Abstract

Gliomas are diffuse and hard to cure brain tumors. A major reason for their aggressive behavior is their property to infiltrate the brain. The gross appearance of the infiltrative component is comparable to normal brain, constituting an obstacle to extended surgical resection. 5-ALA induced PpIX fluorescence measurements enable gains in sensitivity to detect infiltrated cells, but still lack sensitivity to get accurate discrimination between the tumor margin and healthy tissue. In this fluorescence spectroscopic study, we assume that two states of PpIX contribute to total fluorescence to get better discrimination of healthy tissues against tumor margins. We reveal that fluorescence in low-density margins of high-grade gliomas or in low-grade gliomas is mainly influenced by the second state of PpIX centered at 620 nm. We thus conclude that consideration of the contributions of both states to total fluorescence can help to improve fluorescence-guided resection of gliomas by discriminating healthy tissues from tumor margins.

© 2019 Optical Society of America under the terms of the OSA Open Access Publishing Agreement

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2018 (11)

R. Maugeri, A. Villa, M. Pino, A. Imperato, G. R. Giammalva, G. Costantino, F. Graziano, C. Gulì, F. Meli, N. Francaviglia, and D. G. Iacopino, “With a Little Help from My Friends: The Role of Intraoperative Fluorescent Dyes in the Surgical Management of High-Grade Gliomas,” Brain Sci. 8(2), 31 (2018).
[Crossref] [PubMed]

E. D. Bander, R. Magge, and R. Ramakrishna, “Advances in Glioblastoma Operative Techniques,” World Neurosurg. 116, 529–538 (2018).
[Crossref] [PubMed]

N. Haj-Hosseini, J. C. O. Richter, P. Milos, M. Hallbeck, and K. Wårdell, “5-ALA fluorescence and laser Doppler flowmetry for guidance in a stereotactic brain tumor biopsy,” Biomed. Opt. Express 9(5), 2284–2296 (2018).
[Crossref] [PubMed]

B. Kiesel, M. Millesi, A. Woehrer, J. Furtner, A. Bavand, T. Roetzer, M. Mischkulnig, S. Wolfsberger, M. Preusser, E. Knosp, and G. Widhalm, “5-ALA-induced fluorescence as a marker for diagnostic tissue in stereotactic biopsies of intracranial lymphomas: experience in 41 patients,” Neurosurg. Focus 44(6), E7 (2018).
[Crossref] [PubMed]

B. Kiesel, M. Mischkulnig, A. Woehrer, M. Martinez-Moreno, M. Millesi, A. Mallouhi, T. Czech, M. Preusser, J. A. Hainfellner, S. Wolfsberger, E. Knosp, and G. Widhalm, “Systematic histopathological analysis of different 5-aminolevulinic acid-induced fluorescence levels in newly diagnosed glioblastomas,” J. Neurosurg. 129(2), 341–353 (2018).
[Crossref] [PubMed]

E. Belykh, E. J. Miller, A. A. Patel, B. Bozkurt, K. Yağmurlu, T. R. Robinson, P. Nakaji, R. F. Spetzler, M. T. Lawton, L. Y. Nelson, E. J. Seibel, and M. C. Preul, “Optical Characterization of Neurosurgical Operating Microscopes: Quantitative Fluorescence and Assessment of PpIX Photobleaching,” Sci. Rep. 8(1), 12543 (2018).
[Crossref] [PubMed]

T. Yoneda, N. Nonoguchi, N. Ikeda, R. Yagi, S. Kawabata, M. Furuse, Y. Hirose, H. Kuwabara, Y. Tamura, Y. Kajimoto, and T. Kuroiwa, “Spectral Radiance of Protoporphyrin IX Fluorescence and Its Histopathological Implications in 5-Aminolevulinic Acid-Guided Surgery for Glioblastoma,” Photomed. Laser Surg. 36(5), 266–272 (2018).
[Crossref] [PubMed]

S. Kröger, A.-C. Niehoff, A. Jeibmann, M. Sperling, W. Paulus, W. Stummer, and U. Karst, “Complementary Molecular and Elemental Mass-Spectrometric Imaging of Human Brain Tumors Resected by Fluorescence-Guided Surgery,” Anal. Chem. 90(20), 12253–12260 (2018).
[Crossref] [PubMed]

L. Alston, D. Rousseau, M. Hebert, L. Mahieu-Williame, and B. Montcel, “Nonlinear relation between concentration and fluorescence emission of protoporphyrin IX in calibrated phantoms,” J. Biomed. Opt. 23(9), 1–7 (2018).
[Crossref] [PubMed]

K. Omoto, R. Matsuda, I. Nakagawa, Y. Motoyama, and H. Nakase, “False-positive inflammatory change mimicking glioblastoma multiforme under 5-aminolevulinic acid-guided surgery: A case report,” Surg. Neurol. Int. 9(1), 49 (2018).
[Crossref] [PubMed]

E. Yoshioka, V. S. Chelakkot, M. Licursi, S. G. Rutihinda, J. Som, L. Derwish, J. J. King, T. Pongnopparat, K. Mearow, M. Larijani, A. M. Dorward, and K. Hirasawa, “Enhancement of Cancer-Specific Protoporphyrin IX Fluorescence by Targeting Oncogenic Ras/MEK Pathway,” Theranostics 8(8), 2134–2146 (2018).
[Crossref] [PubMed]

2017 (3)

S. Kim, J. E. Kim, Y. H. Kim, T. Hwang, S. K. Kim, W. J. Xu, J.-Y. Shin, J.-I. Kim, H. Choi, H. C. Kim, H. R. Cho, A. Choi, T. Chowdhury, Y. Seo, Y.-S. Dho, J. W. Kim, D. G. Kim, S.-H. Park, H. Kim, S. H. Choi, S. Park, S.-H. Lee, and C.-K. Park, “Glutaminase 2 expression is associated with regional heterogeneity of 5-aminolevulinic acid fluorescence in glioblastoma,” Sci. Rep. 7(1), 12221 (2017).
[Crossref] [PubMed]

