Quantitative fluorescence using 5-aminolevulinic acid-induced protoporphyrin IX biomarker as a surgical adjunct in low-grade glioma surgery

Journal of Neurosurgery

Volumn 123, Issue 3, 2015, Pages 771-780

  Valdés, Pablo A ^a,b,c,d   Jacobs, Valerie ^b,e   Harris, Brent T ^f   Wilson, Brian C ^g   Leblond, Frederic ^h   Paulsen, Keith D ^d   Roberts, David W ^b,c  

^a BRIGHAM AND WOMEN S HOSPITAL   (United States)

^b DARTMOUTH MEDICAL SCHOOL   (United States)

^c DARTMOUTH HITCHCOCK MEDICAL CENTER   (United States)

^d DARTMOUTH COLLEGE   (United States)

^e BOSTON CHILDREN S HOSPITAL   (United States)

^f GEORGETOWN UNIVERSITY MEDICAL CENTER   (United States)

^g UNIVERSITY OF TORONTO   (Canada)

^h ÉCOLE POLYTECHNIQUE DE MONTRÉAL   (Canada)

Author keywords

5 aminolevulinic acid; Biomedical optics; Brain tumor; Fluorescence guided surgery; Low grade glioma; Oncology; Optical spectroscopy; Protoporphyrin IX; Quantitative fluorescence

Indexed keywords

AMINOLEVULINIC ACID; PROTOPORPHYRIN; BIOLOGICAL MARKER; PHOTOSENSITIZING AGENT;

ARTICLE; ASTROCYTOMA; CLINICAL ARTICLE; CONTRAST ENHANCEMENT; DIAGNOSTIC ACCURACY; DIAGNOSTIC TEST ACCURACY STUDY; EPENDYMOMA; FLUORESCENCE IMAGING; GLIOMA; HISTOPATHOLOGY; HUMAN; HUMAN TISSUE; NEUROSURGERY; OLIGODENDROGLIOMA; PLEOMORPHIC XANTHOASTROCYTOMA; PREDICTIVE VALUE; PRIORITY JOURNAL; QUALITATIVE ANALYSIS; QUANTITATIVE ANALYSIS; SURVIVAL; TREATMENT OUTCOME; ADULT; AGED; BRAIN NEOPLASMS; FEMALE; FLUORESCENCE; MALE; METABOLISM; MIDDLE AGED; NEURONAVIGATION; PROCEDURES;

ADULT; AGED; AMINOLEVULINIC ACID; BIOMARKERS; BRAIN NEOPLASMS; FEMALE; FLUORESCENCE; GLIOMA; HUMANS; MALE; MIDDLE AGED; NEURONAVIGATION; PHOTOSENSITIZING AGENTS; PROTOPORPHYRINS;

EID: 84965088620     PISSN: 00223085     EISSN: 19330693     Source Type: Journal    
DOI: 10.3171/2014.12.JNS14391     Document Type: Article

References (52)

