Review of neurosurgical fluorescence imaging methodologies

IEEE Journal on Selected Topics in Quantum Electronics

Volumn 16, Issue 3, 2010, Pages 493-505

  Pogue, Brian W ^a,b   Gibbs Strauss, Summer L ^c   Valdés, Pablo A ^a   Samkoe, Kimberley S ^a   Roberts, David W ^b   Paulsen, Keith D ^a,b  

^a DARTMOUTH COLLEGE   (United States)

^b DARTMOUTH MEDICAL SCHOOL   (United States)

^c HARVARD MEDICAL SCHOOL   (United States)

Author keywords

Brain tumor; Fluorescence; Glioma; Imaging; Microscopy; Neurosurgery; Protoporphyrin; Surgery

Indexed keywords

BRAIN TUMOR; BRAIN TUMORS; GLIOMA; IMAGING MICROSCOPY; MICROSCOPY; PROTOPORPHYRINS;

EXPERIMENTS; NEUROSURGERY; PROBES; TUMORS;

FLUORESCENCE;

EID: 77953291973     PISSN: 1077260X     EISSN: None     Source Type: Journal    
DOI: 10.1109/JSTQE.2009.2034541     Document Type: Article

References (137)

1. G. E. Moore et al., "The clinical use of fluorescein in neurosurgery; the localization of brain tumors," J. Neurosurg., vol.5, pp. 392-398, Jul. 1948.
2. R. Richards-Kortum et al., "Spectroscopic diagnosis of colonic dysplasia," Photochem. Photobiol., vol.53, pp. 777-786, Jun. 1991.
3. N. Ramanujam et al., "Fluorescence spectroscopy: A diagnostic tool for cervical intraepithelial neoplasia (CIN)," Gynecol. Oncol., vol.52, pp. 31-38, Jan. 1994. (Pubitemid 24066849)
4. I. Georgakoudi et al., "NAD(P)H and collagen as in vivo quantitative fluorescent biomarkers of epithelial precancerous changes," Cancer Res., vol.62, pp. 682-687, Feb. 2002.
5. A. C. Croce et al., "Diagnostic potential of autofluorescence for an assisted intraoperative delineation of glioblastoma resection margins," Photochem. Photobiol., vol.77, pp. 309-318, 2003.
6. R. S. DaCosta et al., "Molecular fluorescence excitationemission matrices relevant to tissue spectroscopy," Photochem. Photobiol., vol.78, pp. 384-392, 2003.
7. W. H. Yong et al., "Distinction of brain tissue, low grade and high grade glioma with time-resolved fluorescence spectroscopy," Frontiers Biosci., vol.11, pp. 1255-1263, 2006.
8. W. C. Lin et al., "In vivo brain tumor demarcation using optical spectroscopy," Photochem. Photobiol., vol.73, pp. 396-402, Apr. 2001.
9. S. A. Toms et al., "Intraoperative optical spectroscopy identifies infiltrating glioma margins with high sensitivity," Neurosurgery, vol.57, pp. 382-391, Oct. 2005.
10. S. A. Friesen et al., "5-Aminolevulinic acid-based photodynamic detection and therapy of brain tumors (review)," Int. J. Oncol., vol.21, pp. 577-582, 2002.
11. J. C. Kennedy et al., "Photodynamic therapy (PDT) and photodiagnosis (PD) using endogenous photosensitization induced by 5-aminolevulinic acid (ALA): Mechanisms and clinical results," J. Clin. Laser Med. Surg., vol.14, pp. 289-304, 1996.
12. S. Collaud et al., "On the selectivity of 5-aminolevulinic acid-induced protoporphyrin IX formation," Curr. Med. Chem. Anti Cancer Agents, vol.4, pp. 301-316, 2004.
13. Q. Peng et al., "5-Aminolevulinic acid-based photodynamic therapy. Clinical research and future challenges," Cancer, vol.79, pp. 2282-2308, 1997. (Pubitemid 27251011)
14. A. Bogaards et al., "Increased brain tumor resection using fluorescence image guidance in a preclinical model," Lasers Surg. Med., vol.35, pp. 181-190, 2004.
15. M. Olivo and B. C. Wilson, "Mapping ALA-induced PPIX fluorescence in normal brain and brain tumour using confocal fluorescence microscopy," Int. J. Oncol., vol.25, pp. 37-45, 2004.
16. W. Stummer et al., "Fluorescence-guided resection of glioblastoma multiforme by using 5-aminolevulinic acid-induced porphyrins: A prospective study in 52 consecutive patients," J. Neurosurg., vol.93, pp. 1003-1013, Dec. 2000.
