Gadolinium-and 5-aminolevulinic acid-induced protoporphyrin IX levels in human gliomas: An ex vivo quantitative study to correlate protoporphyrin IX levels and blood-brain barrier breakdown

Journal of Neuropathology and Experimental Neurology

Volumn 71, Issue 9, 2012, Pages 806-813

  Valdés, Pablo A ^a,b,d   Moses, Ziev B ^a   Kim, Anthony ^c   Belden, Clifford J ^d   Wilson, Brian C ^c   Paulsen, Keith D ^b,d   Roberts, David W ^d   Harris, Brent T ^d,e  

^a DARTMOUTH MEDICAL SCHOOL   (United States)

^b DARTMOUTH COLLEGE   (United States)

^c PRINCESS MARGARET HOSPITAL   (Canada)

^d DARTMOUTH HITCHCOCK MEDICAL CENTER   (United States)

^e GEORGETOWN UNIVERSITY MEDICAL CENTER   (United States)

Author keywords

5 Aminolevulinic acid; Contrast enhancement on magnetic resonance imaging; Fluorescence guided surgery; Gadolinium; Mass spectrometry; Microvascular density; Protoporphyrin IX

Indexed keywords

AMINOLEVULINIC ACID; BIOLOGICAL MARKER; CD31 ANTIGEN; GADOLINIUM; PROTOPORPHYRIN;

ARTICLE; ATOMIC EMISSION SPECTROMETRY; BLOOD BRAIN BARRIER; CONTROLLED STUDY; DENSITY; EX VIVO STUDY; FLUORESCENCE IMAGING; GLIOMA; HISTOPATHOLOGY; HUMAN; HUMAN TISSUE; IMMUNOHISTOCHEMISTRY; MAJOR CLINICAL STUDY; MICROVASCULARIZATION; PRIORITY JOURNAL; PROTEIN BLOOD LEVEL; QUANTITATIVE ANALYSIS; TUMOR BIOPSY;

AMINOLEVULINIC ACID; ANTIGENS, CD31; BLOOD-BRAIN BARRIER; BRAIN NEOPLASMS; CRANIOTOMY; CREATININE; FEMALE; GADOLINIUM; GLIOMA; HUMANS; MAGNETIC RESONANCE IMAGING; MALE; MASS SPECTROMETRY; MICROVESSELS; PHOTOSENSITIZING AGENTS; PROTOPORPHYRINS; STATISTICS AS TOPIC; STATISTICS, NONPARAMETRIC;

EID: 84865646305     PISSN: 00223069     EISSN: 15546578     Source Type: Journal    
DOI: 10.1097/NEN.0b013e31826775a1     Document Type: Article

References (48)