M. Zanello, F. Poulon, J. Pallud, P. Varlet, H. Hamzeh, G. Abi Lahoud, F. Andreiuolo, A. Ibrahim, M. Pages, F. Chretien, F. Di Rocco, E. Dezamis, F. Nataf, B. Turak, B. Devaux, and D. Abi Haidar, “Multimodal optical analysis discriminates freshly extracted human sample of gliomas, metastases and meningiomas from their appropriate controls,” Sci. Rep. 7(1), 41724 (2017).
[Crossref] [PubMed]

J. J. Bravo, J. D. Olson, S. C. Davis, D. W. Roberts, K. D. Paulsen, and S. C. Kanick, “Hyperspectral data processing improves PpIX contrast during fluorescence guided surgery of human brain tumors,” Sci. Rep. 7(1), 9455 (2017).
[Crossref] [PubMed]

2016 (5)

D. N. Louis, A. Perry, G. Reifenberger, A. von Deimling, D. Figarella-Branger, W. K. Cavenee, H. Ohgaki, O. D. Wiestler, P. Kleihues, and D. W. Ellison, “The 2016 World Health Organization Classification of Tumors of the Central Nervous System: a summary,” Acta Neuropathol. 131(6), 803–820 (2016).
[Crossref] [PubMed]

Y. M. Li, D. Suki, K. Hess, and R. Sawaya, “The influence of maximum safe resection of glioblastoma on survival in 1229 patients: Can we do better than gross-total resection?” J. Neurosurg. 124(4), 977–988 (2016).
[Crossref] [PubMed]

P. A. Valdés, D. W. Roberts, F.-K. Lu, and A. Golby, “Optical technologies for intraoperative neurosurgical guidance,” Neurosurg. Focus 40(3), E8 (2016).
[Crossref] [PubMed]

M. Marois, J. Bravo, S. C. Davis, and S. C. Kanick, “Characterization and standardization of tissue-simulating protoporphyrin IX optical phantoms,” J. Biomed. Opt. 21(3), 303003 (2016).
[Crossref] [PubMed]

C. K. Hope and S. M. Higham, “Evaluating the effect of local pH on fluorescence emissions from oral bacteria of the genus Prevotella,” J. Biomed. Opt. 21(8), 084003 (2016).
[Crossref] [PubMed]

2015 (3)

D. A. Haidar, B. Leh, M. Zanello, and R. Siebert, “Spectral and lifetime domain measurements of rat brain tumors,” Biomed. Opt. Express 6(4), 1219–1233 (2015).
[Crossref] [PubMed]

P. A. Valdés, V. Jacobs, B. T. Harris, B. C. Wilson, F. Leblond, K. D. Paulsen, and D. W. Roberts, “Quantitative fluorescence using 5-aminolevulinic acid-induced protoporphyrin IX biomarker as a surgical adjunct in low-grade glioma surgery,” J. Neurosurg. 123(3), 771–780 (2015).
[Crossref] [PubMed]

C. G. Hadjipanayis, G. Widhalm, and W. Stummer, “What is the Surgical Benefit of Utilizing 5-Aminolevulinic Acid for Fluorescence-Guided Surgery of Malignant Gliomas?” Neurosurgery 77(5), 663–673 (2015).
[Crossref] [PubMed]

2014 (4)

Y. Li, R. Rey-Dios, D. W. Roberts, P. A. Valdés, and A. A. Cohen-Gadol, “Intraoperative Fluorescence-Guided Resection of High-Grade Gliomas: A Comparison of the Present Techniques and Evolution of Future Strategies,” World Neurosurg. 82(1-2), 175–185 (2014).
[Crossref] [PubMed]

J. T. C. Liu, D. Meza, and N. Sanai, “Trends in Fluorescence Image-Guided Surgery for Gliomas,” Neurosurgery 75(1), 61–71 (2014).
[Crossref] [PubMed]

M. Lacroix and S. A. Toms, “Maximum Safe Resection of Glioblastoma Multiforme,” J. Clin. Oncol. 32(8), 727–728 (2014).
[Crossref] [PubMed]

A. C. Croce and G. Bottiroli, “Autofluorescence spectroscopy and imaging: a tool for biomedical research and diagnosis,” Eur. J. Histochem. 58(4), 2461 (2014).
[Crossref] [PubMed]

2013 (3)

G. A. Barron, R. Valentine, H. Moseley, L. Brancaleon, C. Hill, and J. A. Woods, “Porphyrin profile in four human cell lines after supplementation with 5-aminolaevulinic acid and its methyl ester,” Photodiagn. Photodyn. Ther. 10(4), 654–663 (2013).
[Crossref] [PubMed]

K. Petrecca, M.-C. Guiot, V. Panet-Raymond, and L. Souhami, “Failure pattern following complete resection plus radiotherapy and temozolomide is at the resection margin in patients with glioblastoma,” J. Neurooncol. 111(1), 19–23 (2013).
[Crossref] [PubMed]

B. Montcel, L. Mahieu-Williame, X. Armoiry, D. Meyronet, and J. Guyotat, “Two-peaked 5-ALA-induced PpIX fluorescence emission spectrum distinguishes glioblastomas from low grade gliomas and infiltrative component of glioblastomas,” Biomed. Opt. Express 4(4), 548–558 (2013).
[Crossref] [PubMed]

2011 (6)

T. Ando, E. Kobayashi, H. Liao, T. Maruyama, Y. Muragaki, H. Iseki, O. Kubo, and I. Sakuma, “Precise comparison of protoporphyrin IX fluorescence spectra with pathological results for brain tumor tissue identification,” Brain Tumor Pathol. 28(1), 43–51 (2011).
[Crossref] [PubMed]

P. A. Valdés, F. Leblond, A. Kim, B. T. Harris, B. C. Wilson, X. Fan, T. D. Tosteson, A. Hartov, S. Ji, K. Erkmen, N. E. Simmons, K. D. Paulsen, and D. W. Roberts, “Quantitative fluorescence in intracranial tumor: implications for ALA-induced PpIX as an intraoperative biomarker,” J. Neurosurg. 115(1), 11–17 (2011).
[Crossref] [PubMed]