17. W. Stummer et al., "Fluorescence-guided surgery with 5-aminolevulinic acid for resection of malignant glioma: A randomised controlled multicentre phase III trial," Lancet Oncol., vol.7, pp. 392-401, May 2006.
18. K. M. Hebeda et al., "5-Aminolevulinic acid induced endogenous porphyrin fluorescence in 9L and C6 brain tumours and in the normal rat brain.[erratum appears in Acta Neurochir (Wien) 1998:140(8):881]," Acta Neurochir., vol.140, pp. 503-512, 1998.
19. M. B. Ericson et al., "Photodynamic therapy of actinic keratosis at varying fluence rates: Assessment of photobleaching, pain and primary clinical outcome," Br. J. Dermatol., vol.151, pp. 1204-1212, 2004.
20. A. K. Gupta and J. E. Ryder, "Photodynamic therapy and topical aminolevulinic acid an overview," Amer. J. Clin. Dermatol., vol.4, pp. 699-708, 2003.
21. C. J. Kelty et al., "The use of 5-aminolaevulinic acid as a photosensitiser in photodynamic therapy and photodiagnosis," Photochem. Photobiol. Sci., vol.1, pp. 158-168, 2002.
22. M. T. Truong, "Current role of radiation therapy in the management of malignant brain tumors," Hematol. Oncol. Clin. N. Amer., vol.20, pp. 431-453, 2006.
23. J. Tuettenberg et al., "Angiogenesis in malignant glioma-A target for antitumor therapy?," Crit. Rev. Oncol. Hematol., vol.59, pp. 181-193, 2006.
24. W. Stummer et al., "Intraoperative detection of malignant gliomas by 5-aminolevulinic acid-induced porphyrin fluorescence," Neurosurgery, vol.42, pp. 518-525, Mar. 1998.
25. S. B. Brown et al., "The present and future role of photodynamic therapy in cancer treatment," Lancet Oncol., vol.5, pp. 497-508, 2004.
26. P. Hinnen et al., "Biochemical basis of 5-aminolaevulinic acid-induced protoporphyrin IX accumulation: Astudy in patients with (pre)malignant lesions of the oesophagus," Br. J. Cancer, vol.78, pp. 679-682, 1998.
27. R. Hilf et al., "Effect of delta-aminolevulinic acid on protoporphyrin IX accumulation in tumor cells transfected with plasmids containing porphobilinogen deaminase DNA," Photochem. Photobiol., vol.70, pp. 334-340, 1999.
28. S. L. Gibson et al., "A regulatory role for porphobilinogen deaminase (PBGD) in delta-aminolaevulinic acid (delta-ALA)-induced photosensitization?," Br. J. Cancer, vol.77, pp. 235-243, 1998.
29. R. C. Krieg et al., "Cell-type specific protoporphyrin IX metabolism in human bladder cancer in vitro," Photochem. Photobiol., vol.72, pp. 226-233, 2000.
30. S. L. Gibson et al., "Is delta-aminolevulinic acid dehydratase rate limiting in heme biosynthesis following exposure of cells to deltaaminolevulinic acid?," Photochem. Photobiol., vol.73, pp. 312-317, 2001.
31. S. L. Gibson et al., "Relationship of delta-aminolevulinic acid-induced protoporphyrin IX levels to mitochondrial content in neoplastic cells in vitro," Biochem. Biophys. Res. Commun., vol.265, pp. 315-321, 1999.
32. O. Bech et al., "The pH dependency of protoporphyrin IX formation in cells incubated with 5-aminolevulinic acid," Cancer Lett., vol.113, pp. 25-29, 1997. (Pubitemid 27113224)
33. S. C. Chang et al., "The efficacy of an iron chelator (CP94) in increasing cellular protoporphyrin IX following intravesical 5-aminolaevulinic acid administration: An in vivo study," J. Photochem. Photobiol. B Biol., vol.38, pp. 114-122, 1997.
34. A. K. Sinha et al., "Methotrexate used in combination with aminolaevulinic acid for photodynamic killing of prostate cancer cells," Br. J. Cancer, vol.95, pp. 485-495, Aug. 2006.