1. Albert FK, Forsting M, Sartor K, 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 1994;34:45-60 [discussion-1]
2. Lacroix M, Abi-Said D, Fourney DR, et al. A multivariate analysis of 416 patients with glioblastoma multiforme: Prognosis, extent of resection, and survival. J Neurosurg 2001;95:190-98
3. Sanai N, Berger MS. Glioma extent of resection and its impact on patient outcome. Neurosurgery 2008;62:753-64; [discussion 264-6]
4. Sanai N, Polley MY, McDermott MW, et al. An extent of resection threshold for newly diagnosed glioblastomas. J Neurosurg 2011;115:3-8
5. Pichlmeier U, Bink A, Schackert G, et al. Resection and survival in glioblastoma multiforme: An RTOG recursive partitioning analysis of ALA study patients. Neuro Oncol 2008;10:1025-34
6. Pogue BW, Gibbs-Strauss S, Valdes PA, et al. Review of neurosurgical fluorescence imaging methodologies. IEEE J Sel Top Quantum Electron 2010;16:493-505
7. Roberts DW, Valdes PA, Harris BT, et al. Coregistered fluorescence-enhanced tumor resection of malignant glioma: Relationships between delta-aminolevulinic acidYinduced protoporphyrin IX fluorescence, magnetic resonance imaging enhancement, and neuropathological parameters. J Neurosurg 2011;114:595-603
8. Stummer W, Novotny A, Stepp H, et al. Fluorescence-guided resection of glioblastoma multiforme by using 5-aminolevulinic acidYinduced por-phyrins: A prospective study in 52 consecutive patients. J Neurosurg 2000;93:1003-13
9. Stummer W, Pichlmeier U, Meinel T, et al. Fluorescence-guided surgery with 5-aminolevulinic acid for resection of malignant glioma: A randomised controlled multicentre phase III trial. Lancet Oncol 2006;7: 392-401
10. Stummer W, Reulen HJ, Meinel T, et al. Extent of resection and survival in glioblastoma multiforme: Identification of and adjustment for bias. Neurosurgery 2008;62:564-76; [discussion-76]
11. Stummer W, Reulen HJ, Novotny A, et al. Fluorescence-guided resections of malignant gliomasVAn overview. Acta Neurochir Suppl 2003; 88:9-12
12. Valdes PA, Kim A, Brantsch M, et al. C-Aminolevulinic acid-induced protoporphyrin IX concentration correlates with histopathological markers of malignancy in human gliomas: The need for quantitative fluorescence-guided resection to identify regions of increasing malignancy. Neuro Oncol 2011;13:846-56
13. Roberts DW, Miga MI, Hartov A, et al. Intraoperatively updated neuro-imaging using brain modeling and sparse data. Neurosurgery 1999;45: 1199-206; [discussion 206-7]
14. Sun H, Lunn KE, Farid H, et al. Stereopsis-guided brain shift compensation. IEEE Trans Med Imaging 2005;24:1039-52
15. Valdes PA, Fan X, Ji S, et al. Estimation of brain deformation for volumetric image updating in protoporphyrin IX fluorescenceYguided resection. Stereotact Funct Neurosurg 2010;88:1-10
16. Valdes PA, Leblond F, Kim A, et al. Quantitative fluorescence in intra-cranial tumor: Implications for ALA-induced PpIX as an intraoperative biomarker. J Neurosurg 2011;115:11-7
17. Kim A, Khurana M, Moriyama Y, et al. Quantification of in vivo fluorescence decoupled from the effects of tissue optical properties using fiber-optic spectroscopy measurements. J Biomed Opt 2010;15:067006
18. Richards-Kortum R, Sevick-Muraca E. Quantitative optical spectroscopy for tissue diagnosis. Annu Rev Phys Chem 1996;47:555-606
19. Weersink R, Patterson MS, Diamond K, et al. Noninvasive measurement of fluorophore concentration in turbid media with a simple fluorescence/reflectance ratio technique. Appl Opt 2001;40:6389-95
20. Dijkhuizen RM, Nicolay K. Magnetic resonance imaging in experimental models of brain disorders. J Cereb Blood Flow Metab 2003;23:1383-402
21. Ichikawa H, Itoh K. Blood-arachnoid barrier disruption in experimental rat meningitis detected using gadolinium-enhancement ratio imaging. Brain Res 2011;1390:142-9
22. Knight RA, Barker PB, Fagan SC, et al. Prediction of impending hem-orrhagic transformation in ischemic stroke using magnetic resonance imaging in rats. Stroke 1998;29:144-51
23. Runge VM, Price AC, Wehr CJ, et al. Contrast enhanced MRI. Evaluation of a canine model of osmotic blood-brain barrier disruption. Invest Radiol 1985;20:830-44
24. Schmiedl UP, Kenney J, Maravilla KR. Dyke Award Paper. Kinetics of pathologic blood-brain-barrier permeability in an astrocytic glioma using contrast-enhanced MR. AJNR Am J Neuroradiol 1992;13:5-14