N. Sanai, M.-Y. Polley, M. W. McDermott, A. T. Parsa, and M. S. Berger, “An extent of resection threshold for newly diagnosed glioblastomas,” J. Neurosurg. 115(1), 3–8 (2011).
[Crossref] [PubMed]

C. Senft, A. Bink, K. Franz, H. Vatter, T. Gasser, and V. Seifert, “Intraoperative MRI guidance and extent of resection in glioma surgery: a randomised, controlled trial,” Lancet Oncol. 12(11), 997–1003 (2011).
[Crossref] [PubMed]

P. L. Kubben, K. J. ter Meulen, O. E. Schijns, M. P. ter Laak-Poort, J. J. van Overbeeke, and H. van Santbrink, “Intraoperative MRI-guided resection of glioblastoma multiforme: a systematic review,” Lancet Oncol. 12(11), 1062–1070 (2011).
[Crossref] [PubMed]

P. A. Valdés, A. Kim, M. Brantsch, C. Niu, Z. B. Moses, T. D. Tosteson, B. C. Wilson, K. D. Paulsen, D. W. Roberts, and B. T. Harris, “δ-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(8), 846–856 (2011).
[Crossref] [PubMed]

2010 (3)

N. Haj-Hosseini, J. Richter, S. Andersson-Engels, and K. Wårdell, “Optical touch pointer for fluorescence guided glioblastoma resection using 5-aminolevulinic acid,” Lasers Surg. Med. 42(1), 9–14 (2010).
[Crossref] [PubMed]

A. Kim, M. Khurana, Y. Moriyama, and B. C. Wilson, “Quantification of in vivo fluorescence decoupled from the effects of tissue optical properties using fiber-optic spectroscopy measurements,” J. Biomed. Opt. 15(6), 067006 (2010).
[Crossref] [PubMed]

A. Johansson, G. Palte, O. Schnell, J.-C. Tonn, J. Herms, and H. Stepp, “5-Aminolevulinic Acid-induced Protoporphyrin IX Levels in Tissue of Human Malignant Brain Tumors,” Photochem. Photobiol. 86(6), 1373–1378 (2010).
[Crossref] [PubMed]

2007 (1)

W. Dietel, R. Pottier, W. Pfister, P. Schleier, and K. Zinner, “5-Aminolaevulinic acid (ALA) induced formation of different fluorescent porphyrins: A study of the biosynthesis of porphyrins by bacteria of the human digestive tract,” J. Photochem. Photobiol. B 86(1), 77–86 (2007).
[Crossref] [PubMed]

2006 (2)

W. Stummer, U. Pichlmeier, T. Meinel, O. D. Wiestler, F. Zanella, and H.-J. Reulen, “Fluorescence-guided surgery with 5-aminolevulinic acid for resection of malignant glioma: a randomised controlled multicentre phase III trial,” Lancet Oncol. 7(5), 392–401 (2006).
[Crossref] [PubMed]

G. N. Wu, J. M. Ford, and J. R. Alger, “MRI measurement of the uptake and retention of motexafin gadolinium in glioblastoma multiforme and uninvolved normal human brain,” J. Neurooncol. 77(1), 95–103 (2006).
[Crossref] [PubMed]

2003 (1)

E. R. Laws, I. F. Parney, W. Huang, F. Anderson, A. M. Morris, A. Asher, K. O. Lillehei, M. Bernstein, H. Brem, A. Sloan, M. S. Berger, S. Chang, and Glioma Outcomes Investigators, “Survival following surgery and prognostic factors for recently diagnosed malignant glioma: data from the Glioma Outcomes Project,” J. Neurosurg. 99(3), 467–473 (2003).
[Crossref] [PubMed]

2001 (1)

A. Nabavi, P. M. Black, D. T. Gering, C.-F. Westin, V. Mehta, R. S. Pergolizzi, M. Ferrant, S. K. Warfield, N. Hata, R. B. Schwartz, W. M. Wells, R. Kikinis, and F. A. Jolesz, “Serial intraoperative magnetic resonance imaging of brain shift,” Neurosurgery 48(4), 787–797, discussion 797–798 (2001).
[PubMed]

1998 (1)

W. Stummer, H. Stepp, G. Möller, A. Ehrhardt, M. Leonhard, and H. J. Reulen, “Technical principles for protoporphyrin-IX-fluorescence guided microsurgical resection of malignant glioma tissue,” Acta Neurochir. (Wien) 140(10), 995–1000 (1998).
[Crossref] [PubMed]

1997 (2)

W. Dietel, C. Fritsch, R. H. Pottier, and R. Wendenburg, “5-Aminolaevulinic-acid-induced formation of different porphyrins and their photomodifications,” Lasers Med. Sci. 12(3), 226–236 (1997).
[Crossref] [PubMed]

C. Fuchs, R. Riesenberg, J. Siegert, and R. Baumgartner, “H-dependent formation of 5-aminolaevulinic acid-induced protoporphyrin IX in fibrosarcoma cells,” J. Photochem. Photobiol. B 40(1), 49–54 (1997).
[Crossref] [PubMed]

1990 (1)

G. I. Lozovaya, Z. Masinovsky, and A. A. Sivash, “Protoporphyrin IX as a possible ancient photosensitizer: spectral and photochemical studies,” Orig. Life Evol. Biosph. 20(3-4), 321–330 (1990).
[Crossref]

1987 (1)

H. H. Thaw, “Optimal conditions for the measurement of lipid peroxidation products (lipofuscin) in individual cultivated human glial and glioma cells,” Mech. Ageing Dev. 38(1), 79–87 (1987).
[Crossref] [PubMed]

1986 (1)

T. B. Melø and G. Reisaeter, “The physicochemical state of protoporphyrin IX in aqueous solution investigated by fluorescence and light scattering,” Biophys. Chem. 25(1), 99–104 (1986).
[Crossref] [PubMed]

Abi Haidar, D.

