Combined fluorescence and reflectance spectroscopy for in vivo quantification of cancer biomarkers in low- and high-grade glioma surgery

Journal of Biomedical Optics

Volumn 16, Issue 11, 2011, Pages

  Valdés, Pablo A ^a,b,g   Kim, Anthony ^c   Leblond, Frederic ^a   Conde, Olga M ^d   Harris, Brent T ^e   Paulsen, Keith D ^a,f   Wilson, Brian C ^c   Roberts, David W ^f,g  

^a DARTMOUTH COLLEGE   (United States)

^b DARTMOUTH MEDICAL SCHOOL   (United States)

^c UNIVERSITY OF TORONTO   (Canada)

^d UNIVERSITY OF CANTABRIA   (Spain)

^e GEORGETOWN UNIVERSITY MEDICAL CENTER   (United States)

^f NORRIS COTTON CANCER CENTER   (United States)

^g DARTMOUTH HITCHCOCK MEDICAL CENTER   (United States)

Author keywords

5 aminolevulinic acid; cancer biomarkers; fluorescence guided resection; glioma; optical spectroscopy; protoporphyrin IX

Indexed keywords

5-AMINOLEVULINIC ACID; CANCER BIOMARKERS; FLUORESCENCE-GUIDED RESECTION; GLIOMA; OPTICAL SPECTROSCOPY; PROTOPORPHYRIN IX;

BIOMARKERS; DIAGNOSIS; DISEASES; FLUORESCENCE; HEMOGLOBIN OXYGEN SATURATION; REFLECTION; SCATTERING PARAMETERS; SPECTROSCOPY; SURGERY;

TUMORS;

AMINOLEVULINIC ACID; PROTOPORPHYRIN; TUMOR MARKER;

ARTICLE; BIOLOGICAL MODEL; CHEMISTRY; COMPUTER ASSISTED SURGERY; DIAGNOSTIC IMAGING; GLIOMA; HUMAN; METABOLISM; METHODOLOGY; NONPARAMETRIC TEST; PATHOLOGY; SENSITIVITY AND SPECIFICITY; SPECTROFLUOROMETRY; SUPPORT VECTOR MACHINE;

AMINOLEVULINIC ACID; DIAGNOSTIC IMAGING; GLIOMA; HUMANS; MODELS, BIOLOGICAL; PROTOPORPHYRINS; SENSITIVITY AND SPECIFICITY; SPECTROMETRY, FLUORESCENCE; STATISTICS, NONPARAMETRIC; SUPPORT VECTOR MACHINES; SURGERY, COMPUTER-ASSISTED; TUMOR MARKERS, BIOLOGICAL;

EID: 80655142501     PISSN: 10833668     EISSN: 15602281     Source Type: Journal    
DOI: 10.1117/1.3646916     Document Type: Article

References (70)