1. Beez T, Sarikaya-Seiwert S, Steiger HJ, Hänggi D: Fluorescence-guided surgery with 5-aminolevulinic acid for resection of brain tumors in children-a technical report. Acta Neurochir (Wien) 156:597-604, 2014
2. Bekelis K, Valdés PA, Erkmen K, Leblond F, Kim A, Wilson BC, et al: Quantitative and qualitative 5-aminolevulinic acidinduced protoporphyrin IX fluorescence in skull base meningiomas. Neurosurg Focus 30(5):E8, 2011
3. Bradley RS, Thorniley MS: A review of attenuation correction techniques for tissue fluorescence. J R Soc Interface 3:1-13, 2006
4. Colditz MJ, Jeffree RL: Aminolevulinic acid (ALA)-protoporphyrin IX fluorescence guided tumour resection. Part 1: Clinical, radiological and pathological studies. J Clin Neurosci 19:1471-1474, 2012
5. Colditz MJ, Leyen Kv, Jeffree RL: Aminolevulinic acid (ALA)-protoporphyrin IX fluorescence guided tumour resection. Part 2: theoretical, biochemical and practical aspects. J Clin Neurosci 19:1611-1616, 2012
6. DeAngelis LM: Brain tumors. N Engl J Med 344:114-123, 2001
7. Ewelt C, Floeth FW, Felsberg J, Steiger HJ, Sabel M, Langen KJ, et al: FinDing the anaplastic focus in diffuse gliomas: the value of Gd-DTPA enhanced MRI, FET-PET, and intraoperative, ALA-derived tissue fluorescence. Clin Neurol Neurosurg 113:541-547, 2011
8. Fitzmaurice GM, Laird NM, Ware JH: Applied Longitudinal Analysis. Hoboken, NJ: Wiley, 2004
9. Fitzmaurice M: Principles and pitfalls of diagnostic test de-velopment: implications for spectroscopic tissue diagnosis. J Biomed Opt 5:119-130, 2000
10. Floeth FW, Sabel M, Ewelt C, Stummer W, Felsberg J, Reifenberger G, et al: Comparison of (18)F-FET PET and 5-ALA fluorescence in cerebral gliomas. Eur J Nucl Med Mol Imaging 38:731-741, 2011
11. Floeth FW, Stummer W: The value of metabolic imaging in diagnosis and resection of cerebral gliomas. Nat Clin Pract Neurol 1:62-63, 2005
12. Haj-Hosseini N, Richter J, Andersson-Engels S, Wårdell K: Optical touch pointer for fluorescence guided glioblastoma resection using 5-aminolevulinic acid. Lasers Surg Med 42:9-14, 2010
13. Hefti M, von Campe G, Moschopulos M, Siegner A, Looser H, Landolt H: 5-aminolevulinic acid induced protoporphyrin IX fluorescence in high-grade glioma surgery: a one-year experience at a single institution. Swiss Med Wkly 138:180-185, 2008
14. Hirose Y, Sasaki H, Abe M, Hattori N, Adachi K, Nishiyama Y, et al: Subgrouping of gliomas on the basis of genetic profiles. Brain Tumor Pathol 30:203-208, 2013
15. Ishihara R, Katayama Y, Watanabe T, Yoshino A, Fukushima T, Sakatani K: Quantitative spectroscopic analysis of 5-aminolevulinic acid-induced protoporphyrin IX fluorescence intensity in diffusely infiltrating astrocytomas. Neurol Med Chir (Tokyo) 47:53-57, 2007
16. Kim A, Khurana M, Moriyama Y, Wilson BC: Quantification of in vivo fluorescence decoupled from the effects of tissue optical properties using fiber-optic spectroscopy measurements. J Biomed Opt 15:067006, 2010
17. Marbacher S, Klinger E, Schwyzer L, Fischer I, Nevzati E, Diepers M, et al: Use of fluorescence to guide resection or biopsy of primary brain tumors and brain metastases. Neurosurg Focus 36(2):E10, 2014
18. McGirt MJ, Chaichana KL, Attenello FJ, Weingart JD, Than K, Burger PC, et al: Extent of surgical resection is independently associated with survival in patients with hemispheric infiltrating low-grade gliomas. Neurosurgery 63:700-708, 2008
19. Millesi M, Kiesel B, Woehrer A, Hainfellner JA, Novak K, Martínez-Moreno M, et al: Analysis of 5-aminolevulinic acid-induced fluorescence in 55 different spinal tumors. Neurosurg Focus 36(2):E11, 2014