M. Zanello, F. Poulon, J. Pallud, P. Varlet, H. Hamzeh, G. Abi Lahoud, F. Andreiuolo, A. Ibrahim, M. Pages, F. Chretien, F. Di Rocco, E. Dezamis, F. Nataf, B. Turak, B. Devaux, and D. Abi Haidar, “Multimodal optical analysis discriminates freshly extracted human sample of gliomas, metastases and meningiomas from their appropriate controls,” Sci. Rep. 7(1), 41724 (2017).
[Crossref] [PubMed]

Abi Lahoud, G.

M. Zanello, F. Poulon, J. Pallud, P. Varlet, H. Hamzeh, G. Abi Lahoud, F. Andreiuolo, A. Ibrahim, M. Pages, F. Chretien, F. Di Rocco, E. Dezamis, F. Nataf, B. Turak, B. Devaux, and D. Abi Haidar, “Multimodal optical analysis discriminates freshly extracted human sample of gliomas, metastases and meningiomas from their appropriate controls,” Sci. Rep. 7(1), 41724 (2017).
[Crossref] [PubMed]

Alger, J. R.

G. N. Wu, J. M. Ford, and J. R. Alger, “MRI measurement of the uptake and retention of motexafin gadolinium in glioblastoma multiforme and uninvolved normal human brain,” J. Neurooncol. 77(1), 95–103 (2006).
[Crossref] [PubMed]

Alston, L.

L. Alston, D. Rousseau, M. Hebert, L. Mahieu-Williame, and B. Montcel, “Nonlinear relation between concentration and fluorescence emission of protoporphyrin IX in calibrated phantoms,” J. Biomed. Opt. 23(9), 1–7 (2018).
[Crossref] [PubMed]

Anderson, F.

E. R. Laws, I. F. Parney, W. Huang, F. Anderson, A. M. Morris, A. Asher, K. O. Lillehei, M. Bernstein, H. Brem, A. Sloan, M. S. Berger, S. Chang, and Glioma Outcomes Investigators, “Survival following surgery and prognostic factors for recently diagnosed malignant glioma: data from the Glioma Outcomes Project,” J. Neurosurg. 99(3), 467–473 (2003).
[Crossref] [PubMed]

Andersson-Engels, S.

N. Haj-Hosseini, J. Richter, S. Andersson-Engels, and K. Wårdell, “Optical touch pointer for fluorescence guided glioblastoma resection using 5-aminolevulinic acid,” Lasers Surg. Med. 42(1), 9–14 (2010).
[Crossref] [PubMed]

Ando, T.

T. Ando, E. Kobayashi, H. Liao, T. Maruyama, Y. Muragaki, H. Iseki, O. Kubo, and I. Sakuma, “Precise comparison of protoporphyrin IX fluorescence spectra with pathological results for brain tumor tissue identification,” Brain Tumor Pathol. 28(1), 43–51 (2011).
[Crossref] [PubMed]

Andreiuolo, F.

M. Zanello, F. Poulon, J. Pallud, P. Varlet, H. Hamzeh, G. Abi Lahoud, F. Andreiuolo, A. Ibrahim, M. Pages, F. Chretien, F. Di Rocco, E. Dezamis, F. Nataf, B. Turak, B. Devaux, and D. Abi Haidar, “Multimodal optical analysis discriminates freshly extracted human sample of gliomas, metastases and meningiomas from their appropriate controls,” Sci. Rep. 7(1), 41724 (2017).
[Crossref] [PubMed]

Armoiry, X.

Asher, A.

E. R. Laws, I. F. Parney, W. Huang, F. Anderson, A. M. Morris, A. Asher, K. O. Lillehei, M. Bernstein, H. Brem, A. Sloan, M. S. Berger, S. Chang, and Glioma Outcomes Investigators, “Survival following surgery and prognostic factors for recently diagnosed malignant glioma: data from the Glioma Outcomes Project,” J. Neurosurg. 99(3), 467–473 (2003).
[Crossref] [PubMed]

Bander, E. D.

E. D. Bander, R. Magge, and R. Ramakrishna, “Advances in Glioblastoma Operative Techniques,” World Neurosurg. 116, 529–538 (2018).
[Crossref] [PubMed]

Barron, G. A.

G. A. Barron, R. Valentine, H. Moseley, L. Brancaleon, C. Hill, and J. A. Woods, “Porphyrin profile in four human cell lines after supplementation with 5-aminolaevulinic acid and its methyl ester,” Photodiagn. Photodyn. Ther. 10(4), 654–663 (2013).
[Crossref] [PubMed]

Baumgartner, R.

C. Fuchs, R. Riesenberg, J. Siegert, and R. Baumgartner, “H-dependent formation of 5-aminolaevulinic acid-induced protoporphyrin IX in fibrosarcoma cells,” J. Photochem. Photobiol. B 40(1), 49–54 (1997).
[Crossref] [PubMed]

Bavand, A.

B. Kiesel, M. Millesi, A. Woehrer, J. Furtner, A. Bavand, T. Roetzer, M. Mischkulnig, S. Wolfsberger, M. Preusser, E. Knosp, and G. Widhalm, “5-ALA-induced fluorescence as a marker for diagnostic tissue in stereotactic biopsies of intracranial lymphomas: experience in 41 patients,” Neurosurg. Focus 44(6), E7 (2018).
[Crossref] [PubMed]

Belykh, E.

E. Belykh, E. J. Miller, A. A. Patel, B. Bozkurt, K. Yağmurlu, T. R. Robinson, P. Nakaji, R. F. Spetzler, M. T. Lawton, L. Y. Nelson, E. J. Seibel, and M. C. Preul, “Optical Characterization of Neurosurgical Operating Microscopes: Quantitative Fluorescence and Assessment of PpIX Photobleaching,” Sci. Rep. 8(1), 12543 (2018).
[Crossref] [PubMed]

Berger, M. S.

N. Sanai, M.-Y. Polley, M. W. McDermott, A. T. Parsa, and M. S. Berger, “An extent of resection threshold for newly diagnosed glioblastomas,” J. Neurosurg. 115(1), 3–8 (2011).
[Crossref] [PubMed]

E. R. Laws, I. F. Parney, W. Huang, F. Anderson, A. M. Morris, A. Asher, K. O. Lillehei, M. Bernstein, H. Brem, A. Sloan, M. S. Berger, S. Chang, and Glioma Outcomes Investigators, “Survival following surgery and prognostic factors for recently diagnosed malignant glioma: data from the Glioma Outcomes Project,” J. Neurosurg. 99(3), 467–473 (2003).
[Crossref] [PubMed]

Bernstein, M.