1. L. M. DeAngelis, Brain tumors., N. Engl. J. Med. 344 (2), 114-123 (2001). 10.1056/NEJM200101113440207 (Pubitemid 32052502)
2. M. Jansen, S. Yip, and D. N. Louis, Molecular pathology in adult gliomas: diagnostic, prognostic, and predictive markers., Lancet Neurol. 9 (7), 717-726 (2010). 10.1016/S1474-4422(10)70105-8
3. M. Lacroix, D. Abi-Said, D. R. Fourney, Z. L. Gokaslan, W. Shi, F. DeMonte, F. F. Lang, I. E. McCutcheon, S. J. Hassenbusch, E. Holland, K. Hess, C. Michael, D. Miller, and R. Sawaya, A multivariate analysis of 416 patients with glioblastoma multiforme: prognosis, extent of resection, and survival., J. Neurosurg. 95 (2), 190-198 (2001). 10.3171/jns.2001.95.2.0190 (Pubitemid 32799739)
4. B. W. Pogue, S. Gibbs-Strauss, P. A. Valdes, K. Samkoe, D. W. Roberts, and K. D. Paulsen, Review of neurosurgical fluorescence imaging methodologies., IEEE J. Sel. Top. Quantum Electron. 16 (3), 493-505 (2010). 10.1109/JSTQE.2009. 2034541
5. E. G. Van Meir, C. G. Hadjipanayis, A. D. Norden, H. K. Shu, P. Y. Wen and J. J. Olson, Exciting new advances in neuro-oncology: the avenue to a cure for malignant glioma., Ca-Cancer J. Clin. 60 (3), 166-193 (2010). 10.3322/caac.20069
6. F. W. Floeth and W. Stummer, The value of metabolic imaging in diagnosis and resection of cerebral gliomas., Nat. Clin. Pract. Neurol. 1 (2), 62-63 (2005). 10.1038/ncpneuro0043
7. P. A. Valdes, 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). 10.3171/2011.2.JNS101451
8. F. K. Albert, M. Forsting, K. Sartor, H. P. Adams, and S. Kunze, Early postoperative magnetic resonance imaging after resection of malignant glioma: objective evaluation of residual tumor and its influence on regrowth and prognosis., Neurosurgery 34 (1), 45-60; discussion 60-41 (1994). 10.1227/00006123-199401000-00008
9. M. J. McGirt, K. L. Chaichana, M. Gathinji, F. J. Attenello, K. Than, A. Olivi, J. D. Weingart, H. Brem, and A. R. Quinones-Hinojosa, Independent association of extent of resection with survival in patients with malignant brain astrocytoma., J. Neurosurg. 110 (1), 156-162 (2009). 10.3171/2008.4.17536
10. 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). 10.1016/S1470-2045(06)70665-9
11. 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). 10.1111/j.1751-1097.2010.00799.x
12. D. W. Roberts, P. A. Valdes, B. T. Harris, K. M. Fontaine, A. Hartov, X. Fan, S. Ji, S. S. Lollis, B. W. Pogue, F. Leblond, T. D. Tosteson, B. C. Wilson, and K. D. Paulsen, Coregistered fluorescence-enhanced tumor resection of malignant glioma: relationships between delta-aminolevulinic acid-induced protoporphyrin IX fluorescence, magnetic resonance imaging enhancement, and neuropathological parameters., J. Neurosurg. 114 (3), 595-603 (2011). 10.3171/2010.2.JNS091322
13. W. Stummer, A. Novotny, H. Stepp, C. Goetz, K. Bise, and H. J. Reulen, Fluorescence-guided resection of glioblastoma multiforme by using 5-aminolevulinic acid-induced porphyrins: a prospective study in 52 consecutive patients., J. Neurosurg. 93 (6), 1003-1013 (2000). 10.3171/jns.2000.93.6.1003 (Pubitemid 32800611)
14. P. A. Valdes, 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, -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). 10.1093/neuonc/nor086
15. J. C. Richter, N. Haj-Hosseini, S. Andersson-Engel, and K. Wardell, Fluorescence spectroscopy measurements in ultrasonic navigated resection of malignant brain tumors., Lasers Surg. Med. 43 (1), 8-14 (2011). 10.1002/lsm.21022
16. R. Weissleder and M. J. Pittet, Imaging in the era of molecular oncology., Nature 452 (7187), 580-589 (2008). 10.1038/nature06917 (Pubitemid 351483372)
17. P. Y. Wen and S. Kesari, Malignant gliomas in adults., N. Engl. J. Med. 359 (5), 492-507 (2008). 10.1056/NEJMra0708126
