Bevacizumab impairs oxidative energy metabolism and shows antitumoral effects in recurrent glioblastomas: A 31P/ 1H MRSI and quantitative magnetic resonance imaging study

Neuro-Oncology

Volumn 13, Issue 12, 2011, Pages 1349-1363

  Hattingen, Elke ^a   Jurcoane, Alina ^a   Bähr, Oliver ^b   Rieger, Johannes ^b   Magerkurth, Jörg ^a   Anti, Sandra ^c   Steinbach, Joachim P ^b   Pilatus, Ulrich ^a  

^a GOETHE UNIVERSITY   (Germany)

^b Dr Senckenberg Institute of Neurooncology   (Germany)

^c Brain Imaging Center   (Germany)

Author keywords

ADC; Bevacizumab; Glioblastoma; Phosphorus spectroscopy; T2'.

Indexed keywords

BEVACIZUMAB; GLYCEROPHOSPHOETHANOLAMINE; OXYGEN;

ADULT; AGED; ANTIANGIOGENIC ACTIVITY; ANTINEOPLASTIC ACTIVITY; ARTICLE; BRAIN TISSUE; CANCER SURVIVAL; CARDIOVASCULAR FUNCTION; CASE REPORT; CONTROLLED STUDY; DIFFUSION COEFFICIENT; DRUG EFFECT; EDEMA; ENERGY METABOLISM; FEMALE; GLIOBLASTOMA; HOMEOSTASIS; HUMAN; HYPOXIA; IN VIVO STUDY; MALE; METABOLITE; OVERALL SURVIVAL; OXIDATION; PHOSPHORUS NUCLEAR MAGNETIC RESONANCE; PROGRESSION FREE SURVIVAL; PROTON NUCLEAR MAGNETIC RESONANCE; QUANTITATIVE ANALYSIS; TUMOR RECURRENCE; WILCOXON SIGNED RANKS TEST;

ADULT; AGED; ANGIOGENESIS INHIBITORS; ANTIBODIES, MONOCLONAL, HUMANIZED; BRAIN NEOPLASMS; CELL RESPIRATION; ENERGY METABOLISM; FEMALE; FOLLOW-UP STUDIES; GLIOBLASTOMA; HUMANS; MAGNETIC RESONANCE IMAGING; MALE; MIDDLE AGED; NEOPLASM RECURRENCE, LOCAL; PROSPECTIVE STUDIES; SURVIVAL RATE; TREATMENT OUTCOME;

EID: 84856302564     PISSN: 15228517     EISSN: 15235866     Source Type: Journal    
DOI: 10.1093/neuonc/nor132     Document Type: Article

References (91)