25. Warach S, Latour LL. Evidence of reperfusion injury, exacerbated by thrombolytic therapy, in human focal brain ischemia using a novel imaging marker of early blood-brain barrier disruption. Stroke 2004;35: 2659-61
26. Deeken JF, Loscher W. The blood-brain barrier and cancer: Transporters, treatment, and Trojan horses. Clin Cancer Res 2007;13:1663-74
27. Loreti V, Bettmer J. Determination of the MRI contrast agent Gd-DTPA by SEC-ICP-MS. Anal Bioanal Chem 2004;379:1050-4
28. Weinmann HJ, Brasch RC, Press WR, et al. Characteristics of gadoli-nium-DTPA complex: A potential NMR contrast agent. AJR Am J Roentgenol 1984;142:619-24
29. Kamaly N, Pugh JA, Kalber TL, et al. Imaging of gadolinium spatial distribution in tumor tissue by laser ablation inductively coupled plasma mass spectrometry. Mol Imaging Biol 2010;12:361-6
30. Kindberg GM, Uran S, Friisk G, et al. The fate of Gd and chelate following intravenous injection of gadodiamide in rats. Eur Radiol 2010;20: 1636-43
31. Miles DR, Mesfin M, Mody TD, et al. Validation and use of three complementary analytical methods (LC-FLS, LC-MS/MS and ICP-MS) to evaluate the pharmacokinetics, biodistribution and stability of motex-afin gadolinium in plasma and tissues. Anal Bioanal Chem 2006;385: 345-56
32. Miles DR, Smith JA, Phan SC, et al. Population pharmacokinetics of motexafin gadolinium in adults with brain metastases or glioblastoma multiforme. J Clin Pharmacol 2005;45:299-312
33. Blaum K, Geppert C, Schreiber WG, et al. Trace determination of gadolinium in biomedical samples by diode laserYbased multi-step resonance ionization mass spectrometry. Anal Bioanal Chem 2002;372: 759-65
34. Lilge L, O'Carroll C, Wilson BC. A solubilization technique for photo-sensitizer quantification in ex vivo tissue samples. J Photochem Photobiol B 1997;39:229-35
35. Dysart JS, Patterson MS. Photobleaching kinetics, photoproduct formation, and dose estimation during ALA induced PpIX PDT of MLL cells under well oxygenated and hypoxic conditions. Photochem Photo-biol Sci 2006;5:73-81
36. Frame EM, Uzgiris EE. Gadolinium determination in tissue samples by inductively coupled plasma mass spectrometry and inductively coupled plasma atomic emission spectrometry in evaluation of the action of magnetic resonance imaging contrast agents. Analyst 1998;123:675-9
37. De Stasio G, Casalbore P, Pallini R, et al. Gadolinium in human glio-blastoma cells for gadolinium neutron capture therapy. Cancer Res 2001; 61:4272-7
38. Hasan J, Byers R, Jayson GC. Intra-tumoural microvessel density in human solid tumours. Br J Cancer 2002;86:1566-77
39. Weidner N, Semple JP, Welch WR, et al. Tumor angiogenesis and met-astasisVCorrelation in invasive breast carcinoma. N Engl J Med 1991; 324:1-8
40. Vermeulen PB, Gasparini G, Fox SB, et al. Second international consensus on the methodology and criteria of evaluation of angio-genesis quantification in solid human tumours. Eur J Cancer 2002;38: 1564-79
41. Vermeulen PB, Gasparini G, Fox SB, et al. Quantification of angio-genesis in solid human tumours: An international consensus on the methodology and criteria of evaluation. Eur J Cancer 1996;32A:2474-84
42. Lunn KE, Paulsen KD, Roberts DW, et al. Displacement estimation with co-registered ultrasound for image guided neurosurgery: A quantitative in vivo porcine study. IEEE Trans Med Imaging 2003;22:1358-68
43. Lunn KE, Paulsen KD, Lynch DR, et al. Assimilating intraoperative data with brain shift modeling using the adjoint equations. Med Image Anal 2005;9:281-93
44. Ennis SR, Novotny A, Xiang J, et al. Transport of 5-aminolevulinic acid between blood and brain. Brain Res 2003;959:226-34
45. Ishihara R, Katayama Y, Watanabe T, et al. Quantitative spectroscopic analysis of 5-aminolevulinic acid-induced protoporphyrin IX fluorescence intensity in diffusely infiltrating astrocytomas. Neurol Med Chir (Tokyo) 2007;47:53-7; [discussion 7]
46. Ramanujam N. Fluorescence spectroscopy of neoplastic and non-neoplastic tissues. Neoplasia 2000;2:89-117
47. Runge VM, Schaible TF, Goldstein HA, et al. Gd DTPA. Clinical efficacy. Radiographics 1988;8:147-59
48. Weinmann HJ, Brasch RC, Press W, et al. Characteristics of gadolinium-DTPA complex: A potential NMR contrast agent. AJR 1984;142:619-24