35. S. L. Gibson et al., "Time-dependent intracellular accumulation of deltaaminolevulinic acid, induction of porphyrin synthesis and subsequent phototoxicity," Photochem. Photobiol., vol.65, pp. 416-421, 1997.
36. M. B. Moretti et al., "Delta-aminolevulinic acid transport in murine mammary adenocarcinoma cells is mediated by beta transporters," Br. J. Cancer, vol.87, pp. 471-474, 2002.
37. S. C. Garcia et al., "Mechanistic studies on delta-aminolevulinic acid uptake and efflux in a mammary adenocarcinoma cell line," Br. J.Cancer, vol.89, pp. 173-177, 2003.
38. L. Wyld et al., "Factors affecting aminolaevulinic acid-induced generation of protoporphyrin IX," Br. J. Cancer, vol.76, pp. 705-712, 1997.
39. H. Liang et al., "Subcellular phototoxicity of 5-aminolaevulinic acid (ALA)," Lasers Surg. Med., vol.22, pp. 14-24, 1998.
40. J. Moan et al., "Protoporphyrin IX accumulation in cells treated with 5-aminolevulinic acid: Dependence on cell density, cell size and cell cycle," Int. J. Cancer, vol.75, pp. 134-139, 1998.
41. S. L. Gibbs et al., "Protoporphyrin IX level correlates with number of mitochondria, but increase in production correlates with tumor cell size," Photochem. Photobiol., vol.82, pp. 1334-1341, Sep./Oct. 2006.
42. K. Berg et al., "The influence of iron chelators on the accumulation of protoporphyrin IX in 5-aminolaevulinic acid-treated cells," Br. J. Cancer, vol.74, pp. 688-697, Sep. 1996.
43. B. Ortel et al., "Differentiation-specific increase in ALA-induced protoporphyrin IX accumulation in primary mouse keratinocytes," Br. J. Cancer, vol.77, pp. 1744-1751, Jun. 1998.
44. A. Pye et al., "Enhancement of methyl-aminolevulinate photodynamic therapy by iron chelation with CP94: An in vitro investigation and clinical dose-escalating safety study for the treatment of nodular basal cell carcinoma," J. Cancer Res. Clin. Oncol., vol.134, pp. 841-849, Aug. 2008.
45. B. Ortel et al., "Differentiation enhances aminolevulinic acid-dependent photodynamic treatment of LNCaP prostate cancer cells," Br. J. Cancer, vol.87, pp. 1321-1327, Nov. 2002.
46. N. Sato et al., "Vitamin D enhances ALA-induced protoporphyrin IX production and photodynamic cell death in 3-D organotypic cultures of keratinocytes," J. Invest. Dermatol., vol.127, pp. 925-934, Apr. 2007.
47. C. Pourzand et al., "The iron regulatory protein can determine the effectiveness of 5-aminolevulinic acid in inducing protoporphyrin IX in human primary skin fibroblasts," J. Invest. Dermatol., vol.112, pp. 419-425, Apr. 1999.
48. L. Wyld et al., "Aminolaevulinic acid-induced photodynamic therapy: Cellular responses to glucose starvation," Br. J. Cancer, vol.86, pp. 1343-1347, 2002.
49. L. Wyld et al., "The influence of hypoxia and pH on aminolaevulinic acid-induced photodynamic therapy in bladder cancer cells in vitro," Br. J. Cancer, vol.77, pp. 1621-1627, 1998.
50. I. Georgakoudi et al., "Hypoxia significantly reduces aminolaevulinic acid-induced protoporphyrin IX synthesis in EMT6 cells," Br. J. Cancer, vol.79, pp. 1372-1377, 1999.
51. L. Wyld et al., "Cell cycle phase influences tumour cell sensitivity to aminolaevulinic acid-induced photodynamic therapy in vitro," Br. J. Cancer, vol.78, pp. 50-55, 1998.
52. D. I. Schwartz et al., "Differentiation-dependent photodynamic therapy regulated by porphobilinogen deaminase in B16 melanoma," Br. J. Cancer, vol.90, pp. 1833-1841, 2004.
53. P. Kremer et al., "Intraoperative fluorescence staining of malignant brain tumors using 5-aminofluorescein-labeled albumin," Neurosurgery, vol.64, pp. S53-S61, Mar. 2009.