E. R. Laws, I. F. Parney, W. Huang, F. Anderson, A. M. Morris, A. Asher, K. O. Lillehei, M. Bernstein, H. Brem, A. Sloan, M. S. Berger, S. Chang, and Glioma Outcomes Investigators, “Survival following surgery and prognostic factors for recently diagnosed malignant glioma: data from the Glioma Outcomes Project,” J. Neurosurg. 99(3), 467–473 (2003).
[Crossref] [PubMed]

Bink, A.

C. Senft, A. Bink, K. Franz, H. Vatter, T. Gasser, and V. Seifert, “Intraoperative MRI guidance and extent of resection in glioma surgery: a randomised, controlled trial,” Lancet Oncol. 12(11), 997–1003 (2011).
[Crossref] [PubMed]

Black, P. M.

A. Nabavi, P. M. Black, D. T. Gering, C.-F. Westin, V. Mehta, R. S. Pergolizzi, M. Ferrant, S. K. Warfield, N. Hata, R. B. Schwartz, W. M. Wells, R. Kikinis, and F. A. Jolesz, “Serial intraoperative magnetic resonance imaging of brain shift,” Neurosurgery 48(4), 787–797, discussion 797–798 (2001).
[PubMed]

Bottiroli, G.

A. C. Croce and G. Bottiroli, “Autofluorescence spectroscopy and imaging: a tool for biomedical research and diagnosis,” Eur. J. Histochem. 58(4), 2461 (2014).
[Crossref] [PubMed]

Bozkurt, B.

E. Belykh, E. J. Miller, A. A. Patel, B. Bozkurt, K. Yağmurlu, T. R. Robinson, P. Nakaji, R. F. Spetzler, M. T. Lawton, L. Y. Nelson, E. J. Seibel, and M. C. Preul, “Optical Characterization of Neurosurgical Operating Microscopes: Quantitative Fluorescence and Assessment of PpIX Photobleaching,” Sci. Rep. 8(1), 12543 (2018).
[Crossref] [PubMed]

Brancaleon, L.

G. A. Barron, R. Valentine, H. Moseley, L. Brancaleon, C. Hill, and J. A. Woods, “Porphyrin profile in four human cell lines after supplementation with 5-aminolaevulinic acid and its methyl ester,” Photodiagn. Photodyn. Ther. 10(4), 654–663 (2013).
[Crossref] [PubMed]

Brantsch, M.

P. A. Valdés, A. Kim, M. Brantsch, C. Niu, Z. B. Moses, T. D. Tosteson, B. C. Wilson, K. D. Paulsen, D. W. Roberts, and B. T. Harris, “δ-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(8), 846–856 (2011).
[Crossref] [PubMed]

Bravo, J.

M. Marois, J. Bravo, S. C. Davis, and S. C. Kanick, “Characterization and standardization of tissue-simulating protoporphyrin IX optical phantoms,” J. Biomed. Opt. 21(3), 303003 (2016).
[Crossref] [PubMed]

Bravo, J. J.

J. J. Bravo, J. D. Olson, S. C. Davis, D. W. Roberts, K. D. Paulsen, and S. C. Kanick, “Hyperspectral data processing improves PpIX contrast during fluorescence guided surgery of human brain tumors,” Sci. Rep. 7(1), 9455 (2017).
[Crossref] [PubMed]

Brem, H.

E. R. Laws, I. F. Parney, W. Huang, F. Anderson, A. M. Morris, A. Asher, K. O. Lillehei, M. Bernstein, H. Brem, A. Sloan, M. S. Berger, S. Chang, and Glioma Outcomes Investigators, “Survival following surgery and prognostic factors for recently diagnosed malignant glioma: data from the Glioma Outcomes Project,” J. Neurosurg. 99(3), 467–473 (2003).
[Crossref] [PubMed]

Brokinkel, B.

M. Jaber, C. Ewelt, J. Wölfer, B. Brokinkel, C. Thomas, M. Hasselblatt, O. Grauer, and W. Stummer, “Is Visible Aminolevulinic Acid-Induced Fluorescence an Independent Biomarker for Prognosis in Histologically Confirmed (World Health Organization 2016) Low-Grade Gliomas?” Neurosurgery (2018).
[Crossref] [PubMed]

Cavenee, W. K.

D. N. Louis, A. Perry, G. Reifenberger, A. von Deimling, D. Figarella-Branger, W. K. Cavenee, H. Ohgaki, O. D. Wiestler, P. Kleihues, and D. W. Ellison, “The 2016 World Health Organization Classification of Tumors of the Central Nervous System: a summary,” Acta Neuropathol. 131(6), 803–820 (2016).
[Crossref] [PubMed]

Chang, S.

E. R. Laws, I. F. Parney, W. Huang, F. Anderson, A. M. Morris, A. Asher, K. O. Lillehei, M. Bernstein, H. Brem, A. Sloan, M. S. Berger, S. Chang, and Glioma Outcomes Investigators, “Survival following surgery and prognostic factors for recently diagnosed malignant glioma: data from the Glioma Outcomes Project,” J. Neurosurg. 99(3), 467–473 (2003).
[Crossref] [PubMed]

Chelakkot, V. S.

E. Yoshioka, V. S. Chelakkot, M. Licursi, S. G. Rutihinda, J. Som, L. Derwish, J. J. King, T. Pongnopparat, K. Mearow, M. Larijani, A. M. Dorward, and K. Hirasawa, “Enhancement of Cancer-Specific Protoporphyrin IX Fluorescence by Targeting Oncogenic Ras/MEK Pathway,” Theranostics 8(8), 2134–2146 (2018).
[Crossref] [PubMed]

Cho, H. R.