18. P. A. Valdes, X. Fan, S. Ji, B. T. Harris, K. D. Paulsen, and D. W. Roberts, Estimation of brain deformation for volumetric image updating in protoporphyrin IX fluorescence-guided resection., Stereotact. Funct. Neurosurg. 88 (1), 1-10 (2010). 10.1159/000258143
19. 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). 10.1117/1.3523616
20. A. Kim, M. Roy, F. Dadani, and B. C. Wilson, A fiberoptic reflectance probe with multiple source-collector separations to increase the dynamic range of derived tissue optical absorption and scattering coefficients., Opt. Express 18 (6), 5580-5594 (2010). 10.1364/OE.18.005580
21. J. Wu, M. S. Feld, and R. P. Rava, Analytical model for extracting intrinsic fluorescence in turbid media., Appl. Opt. 32 (19), 3585-3595 (1993). 10.1364/AO.32.003585
22. R. Weersink, M. S. Patterson, K. Diamond, S. Silver, and N. Padgett, Noninvasive measurement of fluorophore concentration in turbid media with a simple fluorescence reflectance ratio technique., Appl. Opt. 40 (34), 6389-6395 (2001). 10.1364/AO.40.006389
23. M. G. Muller, I. Georgakoudi, Q. Zhang, J. Wu, and M. S. Feld, Intrinsic fluorescence spectroscopy in turbid media: disentangling effects of scattering and absorption., Appl. Opt. 40 (25), 4633-4646 (2001). 10.1364/AO.40.004633
24. J. S. Dysart and M. S. Patterson, Photobleaching kinetics, photoproduct formation, and dose estimation during ALA induced PpIX PDT of MLL cells under well oxygenated and hypoxic conditions., Photochem. Photobiol. Sci. 5 (1), 73-81 (2006). 10.1039/b511807g
25. D. N. Louis, H. Ohgaki, O. D. Wiestler, W. K. Cavenee, P. C. Burger, A. Jouvet, B. W. Scheithauer, and P. Kleihues, The 2007 WHO classification of tumours of the central nervous system., Acta Neuropathol. 114 (2), 97-109 (2007). 10.1007/s00401-007-0243-4 (Pubitemid 47103521)
26. D. E. Shapiro, The interpretation of diagnostic tests., Stat. Methods Med. Res. 8 (2), 113-134 (1999). 10.1191/096228099666928387 (Pubitemid 29425899)
27. N. Haj-Hosseini, J. Richter, S. Andersson-Engels and K. Wardell, Optical touch pointer for fluorescence guided glioblastoma resection using 5-aminolevulinic acid., Lasers Surg. Med. 42 (1), 9-14 (2010). 10.1002/lsm.20868
28. R. Ishihara, Y. Katayama, T. Watanabe, A. Yoshino, T. Fukushima and K. Sakatani, Quantitative spectroscopic analysis of 5-aminolevulinic acid-induced protoporphyrin IX fluorescence intensity in diffusely infiltrating astrocytomas., Neurol. Med. Chir. (Tokyo) 47 (2), 53-57; discussion 57 (2007). 10.2176/nmc.47.53
29. W. C. Lin, D. I. Sandberg, S. Bhatia, M. Johnson, G. Morrison, and J. Ragheb, Optical spectroscopy for in-vitro differentiation of pediatric neoplastic and epileptogenic brain lesions., J. Biomed. Opt. 14 (1), 014028 (2009). 10.1117/1.3080144
30. W. C. Lin, D. I. Sandberg, S. Bhatia, M. Johnson, S. Oh, and J. Ragheb, Diffuse reflectance spectroscopy for in vivo pediatric brain tumor detection., J. Biomed. Opt. 15 (6), 061709 (2010). 10.1117/1.3505012
31. W. C. Lin, S. A. Toms, M. Johnson, E. D. Jansen, and A. Mahadevan-Jansen, In vivo brain tumor demarcation using optical spectroscopy., Photochem. Photobiol. 73 (4), 396-402 (2001). 10.1562/0031-8655(2001)0730396:IVBTDU2.0.CO;2
32. L. Marcu, J. A. Jo, P. V. Butte, W. H. Yong, B. K. Pikul, K. L. Black, and R. C. Thompson, Fluorescence lifetime spectroscopy of glioblastoma multiforme., Photochem. Photobiol. 80, 98-103 (2004). 10.1562/2003-12-09-RA-023. 1
33. S. K. Majumder, S. Gebhart, M. D. Johnson, R. Thompson, W. C. Lin, and A. Mahadevan-Jansen, A probability-based spectroscopic diagnostic algorithm for simultaneous discrimination of brain tumor and tumor margins from normal brain tissue., Appl. Spectrosc. 61 (5), 548-557 (2007). 10.1366/000370207780807704 (Pubitemid 46770369)
34. P. V. Butte, Q. Fang, J. A. Jo, W. H. Yong, B. K. Pikul, K. L. Black, and L. Marcu, Intraoperative delineation of primary brain tumors using time-resolved fluorescence spectroscopy., J. Biomed. Opt. 15 (2), 027008 (2010). 10.1117/1.3374049