20. Montcel B, Mahieu-Williame L, Armoiry X, Meyronet D, Guyotat J: Two-peaked 5-ALA-induced PpIX fluorescence emission spectrum distinguishes glioblastomas from low grade gliomas and infiltrative component of glioblastomas. Biomed Opt Express 4:548-558, 2013
21. Nabavi A, Thurm H, Zountsas B, Pietsch T, Lanfermann H, Pichlmeier U, et al: Five-aminolevulinic acid for fluorescence-guided resection of recurrent malignant gliomas: a phase II study. Neurosurgery 65:1070-1077, 2009
22. Nakazato Y: [Revised WHO classification of brain tumours.] Brain Nerve 60:59-77, 2008 (Jpn)
23. Pichlmeier U, Bink A, Schackert G, Stummer W: Resection and survival in glioblastoma multiforme: an RTOG recursive partitioning analysis of ALA study patients. Neuro Oncol 10:1025-1034, 2008
24. Pogue BW, Gibbs-Strauss S, Valdés PA, Samkoe K, Roberts DW, Paulsen KD: Review of neurosurgical fluorescence imaging methodologies. IEEE J Sel Top Quantum Electron 16:493-505, 2010
25. Richards-Kortum R, Sevick-Muraca E: Quantitative optical spectroscopy for tissue diagnosis. Annu Rev Phys Chem 47:555-606, 1996
26. Roberts DW, Valdés PA, Harris BT, Fontaine KM, Hartov A, Fan X, et al: Coregistered fluorescence-enhanced tumor resection of malignant glioma: relationships between daminolevulinic acid-induced protoporphyrin IX fluorescence, magnetic resonance imaging enhancement, and neuropathological parameters. Clinical article. J Neurosurg 114:595-603, 2011
27. Roberts DW, Valdés PA, Harris BT, Hartov A, Fan X, Ji S, et al: Adjuncts for maximizing resection: 5-aminolevuinic acid. Clin Neurosurg 59:75-78, 2012
28. Roberts DW, Valdés PA, Harris BT, Hartov A, Fan X, Ji S, et al: Glioblastoma multiforme treatment with clinical trials for surgical resection (aminolevulinic acid). Neurosurg Clin N Am 23:371-377, 2012
29. Ruge JR, Liu J: Use of 5-aminolevulinic acid for visualization and resection of a benign pediatric brain tumor. J Neurosurg Pediatr 4:484-486, 2009
30. Sanai N, Snyder LA, Honea NJ, Coons SW, Eschbacher JM, Smith KA, et al: Intraoperative confocal microscopy in the visualization of 5-aminolevulinic acid fluorescence in lowgrade gliomas. J Neurosurg 115:740-748, 2011
31. Schomas DA, Laack NN, Rao RD, Meyer FB, Shaw EG, O'Neill BP, et al: Intracranial low-grade gliomas in adults: 30-year experience with long-term follow-up at Mayo Clinic. Neuro Oncol 11:437-445, 2009
32. Shapiro DE: The interpretation of diagnostic tests. Stat Methods Med Res 8:113-134, 1999
33. Smith JS, Chang EF, Lamborn KR, Chang SM, Prados MD, Cha S, et al: Role of extent of resection in the long-term outcome of low-grade hemispheric gliomas. J Clin Oncol 26:1338-1345, 2008
34. Stockhammer F, Misch M, Horn P, Koch A, Fonyuy N, Plotkin M: Association of F18-fluoro-ethyl-tyrosin uptake and 5-aminolevulinic acid-induced fluorescence in gliomas. Acta Neurochir (Wien) 151:1377-1383, 2009
35. Stummer W, Novotny A, Stepp H, Goetz C, Bise K, Reulen HJ: Fluorescence-guided resection of glioblastoma multiforme by using 5-aminolevulinic acid-induced porphyrins: a prospective study in 52 consecutive patients. J Neurosurg 93:1003-1013, 2000
36. Stummer W, Pichlmeier U, Meinel T, Wiestler OD, Zanella F, Reulen HJ: Fluorescence-guided surgery with 5-aminolevulinic acid for resection of malignant glioma: a randomised controlled multicentre phase III trial. Lancet Oncol 7:392-401, 2006