S. Kim, J. E. Kim, Y. H. Kim, T. Hwang, S. K. Kim, W. J. Xu, J.-Y. Shin, J.-I. Kim, H. Choi, H. C. Kim, H. R. Cho, A. Choi, T. Chowdhury, Y. Seo, Y.-S. Dho, J. W. Kim, D. G. Kim, S.-H. Park, H. Kim, S. H. Choi, S. Park, S.-H. Lee, and C.-K. Park, “Glutaminase 2 expression is associated with regional heterogeneity of 5-aminolevulinic acid fluorescence in glioblastoma,” Sci. Rep. 7(1), 12221 (2017).
[Crossref] [PubMed]

Choi, A.

S. Kim, J. E. Kim, Y. H. Kim, T. Hwang, S. K. Kim, W. J. Xu, J.-Y. Shin, J.-I. Kim, H. Choi, H. C. Kim, H. R. Cho, A. Choi, T. Chowdhury, Y. Seo, Y.-S. Dho, J. W. Kim, D. G. Kim, S.-H. Park, H. Kim, S. H. Choi, S. Park, S.-H. Lee, and C.-K. Park, “Glutaminase 2 expression is associated with regional heterogeneity of 5-aminolevulinic acid fluorescence in glioblastoma,” Sci. Rep. 7(1), 12221 (2017).
[Crossref] [PubMed]

Choi, H.

S. Kim, J. E. Kim, Y. H. Kim, T. Hwang, S. K. Kim, W. J. Xu, J.-Y. Shin, J.-I. Kim, H. Choi, H. C. Kim, H. R. Cho, A. Choi, T. Chowdhury, Y. Seo, Y.-S. Dho, J. W. Kim, D. G. Kim, S.-H. Park, H. Kim, S. H. Choi, S. Park, S.-H. Lee, and C.-K. Park, “Glutaminase 2 expression is associated with regional heterogeneity of 5-aminolevulinic acid fluorescence in glioblastoma,” Sci. Rep. 7(1), 12221 (2017).
[Crossref] [PubMed]

Choi, S. H.

S. Kim, J. E. Kim, Y. H. Kim, T. Hwang, S. K. Kim, W. J. Xu, J.-Y. Shin, J.-I. Kim, H. Choi, H. C. Kim, H. R. Cho, A. Choi, T. Chowdhury, Y. Seo, Y.-S. Dho, J. W. Kim, D. G. Kim, S.-H. Park, H. Kim, S. H. Choi, S. Park, S.-H. Lee, and C.-K. Park, “Glutaminase 2 expression is associated with regional heterogeneity of 5-aminolevulinic acid fluorescence in glioblastoma,” Sci. Rep. 7(1), 12221 (2017).
[Crossref] [PubMed]

Chowdhury, T.

S. Kim, J. E. Kim, Y. H. Kim, T. Hwang, S. K. Kim, W. J. Xu, J.-Y. Shin, J.-I. Kim, H. Choi, H. C. Kim, H. R. Cho, A. Choi, T. Chowdhury, Y. Seo, Y.-S. Dho, J. W. Kim, D. G. Kim, S.-H. Park, H. Kim, S. H. Choi, S. Park, S.-H. Lee, and C.-K. Park, “Glutaminase 2 expression is associated with regional heterogeneity of 5-aminolevulinic acid fluorescence in glioblastoma,” Sci. Rep. 7(1), 12221 (2017).
[Crossref] [PubMed]

Chretien, F.

M. Zanello, F. Poulon, J. Pallud, P. Varlet, H. Hamzeh, G. Abi Lahoud, F. Andreiuolo, A. Ibrahim, M. Pages, F. Chretien, F. Di Rocco, E. Dezamis, F. Nataf, B. Turak, B. Devaux, and D. Abi Haidar, “Multimodal optical analysis discriminates freshly extracted human sample of gliomas, metastases and meningiomas from their appropriate controls,” Sci. Rep. 7(1), 41724 (2017).
[Crossref] [PubMed]

Cohen-Gadol, A. A.

Y. Li, R. Rey-Dios, D. W. Roberts, P. A. Valdés, and A. A. Cohen-Gadol, “Intraoperative Fluorescence-Guided Resection of High-Grade Gliomas: A Comparison of the Present Techniques and Evolution of Future Strategies,” World Neurosurg. 82(1-2), 175–185 (2014).
[Crossref] [PubMed]

Costantino, G.

R. Maugeri, A. Villa, M. Pino, A. Imperato, G. R. Giammalva, G. Costantino, F. Graziano, C. Gulì, F. Meli, N. Francaviglia, and D. G. Iacopino, “With a Little Help from My Friends: The Role of Intraoperative Fluorescent Dyes in the Surgical Management of High-Grade Gliomas,” Brain Sci. 8(2), 31 (2018).
[Crossref] [PubMed]

Croce, A. C.

A. C. Croce and G. Bottiroli, “Autofluorescence spectroscopy and imaging: a tool for biomedical research and diagnosis,” Eur. J. Histochem. 58(4), 2461 (2014).
[Crossref] [PubMed]

Czech, T.

B. Kiesel, M. Mischkulnig, A. Woehrer, M. Martinez-Moreno, M. Millesi, A. Mallouhi, T. Czech, M. Preusser, J. A. Hainfellner, S. Wolfsberger, E. Knosp, and G. Widhalm, “Systematic histopathological analysis of different 5-aminolevulinic acid-induced fluorescence levels in newly diagnosed glioblastomas,” J. Neurosurg. 129(2), 341–353 (2018).
[Crossref] [PubMed]

Davis, S. C.

J. J. Bravo, J. D. Olson, S. C. Davis, D. W. Roberts, K. D. Paulsen, and S. C. Kanick, “Hyperspectral data processing improves PpIX contrast during fluorescence guided surgery of human brain tumors,” Sci. Rep. 7(1), 9455 (2017).
[Crossref] [PubMed]

M. Marois, J. Bravo, S. C. Davis, and S. C. Kanick, “Characterization and standardization of tissue-simulating protoporphyrin IX optical phantoms,” J. Biomed. Opt. 21(3), 303003 (2016).
[Crossref] [PubMed]

Derwish, L.