35. P. V. Butte, A. N. Mamelak, M. Nuno, S. I. Bannykh, K. L. Black, and L. Marcu, Fluorescence lifetime spectroscopy for guided therapy of brain tumors., Neuroimage 54S1, S125-S135 (2011). 10.1016/j.neuroimage.2010.11.001
36. N. Ramanujam, Fluorescence spectroscopy of neoplastic and non-neoplastic tissues., Neoplasia 2 (1-2), 89-117 (2000). 10.1038/sj.neo.7900077 (Pubitemid 30123183)
37. R. Richards-Kortum and E. Sevick-Muraca, Quantitative optical spectroscopy for tissue diagnosis., Annu. Rev. Phys. Chem. 47, 555-606 (1996). 10.1146/annurev.physchem.47.1.555 (Pubitemid 126416975)
38. K. Sokolov, M. Follen, and R. Richards-Kortum, Optical spectroscopy for detection of neoplasia., Curr. Opin. Chem. Biol. 6 (5), 651-658 (2002). 10.1016/S1367-5931(02)00381-2 (Pubitemid 35284197)
39. S. A. Toms, P. E. Konrad, W. C. Lin, and R. J. Weil, Neuro-oncological applications of optical spectroscopy., Technol. Cancer Res. Treat. 5 (3), 231-238 (2006). (Pubitemid 43946256)
40. S. A. Toms, W. C. Lin, R. J. Weil, M. D. Johnson, E. D. Jansen, and A. Mahadevan-Jansen, Intraoperative optical spectroscopy identifies infiltrating glioma margins with high sensitivity., Neurosurgery 57 (4 Suppl), 382-391; discussion 382-391 (2005). 10.1227/01.NEU.000176855.39826.2D (Pubitemid 41464062)
41. W. H. Yong, P. V. Butte, B. K. Pikul, J. A. Jo, Q. Fang, T. Papaioannou, K. Black, and L. Marcu, Distinction of brain tissue, low grade and high grade glioma with time-resolved fluorescence spectroscopy., Front Biosci. 11, 1255-1263 (2006). 10.2741/1878 (Pubitemid 43253417)
42. C. J. C. Burges, A tutorial on support vector machines for pattern recognition., Data Min. Knowl. Discov. 2 (2), 121-167 (1998). 10.1023/A:1009715923555 (Pubitemid 128126769)
43. R. O. Duda, P. E. Hart, and D. G. Stork, Pattern classification, Wiley, New York (2001).
44. W. S. Noble, What is a support vector machine, Nat. Biotechnol. 24 (12), 1565-1567 (2006). 10.1038/nbt1206-1565 (Pubitemid 44967481)
45. R. G. Brereton and G. R. Lloyd, Support vector machines for classification and regression., Analyst 135 (2), 230-267 (2010). 10.1039/b918972f
46. M. S. Eljamel, G. Leese and H. Moseley, Intraoperative optical identification of pituitary adenomas., J. Neuro-Oncol. 92 (3), 417-421 (2009). 10.1007/s11060-009-9820-9
47. M. Hefti, G. von Campe, M. Moschopulos, A. Siegner, H. Looser, and H. Landolt, 5-aminolevulinic acid induced protoporphyrin IX fluorescence in high-grade glioma surgery: a one-year experience at a single institutuion., Swiss Med. Wkly. 138 (11-12), 180-185 (2008).
48. T. Kuroiwa, Y. Kajimoto, and T. Ohta, Comparison between operative findings on malignant glioma by a fluorescein surgical microscopy and histological findings., Neurol. Res. 21 (1), 130-134 (1999). (Pubitemid 29100389)
49. A. Nabavi, H. Thurm, B. Zountsas, T. Pietsch, H. Lanfermann, U. Pichlmeier, and M. Mehdorn, Five-aminolevulinic acid for fluorescence-guided resection of recurrent malignant gliomas: a phase ii study., Neurosurgery 65 (6), 1070-1076; discussion 1076-1077 (2009). 10.1227/01.NEU.0000360128.03597.C7
50. U. Pichlmeier, A. Bink, G. Schackert, and W. Stummer, Resection and survival in glioblastoma multiforme: an RTOG recursive partitioning analysis of ALA study patients., J. Neuro-Oncol. 10 (6), 1025-1034 (2008). 10.1215/15228517-2008-052
51. W. Stummer, H. J. Reulen, T. Meinel, U. Pichlmeier, W. Schumacher, J. C. Tonn, V. Rohde, F. Oppel, B. Turowski, C. Woiciechowsky, K. Franz, and T. Pietsch, Extent of resection and survival in glioblastoma multiforme: identification of and adjustment for bias., Neurosurgery 62 (3), 564-576; discussion 564-576 (2008). 10.1227/01.neu.0000317304.31579.17
