith T, Rainov NG (2004) Vanishing contrast enhancement in malignant glioma after corticosteroid treatment. Acta Neurochir 146:841–845CrossRefPubMedGoogle Scholar
  52. 52.
    Zoeller GK, Benveniste RJ, Landy H, Morcos JJ, Jagid J (2009) Outcomes and management strategies after nondiagnostic stereotactic biopsies of brain lesions. Stereotact Funct Neurosurg 87:174–181CrossRefPubMedGoogle Scholar

Copyright information

© Springer-Verlag GmbH Austria, part of Springer Nature 2017

Authors and Affiliations

  • Ady Thien
    • 1
  • Julian Xinguang Han
    • 1
  • Krishan Kumar
    • 1
  • Yew Poh Ng
    • 1
  • Jai Prashanth Rao
    • 1
  • Wai Hoe Ng
    • 1
  • Nicolas Kon Kam King
    • 1
  1. 1.Department of NeurosurgeryNational Neuroscience InstituteSingaporeSingapore

Personalised recommendations