E. Yoshioka, V. S. Chelakkot, M. Licursi, S. G. Rutihinda, J. Som, L. Derwish, J. J. King, T. Pongnopparat, K. Mearow, M. Larijani, A. M. Dorward, and K. Hirasawa, “Enhancement of Cancer-Specific Protoporphyrin IX Fluorescence by Targeting Oncogenic Ras/MEK Pathway,” Theranostics 8(8), 2134–2146 (2018).
[Crossref] [PubMed]

Devaux, B.

M. Zanello, F. Poulon, J. Pallud, P. Varlet, H. Hamzeh, G. Abi Lahoud, F. Andreiuolo, A. Ibrahim, M. Pages, F. Chretien, F. Di Rocco, E. Dezamis, F. Nataf, B. Turak, B. Devaux, and D. Abi Haidar, “Multimodal optical analysis discriminates freshly extracted human sample of gliomas, metastases and meningiomas from their appropriate controls,” Sci. Rep. 7(1), 41724 (2017).
[Crossref] [PubMed]

Dezamis, E.

M. Zanello, F. Poulon, J. Pallud, P. Varlet, H. Hamzeh, G. Abi Lahoud, F. Andreiuolo, A. Ibrahim, M. Pages, F. Chretien, F. Di Rocco, E. Dezamis, F. Nataf, B. Turak, B. Devaux, and D. Abi Haidar, “Multimodal optical analysis discriminates freshly extracted human sample of gliomas, metastases and meningiomas from their appropriate controls,” Sci. Rep. 7(1), 41724 (2017).
[Crossref] [PubMed]

Dho, Y.-S.

S. Kim, J. E. Kim, Y. H. Kim, T. Hwang, S. K. Kim, W. J. Xu, J.-Y. Shin, J.-I. Kim, H. Choi, H. C. Kim, H. R. Cho, A. Choi, T. Chowdhury, Y. Seo, Y.-S. Dho, J. W. Kim, D. G. Kim, S.-H. Park, H. Kim, S. H. Choi, S. Park, S.-H. Lee, and C.-K. Park, “Glutaminase 2 expression is associated with regional heterogeneity of 5-aminolevulinic acid fluorescence in glioblastoma,” Sci. Rep. 7(1), 12221 (2017).
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Di Rocco, F.

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A. Nabavi, P. M. Black, D. T. Gering, C.-F. Westin, V. Mehta, R. S. Pergolizzi, M. Ferrant, S. K. Warfield, N. Hata, R. B. Schwartz, W. M. Wells, R. Kikinis, and F. A. Jolesz, “Serial intraoperative magnetic resonance imaging of brain shift,” Neurosurgery 48(4), 787–797, discussion 797–798 (2001).
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Hadjipanayis, C. G.

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P. A. Valdés, V. Jacobs, B. T. Harris, B. C. Wilson, F. Leblond, K. D. Paulsen, and D. W. Roberts, “Quantitative fluorescence using 5-aminolevulinic acid-induced protoporphyrin IX biomarker as a surgical adjunct in low-grade glioma surgery,” J. Neurosurg. 123(3), 771–780 (2015).
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M. Zanello, F. Poulon, J. Pallud, P. Varlet, H. Hamzeh, G. Abi Lahoud, F. Andreiuolo, A. Ibrahim, M. Pages, F. Chretien, F. Di Rocco, E. Dezamis, F. Nataf, B. Turak, B. Devaux, and D. Abi Haidar, “Multimodal optical analysis discriminates freshly extracted human sample of gliomas, metastases and meningiomas from their appropriate controls,” Sci. Rep. 7(1), 41724 (2017).
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R. Maugeri, A. Villa, M. Pino, A. Imperato, G. R. Giammalva, G. Costantino, F. Graziano, C. Gulì, F. Meli, N. Francaviglia, and D. G. Iacopino, “With a Little Help from My Friends: The Role of Intraoperative Fluorescent Dyes in the Surgical Management of High-Grade Gliomas,” Brain Sci. 8(2), 31 (2018).
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P. A. Valdés, V. Jacobs, B. T. Harris, B. C. Wilson, F. Leblond, K. D. Paulsen, and D. W. Roberts, “Quantitative fluorescence using 5-aminolevulinic acid-induced protoporphyrin IX biomarker as a surgical adjunct in low-grade glioma surgery,” J. Neurosurg. 123(3), 771–780 (2015).
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A. Johansson, G. Palte, O. Schnell, J.-C. Tonn, J. Herms, and H. Stepp, “5-Aminolevulinic Acid-induced Protoporphyrin IX Levels in Tissue of Human Malignant Brain Tumors,” Photochem. Photobiol. 86(6), 1373–1378 (2010).
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A. Nabavi, P. M. Black, D. T. Gering, C.-F. Westin, V. Mehta, R. S. Pergolizzi, M. Ferrant, S. K. Warfield, N. Hata, R. B. Schwartz, W. M. Wells, R. Kikinis, and F. A. Jolesz, “Serial intraoperative magnetic resonance imaging of brain shift,” Neurosurgery 48(4), 787–797, discussion 797–798 (2001).
[PubMed]

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T. Yoneda, N. Nonoguchi, N. Ikeda, R. Yagi, S. Kawabata, M. Furuse, Y. Hirose, H. Kuwabara, Y. Tamura, Y. Kajimoto, and T. Kuroiwa, “Spectral Radiance of Protoporphyrin IX Fluorescence and Its Histopathological Implications in 5-Aminolevulinic Acid-Guided Surgery for Glioblastoma,” Photomed. Laser Surg. 36(5), 266–272 (2018).
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[Crossref] [PubMed]

B. Kiesel, M. Mischkulnig, A. Woehrer, M. Martinez-Moreno, M. Millesi, A. Mallouhi, T. Czech, M. Preusser, J. A. Hainfellner, S. Wolfsberger, E. Knosp, and G. Widhalm, “Systematic histopathological analysis of different 5-aminolevulinic acid-induced fluorescence levels in newly diagnosed glioblastomas,” J. Neurosurg. 129(2), 341–353 (2018).
[Crossref] [PubMed]

Kikinis, R.