54. A. K. Iyer et al., "Exploiting the enhanced permeability and retention effect for tumor targeting," Drug Discov. Today, vol.11, pp. 812-818, 2006.
55. K. J. Murray, "Improved surgical resection of human brain tumors: Part 1. A preliminary study," Surg. Neurol., vol.17, pp. 316-319, 1982.
56. K.Koc et al., "Fluorescein sodium-guided surgery in glioblastoma multiforme: A prospective evaluation," Br. J. Neurosurg., vol.22, pp. 99-103, Feb. 2008.
57. T. Okuda et al., "Metastatic brain tumor surgery using fluorescein sodium: Technical note," Minim. Invasive Neurosurg., vol.50, pp. 382-384, 2007.
58. J. Shinoda et al., "Fluorescence-guided resection of glioblastoma multiforme, by using high-dose fluorescein sodium-Technical note," J. Neurosurg., vol.99, pp. 597-603, Sep. 2003.
59. T. Uzuka et al., "Surgical strategy for malignant glioma resection with intraoperative use of fluorescein Na," Neurol. Surg., vol.35, pp. 557-562, Jun. 2007.
60. T. Kuroiwa et al., "Development of a fluorescein operative microscope for use during malignant glioma surgery: A technical note and preliminary report," Surg. Neurol., vol.50, pp. 41-49, 1998.
61. G. E. Moore et al., "The clinical use of fluorescein in neurosurgery: The localization of brain tumors," J. Neurosurg., vol.5, pp. 392-398, 1948.
62. D. A. Hansen et al., "Indocyanine green (Icg) staining and demarcation of tumormargins in a rat glioma model," Surg. Neurol., vol.40, pp. 451-456, Dec. 1993.
63. M. M. Haglund et al., "Enhanced optical imaging of rat gliomas and tumor margins," Neurosurgery, vol.35, pp. 930-940, Nov. 1994.
64. M. M. Haglund et al., "Enhanced optical imaging of human gliomas and tumor margins," Neurosurgery, vol.38, pp. 308-317, Feb. 1996.
65. G. W. Britz et al., "Intracarotid RMP-7 enhanced indocyanine green staining of tumors in a rat glioma model," J. Neuro-Oncol., vol.56, pp. 227-232, Feb. 2002.
66. W. C. W. Chan et al., "Luminescent quantum dots for multiplexed biological detection and imaging," Curr. Opin. Biotechnol., vol.13, pp. 40-46, Feb. 2002.
67. B. Dubertret et al., "In vivo imaging of quantum dots encapsulated in phospholipid micelles," Science, vol.298, pp. 1759-1762, Nov. 2002.
68. O. Muhammad et al., "Macrophage-mediated colocalization of quantum dots in experimental glioma," Methods Mol. Biol., vol.374, pp. 161-171, 2007. (Pubitemid 350183406)
69. H. Jackson et al., "Quantum dots are phagocytized by macrophages and colocalize with experimental gliomas," Neurosurgery, vol.60, pp. 524-529, Mar. 2007.
70. D. J. Arndt-Jovin et al., "Tumor-targeted quantum dots can help surgeons find tumor boundaries," IEEE Trans. Nanobiosci., vol.8, no.1, pp. 65-71, Mar. 2009.
71. J.Wang et al., "Receptor-targeted quantum dots: Fluorescent probes for brain tumor diagnosis," J. Biomed. Opt., vol.12, p. 044021, Jul./Aug. 2007.
72. W. Cai et al., "Peptide-labeled near-infrared quantum dots for imaging tumor vasculature in living subjects," Nano Lett., vol.6, pp. 669-676, 2006.
73. S. Singh and H. S. Nalwa, "Nanotechnology and health safety-Toxicity and risk assessments of nanostructured materials on human health," J. Nanosci. Nanotechnol., vol.7, pp. 3048-3070, Sep. 2007.
74. H. S. Choi et al., "Renal clearance of quantum dots," Nature Biotechnol., vol.25, pp. 1165-1170, Oct. 2007.
75. H. Sarin et al., "Effective transvascular delivery of nanoparticles across the blood-brain tumor barrier into malignant glioma cells," J. Transl. Med., vol.6, p. 80, Dec. 2008.
76. D. A. Orringer et al., "In vitro characterization of a targeted, dye-loaded nanodevice for intraoperative tumor delineation," Neurosurgery, vol.64, pp. 965-971, May 2009.