1. Wong ET, Hess KR, Gleason MJ, et al. Outcomes and prognostic factors in recurrent glioma patients enrolled onto phase II clinical trials. J Clin Oncol. 1999;17(8):2572-2578. (Pubitemid 29368260)
2. Wick W, Puduvalli VK, Chamberlain MC, et al. Phase III study of enzastaurin compared with lomustine in the treatment of recurrent intracranial glioblastoma. J Clin Oncol. 2010;28(7):1168-1174.
3. Vredenburgh JJ, Desjardins A, Herndon JE, 2nd, et al. Bevacizumab plus irinotecan in recurrent glioblastoma multiforme. J Clin Oncol. 2007;25(30):4722-4729. (Pubitemid 350086473)
4. Friedman HS, Prados MD, Wen PY, et al. Bevacizumab alone and in combination with irinotecan in recurrent glioblastoma. J Clin Oncol. 2009;27(28):4733-4740.
5. de Groot JF, Fuller G, Kumar AJ, et al. Tumor invasion after treatment of glioblastoma with bevacizumab: Radiographic and pathologic correlation in humans and mice. Neuro Oncol. 2010;12(3):233-242.
6. Rieger J, Bähr O, Muller K, Franz K, Steinbach J, Hattingen E. Bevacizumab-induced diffusion-restricted lesions in malignant glioma patients. Neuro Oncol. 2010;99(1):49-56.
7. Rampling R, Cruickshank G, Lewis AD, Fitzsimmons SA, Workman P. Direct measurement of pO2 distribution and bioreductive enzymes in human malignant brain tumors. Int J Radiat Oncol Biol Phys. 1994;29(3):427-431. (Pubitemid 24187904)
8. Carmeliet P, Dor Y, Herbert JM, et al. Role of HIF-1alpha in hypoxiamediated apoptosis, cell proliferation and tumour angiogenesis. Nature. 1998;394(6692):485-490. (Pubitemid 28373960)
9. Ryan HE, Poloni M, McNulty W, et al. Hypoxia-inducible factor-1alpha is a positive factor in solid tumor growth. Cancer Res. 2000;60(15):4010-4015. (Pubitemid 30636574)
10. Ronellenfitsch MW, Brucker DP, Burger MC, et al. Antagonism of the mammalian target of rapamycin selectively mediates metabolic effects of epidermal growth factor receptor inhibition and protects human malignant glioma cells from hypoxia-induced cell death. Brain. 2009;132(Pt 6):1509-1522.
11. Tennant DA, Durán RV, Gottlieb E. Targeting metabolic transformation for cancer therapy. Nat Rev Cancer. 2010;10(4):267-277.
12. Semenza GL, Wang GL. A nuclear factor induced by hypoxia via de novo protein synthesis binds to the human erythropoietin gene enhancer at a site required for transcriptional activation. Mol Cell Biol. 1992;12:5447-5454.
13. Collingridge DR, Piepmeier JM, Rockwell S, Knisely JP. Polarographic measurements of oxygen tension in human glioma and surrounding peritumoural braintissue. Radiother Oncol. 1999;53(2):127-131.
14. Ivanov S, Liao SY, Ivanova A, et al. Expression of hypoxia-inducible cellsurface transmembrane carbonic anhydrases in human cancer. Am J Pathol. 2001;158(3):905-919. (Pubitemid 32221783)
15. Chiche J, Ilc K, Laferrière J, et al. Hypoxia-inducible carbonic anhydrase IX and XII promote tumor cell growth by counteracting acidosis through the regulation of the intracellular pH. Cancer Res. 2009;69(1):358-368.
16. Seidel S, Garvalov BK, Wirta V, et al. A hypoxic niche regulates glioblastoma stem cells through hypoxia inducible factor 2 alpha. Brain. 2010;133(Pt 4):983-995.
17. Brat DJ, Van Meir EG. Vaso-occlusive and prothrombotic mechanisms associated with tumor hypoxia, necrosis, and accelerated growth in glioblastoma. Lab Invest. 2004;84(4):397-405. (Pubitemid 41656467)
18. Jain RK. Normalization of tumor vasculature: An emerging concept in antiangiogenic therapy. Science. 2005;307(5706):58-62. (Pubitemid 40093472)
19. Batchelor TT, Sorensen AG, di Tomaso E, et al. AZD2171, a pan-VEGF receptor tyrosine kinase inhibitor, normalizes tumor vasculature and alleviates edema in glioblastoma patients. Cancer Cell. 2007;11(1):83-95. (Pubitemid 46075199)
20. Winkler F, Kozin SV, Tong RT, et al. Kinetics of vascular normalization by VEGFR2 blockade governs brain tumor response to radiation: Role of oxygenation, angiopoietin-1, and matrix metalloproteinases. Cancer Cell. 2004;6(6):553-563. (Pubitemid 40017699)
21. Dings RP, Loren M, Heun H, et al. Scheduling of radiation with angiogenesis inhibitors anginex and Avastin improves therapeutic outcome via vessel normalization. Clin Cancer Res. 2007;13(11):3395-3402. (Pubitemid 46944928)
22. Erber R, Thurnher A, Katsen AD, et al. Combined inhibition of VEGF and PDGF signaling enforces tumor vessel regression by interfering with pericyte-mediated endothelial cell survival mechanisms. FASEB J. 2004;18(2):338-340.
23. Casanovas O, Hicklin DJ, Bergers G, Hanahan D. Drug resistance by evasion of antiangiogenic targeting of VEGF signaling in late-stage pancreatic islet tumors. Cancer Cell. 2005;8(4):299-309. (Pubitemid 41443415)
24. Wen PY, Macdonald DR, Reardon DA, et al. Updated response assessment criteria for high-grade gliomas: Response assessment in neuro-oncology working group. J Clin Oncol. 2010;28(11):1963-1972.
25. Saitta L, Heese O, Förster AF, et al. Signal intensity in T2' magnetic resonance imaging is related to brain glioma grade. Eur Radiol. 2011;21(5):1068-1076.