A. Nabavi, P. M. Black, D. T. Gering, C.-F. Westin, V. Mehta, R. S. Pergolizzi, M. Ferrant, S. K. Warfield, N. Hata, R. B. Schwartz, W. M. Wells, R. Kikinis, and F. A. Jolesz, “Serial intraoperative magnetic resonance imaging of brain shift,” Neurosurgery 48(4), 787–797, discussion 797–798 (2001).
[PubMed]

Kim, A.

P. A. Valdés, F. Leblond, A. Kim, B. T. Harris, B. C. Wilson, X. Fan, T. D. Tosteson, A. Hartov, S. Ji, K. Erkmen, N. E. Simmons, K. D. Paulsen, and D. W. Roberts, “Quantitative fluorescence in intracranial tumor: implications for ALA-induced PpIX as an intraoperative biomarker,” J. Neurosurg. 115(1), 11–17 (2011).
[Crossref] [PubMed]

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K. Omoto, R. Matsuda, I. Nakagawa, Y. Motoyama, and H. Nakase, “False-positive inflammatory change mimicking glioblastoma multiforme under 5-aminolevulinic acid-guided surgery: A case report,” Surg. Neurol. Int. 9(1), 49 (2018).
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K. Omoto, R. Matsuda, I. Nakagawa, Y. Motoyama, and H. Nakase, “False-positive inflammatory change mimicking glioblastoma multiforme under 5-aminolevulinic acid-guided surgery: A case report,” Surg. Neurol. Int. 9(1), 49 (2018).
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K. Omoto, R. Matsuda, I. Nakagawa, Y. Motoyama, and H. Nakase, “False-positive inflammatory change mimicking glioblastoma multiforme under 5-aminolevulinic acid-guided surgery: A case report,” Surg. Neurol. Int. 9(1), 49 (2018).
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S. Kröger, A.-C. Niehoff, A. Jeibmann, M. Sperling, W. Paulus, W. Stummer, and U. Karst, “Complementary Molecular and Elemental Mass-Spectrometric Imaging of Human Brain Tumors Resected by Fluorescence-Guided Surgery,” Anal. Chem. 90(20), 12253–12260 (2018).
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P. A. Valdés, A. Kim, M. Brantsch, C. Niu, Z. B. Moses, T. D. Tosteson, B. C. Wilson, K. D. Paulsen, D. W. Roberts, and B. T. Harris, “δ-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(8), 846–856 (2011).
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J. J. Bravo, J. D. Olson, S. C. Davis, D. W. Roberts, K. D. Paulsen, and S. C. Kanick, “Hyperspectral data processing improves PpIX contrast during fluorescence guided surgery of human brain tumors,” Sci. Rep. 7(1), 9455 (2017).
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S. Kröger, A.-C. Niehoff, A. Jeibmann, M. Sperling, W. Paulus, W. Stummer, and U. Karst, “Complementary Molecular and Elemental Mass-Spectrometric Imaging of Human Brain Tumors Resected by Fluorescence-Guided Surgery,” Anal. Chem. 90(20), 12253–12260 (2018).
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K. Petrecca, M.-C. Guiot, V. Panet-Raymond, and L. Souhami, “Failure pattern following complete resection plus radiotherapy and temozolomide is at the resection margin in patients with glioblastoma,” J. Neurooncol. 111(1), 19–23 (2013).
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N. Sanai, M.-Y. Polley, M. W. McDermott, A. T. Parsa, and M. S. Berger, “An extent of resection threshold for newly diagnosed glioblastomas,” J. Neurosurg. 115(1), 3–8 (2011).
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W. Stummer, U. Pichlmeier, T. Meinel, O. D. Wiestler, F. Zanella, and H.-J. Reulen, “Fluorescence-guided surgery with 5-aminolevulinic acid for resection of malignant glioma: a randomised controlled multicentre phase III trial,” Lancet Oncol. 7(5), 392–401 (2006).
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P. A. Valdés, V. Jacobs, B. T. Harris, B. C. Wilson, F. Leblond, K. D. Paulsen, and D. W. Roberts, “Quantitative fluorescence using 5-aminolevulinic acid-induced protoporphyrin IX biomarker as a surgical adjunct in low-grade glioma surgery,” J. Neurosurg. 123(3), 771–780 (2015).
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Figures (6)

Fig. 1
Fig. 1 Drawing of the setup with a picture of the end of the probe.
Fig. 2
Fig. 2 Data processing: removing of autofluorescence (a) and fit of PpIX and lipofuscin contribution (b). Experimental data (solid black line), fit (solid red curve), normalized spectrum by the autofluorescence (dotted black line), lipofuscin (solid green line), State 620 (dotted blue) and State 634 (dotted purple) measured in a low density margin of a patient aged 55 years old presenting an high grade glioma.
Fig. 3
Fig. 3 Mean and standard error of State 634 contribution versus the ones of State 620 for each class: HGG solid part (red star); HGG margins (purple diamond) HGG margins of low density (blue square), LGG (grey circle) and healthy tissues (green triangle). Insert at the top right is a zoom for the low values of state 634.
Fig. 4
Fig. 4 Ratio of the contribution of State 620 over the one of State 634 for each class.
Fig. 5
Fig. 5 SNR634 versus SNR620 for HGG, with a zoom. Markers indicate anatomo-histopathological classification: solid part of HGG (red stars), HGG margins (orange diamonds), HGG margins with low density of tumor cells (blue squares) and healthy tissues (green triangles). Dotted line shows the equality of both SNR contributions.
Fig. 6
Fig. 6 SNR634 versus SNR620 for LGG. Markers reveal anatomo-histopathological classification: LGG (black circles) and healthy tissues (green triangle). Dotted line shows the equality of both SNR contributions.

Tables (1)

Tables Icon

Table 1 mean value and standard error of estimated biomarkers: fluorescence intensity between 600 nm and 650 nm; Central wavelength and contribution of each state.

Equations (1)

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S(λ)= α 620 S 620 (λ)+ α 634 S 634 (λ)+ A lipo exp( (λ λ lipo ) 2 2 σ lipo 2 )

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