77. S. E. Barry, "Challenges in the development of magnetic particles for therapeutic applications," Int. J. Hyperthermia, vol.24, pp. 451-466, 2008.
78. T. Islam and L. Josephson, "Current state and future applications of active targeting in malignancies using superparamagnetic iron oxide nanoparticles," Cancer Biomarkers, vol.5, pp. 99-107, 2009.
79. M. F. Kircher et al., "A multimodal nanoparticle for preoperative magnetic resonance imaging and intraoperative optical brain tumor delineation," Cancer Res., vol.63, pp. 8122-8125, Dec. 2003.
80. A. K. Gupta and M. Gupta, "Synthesis and surface engineering of iron oxide nanoparticles for biomedical applications," Biomaterials, vol.26, pp. 3995-4021, Jun. 2005.
81. R. Trehin et al., "Fluorescent nanoparticle uptake for brain tumor visualization," Neoplasia, vol.8, pp. 302-311, Apr. 2006.
82. O. Veiseh et al., "Inhibition of tumor-cell invasion with chlorotoxinbound superparamagnetic nanoparticles," Small, vol.5, pp. 256-264, Jan. 2009.
83. O. Veiseh et al., "Optical and MRI multifunctional nanoprobe for targeting gliomas," Nano Lett., vol.5, pp. 1003-1008, Jun. 2005.
84. C. Sun et al., "In vivo MRI detection of gliomas by chlorotoxinconjugated superparamagnetic nanoprobes," Small, vol.4, pp. 372-379, Mar. 2008.
85. M. M. Patel et al., "Getting into the brain: Approaches to enhance brain drug delivery," CNS Drugs, vol.23, pp. 35-58, 2009.
86. C. Andersson et al., "Identification of tissue sites for increased albumin degradation in sarcoma-bearing mice," J. Surg. Res., vol.50, pp. 156-162, Feb. 1991.
87. G. Stehle et al., "Plasma protein (albumin) catabolism by the tumor itself-Implications for tumor metabolism and the genesis of cachexia," Crit. Rev. Oncol./Hematol., vol.26, pp. 77-100, Jul. 1997.
88. A. Wunder et al., "Enhanced albumin uptake by rat tumors," Int. J. Oncol., vol.11, pp. 497-507, Sep. 1997.
89. P. Kremer et al., "Laser-induced fluorescence detection of malignant gliomas using fluorescein-labeled serum albumin: Experimental and preliminary clinical results," Neurol. Res., vol.22, pp. 481-489, Jul. 2000.
90. S. H. Torp et al., "Epidermal growth-factor receptor expression in human gliomas," Cancer Immunol. Immunother., vol.33, pp. 61-64, Mar. 1991.
91. S. L. Gibbs-Strauss et al., "Diagnostic detection of diffuse glioma tumors in vivo with molecular fluorescent probe-based transmission spectroscopy," Med. Phys., vol.36, pp. 974-983, Mar. 2009.
92. S. C. Davis et al., "Magnetic resonance-coupled fluorescence tomography scanner for molecular imaging of tissue," Rev. Sci. Instrum., vol.79, pp. 064302-1-064302-10, Jun. 2008.
93. R.Weissleder et al., "In vivo imaging of tumors with protease-activated near-infrared fluorescent probes," Nat. Biotechnol., vol.17, pp. 375-378, Apr. 1999.
94. C. M. McCann et al., "Combined magnetic resonance and fluorescence imaging of the living mouse brain reveals glioma response to chemotherapy," Neuroimage, vol.45, pp. 360-369, Apr. 2009.
95. M. Mammen et al., "Polyvalent interactions in biological systems: Implications for design and use of multivalent ligands and inhibitors," Angew. Chem. Int. Ed., vol.37, pp. 2755-2794, 1998.
96. X. Chen et al., "In vivo near-infrared fluorescence imaging of integrin {alpha}v{beta}3 in brain tumor xenografts," Cancer Res., vol.64, pp. 8009-8014, Nov. 2004.
97. A. R. Hsu et al., "In vivo near-infrared fluorescence imaging of integrin alphavbeta3 in an orthotopic glioblastoma model," Mol. Imag. Biol., vol.8, pp. 315-323, Nov./Dec. 2006.