52. S. Utsuki, N. Miyoshi, H. Oka, Y. Miyajima, S. Shimizu, S. Suzuki, and K. Fujii, Fluorescence-guided resection of metastatic brain tumors using a 5-aminolevulinic acid-induced protoporphyrin IX: pathological study., Brain Tumor Pathol. 24 (2), 53-55 (2007). 10.1007/s10014-007-0223-3 (Pubitemid 350165714)
53. J. D. Johansson, Spectroscopic method for determination of the absorption coefficient in brain tissue., J. Biomed. Opt. 15 (5), 057005 (2010). 10.1117/1.3495719
54. P. V. Butte, B. K. Pikul, A. Hever, W. H. Yong, K. L. Black, and L. Marcu, Diagnosis of meningioma by time-resolved fluorescence spectroscopy., J. Biomed. Opt. 10 (6), 064026 (2005). 10.1117/1.2141624 (Pubitemid 44255979)
55. A. N. Yaroslavsky, P. C. Schulze, I. V. Yaroslavsky, R. Schober, F. Ulrich, and H. J. Schwarzmaier, Optical properties of selected native and coagulated human brain tissues in vitro in the visible and near infrared spectral range., Phys. Med. Biol. 47 (12), 2059-2073 (2002). 10.1088/0031-9155/47/12/305 (Pubitemid 34727494)
56. Z. Volynskaya, A. S. Haka, K. L. Bechtel, M. Fitzmaurice, R. Shenk, N. Wang, J. Nazemi, R. R. Dasari, and M. S. Feld, Diagnosing breast cancer using diffuse reflectance spectroscopy and intrinsic fluorescence spectroscopy., J. Biomed. Opt. 13 (2), 024012 (2008). 10.1117/1.2909672
57. S. C. Gebhart, W. C. Lin, and A. Mahadevan-Jansen, In vitro determination of normal and neoplastic human brain tissue optical properties using inverse adding-doubling., Phys. Med. Biol. 51 (8), 2011-2027 (2006). 10.1088/0031-9155/51/8/004
58. N. N. Boustany, S. A. Boppart, and V. Backman, Microscopic imaging and spectroscopy with scattered light., Annu. Rev. Biomed. Eng. 12, 285-314 (2010). 10.1146/annurev-bioeng-061008-124811
59. W. C. Lin, S. A. Toms, M. Motamedi, E. D. Jansen, and A. Mahadevan-Jansen, Brain tumor demarcation using optical spectroscopy; an in vitro study., J. Biomed. Opt. 5 (2), 214-220 (2000). 10.1117/1.429989
60. R. F. Deighton, R. McGregor, J. Kemp, J. McCulloch, and I. R. Whittle, Glioma pathophysiology: insights emerging from proteomics., Brain Pathol. 20 (4), 691-703 (2010). 10.1111/j.1750-3639.2010.00376.x
61. S. Collaud, A. Juzeniene, J. Moan, and N. Lange, On the selectivity of 5-aminolevulinic acid-induced protoporphyrin IX formation., Curr. Med. Chem. 4 (3), 301-316 (2004). (Pubitemid 38647588)
62. G. L. Semenza, Targeting HIF-1 for cancer therapy., Nat. Rev. Cancer 3 (10), 721-732 (2003). 10.1038/nrc1187 (Pubitemid 37328811)
63. G. Bergers and L. E. Benjamin, Tumorigenesis and the angiogenic switch., Nat. Rev. Cancer 3 (6), 401-410 (2003). 10.1038/nrc1093 (Pubitemid 37328844)
64. D. Liao and R. S. Johnson, Hypoxia: a key regulator of angiogenesis in cancer., Cancer Metastasis Rev. 26 (2), 281-290 (2007). 10.1007/s10555-007-9066- y (Pubitemid 47101669)
65. D. J. Brat and T. B. Mapstone, Malignant glioma physiology: cellular response to hypoxia and its role in tumor progression., Ann. Intern. Med. 138 (8), 659-668 (2003). (Pubitemid 38124658)
66. P. Carmeliet, Mechanisms of angiogenesis and arteriogenesis., Nat. Med. 6 (4), 389-395 (2000). 10.1038/74651 (Pubitemid 30208155)
67. J. T. Grier and T. Batchelor, Low-grade gliomas in adults., Oncologist 11 (6), 681-693 (2006). 10.1634/theoncologist.11-6-681 (Pubitemid 43967623)
68. P. Rolfe, In vivo near-infrared spectroscopy., Annu. Rev. Biomed. Eng. 2, 715-754 (2000). 10.1146/annurev.bioeng.2.1.715
69. S. Srinivasan, B. W. Pogue, S. Jiang, H. Dehghani, C. Kogel, S. Soho, J. J. Gibson, T. D. Tosteson, S. P. Poplack, and K. D. Paulsen, Interpreting hemoglobin and water concentration, oxygen saturation, and scattering measured in vivo by near-infrared breast tomography., Proc. Natl. Acad. Sci. U.S.A. 100 (21), 12349-12354 (2003). 10.1073/pnas.2032822100 (Pubitemid 37271563)
70. O. Ivanciuc, Applications of support vector machines in chemistry., Reviews in Computational Chemistry, K. B. Lipkowitz, and, T. R. Cundari, Eds., pp. 291-400, Wiley, New York (2007).