37. Stummer W, Reulen HJ, Meinel T, Pichlmeier U, Schumacher W, Tonn JC, et al: Extent of resection and survival in glioblastoma multiforme: identification of and adjustment for bias. Neurosurgery 62:564-576, 2008
38. Stummer W, Stepp H, Möller G, Ehrhardt A, Leonhard M, Reulen HJ: Technical principles for protoporphyrin-IX-fluorescence guided microsurgical resection of malignant glioma tissue. Acta Neurochir (Wien) 140:995-1000, 1998
39. Stummer W, Tonn JC, Goetz C, Ullrich W, Stepp H, Bink A, et al: 5-ALA-derived tumor fluorescence: the diagnostic accuracy of visible fluorescence qualities as corroborated by spectrometry and histology and post-operative imaging. Neurosurgery 74:310-319, 2013
40. Stummer W, Tonn JC, Mehdorn HM, Nestler U, Franz K, Goetz C, et al: Counterbalancing risks and gains from extended resections in malignant glioma surgery: a supplemental analysis from the randomized 5-aminolevulinic acid glioma resection study. J Neurosurg 114:613-623, 2011
41. Utsuki S, Oka H, Sato S, Suzuki S, Shimizu S, Tanaka S, et al: Possibility of using laser spectroscopy for the intraoperative detection of nonfluorescing brain tumors and the boundaries of brain tumor infiltrates. Technical note. J Neurosurg 104:618-620, 2006
42. Valdés PA, Bekelis K, Harris BT, Wilson BC, Leblond F, Kim A, et al: 5-Aminolevulinic acid-induced protoporphyrin IX fluorescence in meningioma: qualitative and quantitative measurements in vivo. Neurosurgery 10 (Suppl 1):74-83, 2014
43. Valdés PA, Fan X, Ji S, Harris BT, Paulsen KD, Roberts DW: Estimation of brain deformation for volumetric image updating in protoporphyrin IX fluorescence-guided resection. Stereotact Funct Neurosurg 88:1-10, 2010
44. Valdés PA, Leblond F, Jacobs VL, Paulsen KD, Roberts DW,: In vivo fluorescence detection in surgery: A review of principles, methods, and applications. Curr Med Imaging Rev 8:211-232, 2012
45. Valdés PA, Jacobs VL, Wilson BC, Leblond F, Roberts DW, Paulsen KD: System and methods for wide-field quantitative fluorescence imaging during neurosurgery. Opt Lett 38:2786-2788, 2013
46. Valdés PA, Kim A, Brantsch M, Niu C, Moses ZB, Tosteson TD, et al: d-aminolevulinic acid-induced protoporphyrin IX concentration correlates with histopathologic markers of malignancy in human gliomas: the need for quantitative fluorescence-guided resection to identify regions of increasing malignancy. Neuro Oncol 13:846-856, 2011
47. Valdés PA, Kim A, Leblond F, Conde OM, Harris BT, Paulsen KD, et al: Combined fluorescence and reflectance spectroscopy for in vivo quantification of cancer biomarkers in low-and high-grade glioma surgery. J Biomed Opt 16:116007, 2011
48. Valdés PA, Leblond F, Jacobs VL, Wilson BC, Paulsen KD, Roberts DW: Quantitative, spectrally-resolved intraoperative fluorescence imaging. Sci Rep 2:798, 2012
49. Valdés PA, Leblond F, Kim A, Harris BT, Wilson BC, Fan X, et al: Quantitative fluorescence in intracranial tumor: implications for ALA-induced PpIX as an intraoperative biomarker. J Neurosurg 115:11-17, 2011
50. Valdés PA, Leblond F, Kim A, Wilson BC, Paulsen KD, Roberts DW: A spectrally constrained dual-band normalization technique for protoporphyrin IX quantification in fluorescence-guided surgery. Opt Lett 37:1817-1819, 2012
51. Weissleder R, Pittet MJ: Imaging in the era of molecular oncology. Nature 452:580-589, 2008
52. Widhalm G, Wolfsberger S, Minchev G, Woehrer A, Krssak M, Czech T, et al: 5-aminolevulinic acid is a promising marker for detection of anaplastic foci in diffusely infiltrating gliomas with nonsignificant contrast enhancement. Cancer 116:1545-1552, 2010