98. S. R. Kantelhardt et al., "Multiphoton excitation fluorescence microscopy of 5-aminolevulinic acid induced fluorescence in experimental gliomas," Lasers Surg. Med., vol.40, pp. 273-281, Apr. 2008.
99. C. C. Hoyt et al., "Remote biomedical spectroscopic imaging of human artery wall," Lasers Surg. Med., vol.8, pp. 1-9, 1988.
100. Y. Tamura et al., "Endoscopic identification and biopsy sampling of an intraventricular malignant glioma using a 5-aminolevulinic acid-induced protoporphyrin IX fluorescence imaging system. Technical note," J. Neurosurg., vol.106, pp. 507-510, Mar. 2007.
101. G. A. Wagnieres et al., "In vivo fluorescence spectroscopy and imaging for oncological applications," Photochem. Photobiol., vol.68, pp. 603-632, Nov. 1998.
102. U. Utzinger and R. R. Richards-Kortum, "Fiber optic probes for biomedical optical spectroscopy," J. Biomed. Opt., vol.8, pp. 121-147, 2003.
103. B.W. Pogue et al., "Analysis of sampling volume and tissue heterogeneity upon the in vivo detection of fluorescence," J. Biomed. Opt., vol.10, p. 41206, 2005.
104. B.W. Pogue and G. C. Burke, "Fiber optic bundle design for quantitative fluorescence measurement from tissue," Appl. Opt., vol.37, pp. 7429-7436, 1998.
105. M. Sinaasappel and H. J. C. M. Sterenborg, "Quantification of the hematoporphyrin derivative by fluorescence measurement using dualwavelength excitation and dual-wavelength detection," Appl. Opt., vol.32, pp. 541-548, 1993.
106. H. J. Sterenborg et al., "Evaluation of spectral correction techniques for fluorescence measurements on pigmented lesions in vivo," J. Photochem. Photobiol., vol.B-Biology. 35, pp. 159-165, Sep. 1996.
107. R. Ishihara et al., "Quantitative spectroscopic analysis of 5-aminolevulinic acid-induced protoporphyrin IX fluorescence intensity in diffusely infiltrating astrocytomas," Neurol. Med.-Chir., vol.47, pp. 53-57, Feb. 2007.
108. S. Utsuki et al., "Auditory alert system for fluorescence-guided resection of gliomas," Neurol. Med.-Chir., vol.48, pp. 95-97, Feb. 2008.
109. S. Utsuki 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., vol.104, pp. 618-620, Apr. 2006.
110. V. X. D. Yang et al., "A multispectral fluorescence imaging system: Design and initial clinical tests in intra-operative photofrin-photodynamic therapy of brain tumors," Lasers Surg. Med., vol.32, pp. 224-232, 2003.
111. T. Kuroiwa et al., "Comparison between operative findings on malignant glioma by a fluorescein surgical microscopy and histological findings," Neurol. Res., vol.21, pp. 130-134, Jan. 1999.
112. W. Stummer et al., "Technical principles for protoporphyrin- IXfluorescence guidedmicrosurgical resection ofmalignant glioma tissue," Acta Neurochir., vol.140, pp. 995-1000, 1998.
113. S. C. Gebhart et al., "Liquid-crystal tunable filter spectral imaging for brain tumor demarcation," Appl. Opt., vol.46, pp. 1896-1910, Apr. 2007.
114. V. X. Yang et al., "A multispectral fluorescence imaging system: Design and initial clinical tests in intra-operative photofrin-photodynamic therapy of brain tumors," Lasers Surg. Med., vol.32, pp. 224-232, 2003.
115. S. C. Davis et al., "Magnetic resonance-coupled fluorescence tomography scanner for molecular imaging of small animals and human breasts," Rev. Sci., to be published.
116. L. M. DeAngelis, "Brain tumors," New Engl. J.Med., vol.344, pp. 114-123, Jan. 2001.
117. P. Y. Wen and S. Kesari, "Malignant gliomas in adults," New Engl. J. Med., vol.359, pp. 492-507, Jul. 2008.
118. A. Michotte et al., "Neuropathological and molecular aspects of lowgrade and high-grade gliomas," Acta Neurol. Belg., vol.104, pp. 148-153, Dec. 2004.
119. M. L. Bondy et al., "Brain tumor epidemiology: Consensus from the brain tumor epidemiology consortium," Cancer, vol.113, pp. 1953-1968, Oct. 2008.
120. F. K. Albert et al., "Early postoperative magnetic resonance imaging after resection of malignant glioma: Objective evaluation of residual tumor and its influence on regrowth and prognosis," Neurosurgery, vol.34, pp. 45-60, Jan. 1994.
121. F. G. Barker, II et al., "Radiation response and survival time in patients with glioblastoma multiforme," J. Neurosurg., vol.84, pp. 442-448, Mar. 1996.
122. M. Lacroix et al., "A multivariate analysis of 416 patients with glioblastoma multiforme: Prognosis, extent of resection, and survival," J. Neurosurg., vol.95, pp. 190-198, Aug. 2001.
123. U. Pichlmeier et al., "Resection and survival in glioblastoma multiforme: An RTOG recursive partitioning analysis of ALA study patients," Neuro Oncol., vol.10, pp. 1025-1034, Dec. 2008.
124. W. Stummer et al., "Extent of resection and survival in glioblastoma multiforme: Identification of and adjustment for bias," Neurosurgery, vol.62, pp. 564-576, Mar. 2008.
125. C. J. Vecht et al., "The influence of the extent of surgery on the neurological function and survival in malignant glioma. A retrospective analysis in 243 patients," J. Neurol. Neurosurg. Psychiatry, vol.53, pp. 466-471, Jun. 1990.
126. S. Utsuki et al., "Fluorescence-guided resection of metastatic brain tumors using a 5-aminolevulinic acid-induced protoporphyrin IX: Pathological study," Brain Tumor Pathol., vol.24, pp. 53-55, 2007.
127. S. Utsuki et al., "Histological examination of false positive tissue resection using 5-aminolevulinic acid-induced fluorescence guidance," Neurol. Med.-Chir., vol.47, pp. 210-213, May 2007.
128. M. Toda, "Intraoperative navigation and fluorescence imagings in malignant glioma surgery," Keio J. Med., vol.57, pp. 155-161, Sep. 2008.
129. Y. Morofuji et al., "Usefulness of intraoperative photodynamic diagnosis using 5-aminolevulinic acid for meningiomas with cranial invasion: technical case report," Neurosurgery, vol.62, pp. 102-103, Mar. 2008.
130. S. Miyatake et al., "Fluorescence of non-neoplastic, magnetic resonance imaging-enhancing tissue by 5-aminolevulinic acid: Case report," Neurosurgery, vol.61, pp. E1101-E1103, Nov. 2007.
131. Y. Kajimoto et al., "Use of 5-aminolevulinic acid in fluorescence-guided resection of meningioma with high risk of recurrence. Case report," J. Neurosurg., vol.106, pp. 1070-1074, Jun. 2007.
132. M. Hefti et al., "5-aminolevulinic acid induced protoporphyrin IX fluorescence in high-grade glioma surgery: A one-year experience at a single institutuion," Swiss Med. Wkly., vol.138, pp. 180-185, Mar. 2008.
133. P. Valdes et al., "Brain tumor resection guided by fluorescence imaging andMRI image guidance," in Proc. SPIE, Med. Imag. 2009: Vis., Image-Guided Proced., Model., vol.7261, pp. 726103-1-726103-8.
134. F. Leblond et al., "Brain tumor resection guided by fluorescence imaging," in Proc. SPIE-Int. Soc. Opt. Eng., vol.7164, pp. 71640M-1-71640M-8, 2009.
135. S.-I. Miyatake et al., "Fluorescence of non-neoplastic, magnetic resonance imaging-enhancing tissue by 5-aminolevulinic acid: Case report," Neurosurgery, vol.61, pp. E1101-E1103, Nov. 2007.
136. W. Stummer et al., "Fluorescence-guided resections of malignant gliomas-An overview," Acta Neurochir.-Suppl., vol.88, pp. 9-12, 2003.
137. M. S. Eljamel et al., "ALA and photofrin fluorescence-guided resection and repetitive PDT in glioblastoma multiforme: A single centre Phase III randomised controlled trial," Lasers Med. Sci., vol.23, pp. 361-367, Oct. 2008.