26. Papandreou I, Cairns RA, Fontana L, Lim AL, Denko NC. HIF-1 mediates adaptation to hypoxia by actively downregulating mitochondrial oxygen consumption. Cell Metab. 2006;3(3):187-197.
27. Moolenaar WH, Tsien RY, van der Saag PT, de Laat SW. Na+/H+ exchange and cytoplasmic pH in the action of growth factors in human fibroblasts. Nature. 1983;304(5927):645-648. (Pubitemid 13035506)
28. Kallinowski F, Vaupel P. pH distributions in spontaneous and isotransplanted rat tumours. Br J Cancer. 1988;58(3):314-321.
29. Gerweck LE, Seetharaman K. Cellular pH gradient in tumor versus normal tissue: Potential exploitation for the treatment of cancer. Cancer Res. 1996;56:1194-1198. (Pubitemid 26080953)
30. McLean LA, Roscoe J, Jorgensen NK, Gorin FA, Cala PM. Malignant gliomas display altered pH regulation by NHE1 compared with nontransformed astrocytes. Am J Physiol Cell Physiol. 2000;278(4):C676-C688. (Pubitemid 30211300)
31. Gillies RJ, Liu Z, Bhujwalla Z. 31P-MRS measurements of extracellular pH of tumors using 3-aminopropylphosphonate. Am J Physiol. 1994;267(1, pt 1):C195-C203.
32. Vaupel P, Kallinowski F, Okunieff P. Blood flow, oxygen and nutrient supply, and metabolic microenvironment of human tumors: A review. Cancer Res. 1989;49:6449-6465. (Pubitemid 20008770)
33. Bhakoo KK, Williams SR, Florian CL, Land H, Noble MD. Immortalization and transformation are associated with specific alterations in choline metabolism. Cancer Res. 1996;56(20):4630-4635. (Pubitemid 26338062)
34. Aiken NR, Szwergold ES, Kappler F, et al. Metabolism of phosphonium choline by rat-2 fibroblasts: Effects of mitogenic stimulation studied using 31P NMR spectroscopy. Anticancer Res. 1996;16(3B):1357-1363. (Pubitemid 26257803)
35. Podo F. Tumour phospholipid metabolism. NMR Biomed. 1999;12(7):413-439. Review. (Pubitemid 30016999)
36. Hattingen E, Magerkurth J, Pilatus U, et al. Phosphorus and proton magnetic resonance spectroscopy demonstrates mitochondrial dysfunction in early and advanced Parkinson's disease. Brain. 2009;132(Pt 12):3285-3297.
37. Macdonald D, Cascino T, Schold SJ, Cairncross J. Response criteria for phase II studies of supratentorial malignant glioma. J Clin Oncol. 1990;8(7):1277-1280. (Pubitemid 20195640)
38. Frahm J, Haase A, Matthaei D. Rapid 3-dimensional MR imaging using the flash technique. J Comput Assist Tomogr. 1986;10(2):363-368. (Pubitemid 16113434)
39. Ericsson A, Weis J, Hemmingsson A, Wikstrom M, Sperber GO. Measurements of magnetic-field variations in the human brain using a 3D-Ft multiple gradient-echo technique. Magn Reson Med. 1995;33(2):171-177.
40. Provencher SW. Estimation of metabolite concentrations from localized in vivo proton NMR spectra. Magn Reson Med. 1993;30(6): 672-679. (Pubitemid 23360802)
41. Vanhamme L, van den Boogaart A, Van Huffel S. Improved method for accurate and efficient quantification of MRS data with use of prior knowledge. J Magn Reson. 1997;129(1):35-43. (Pubitemid 127454051)
42. Hattingen E, Pilatus U, Franz K, Zanella FE, Lanfermann H. Evaluation of optimal echo time for 1H-spectroscopic imaging of brain tumors at 3 Tesla. J Magn Reson Imaging. 2007;26(2):427-431. (Pubitemid 47257745)
43. Hattingen E, Magerkurth J, Pilatus U, Hübers A, Wahl M, Ziemann U. Combined (1)H and (31)P spectroscopy provides new insights into the pathobiochemistry of brain damage in multiple sclerosis. NMR Biomed. 2011;24(5):536-546.
44. Kanowski M, Kaufmann J, Braun J, Bernarding J, Tempelmann C. Quantitation of simulated short echo time 1H human brain spectra by LCModel and AMARES. Magn Reson Med. 2004;51(5):904-912. (Pubitemid 38580602)
45. Petroff OA, Prichard JW, Behar KL, Rothman DL, Alger JR, Shulman RG. Cerebral metabolism in hyper- and hypocarbia: 31P and 1H nuclear magnetic resonance studies. Neurology. 1985;35:1681-1688. (Pubitemid 16222748)
46. Kreis R. Issues of spectral quality in clinical 1H-magnetic resonance spectroscopy and a gallery of artifacts. NMR Biomed. 2004;17(6):361-381. (Pubitemid 39335175)
47. Baudrexel S, Nurnberger L, Rub U, et al. Quantitative mapping of T1 and T2* discloses nigral and brainstem pathology in early Parkinson's disease. Neuroimage. 2010;51(2):512-520.
48. Magerkurth J, Volz S, Wagner M, et al. Quantitative T2*-mapping based on multi-slice multiple gradient echo FLASH imaging: Retrospective correction for subject motion effects. Magn Reson Med. 2011. doi: 10.1002/mrm.22878.
49. Smith SM. Fast robust automated brain extraction. Hum Brain Mapp. 2002;17(3):143-155. (Pubitemid 35253488)
50. Smith SM, Jenkinson M, Woolrich MW, et al. Advances in functional and structural MR image analysis and implementation as FSL. Neuroimage. 2004;23(Suppl 1):S208-S219. (Pubitemid 39421720)
51. Jenkinson M, Bannister P, Brady M, Smith S. Improved optimization for the robust and accurate linear registration and motion correction of brain images. Neuroimage. 2002;17(2):825-841. (Pubitemid 35317016)
52. Rorden C, Karnath HO, Bonilha L. Improving lesion-symptom mapping. J Cogn Neurosci. 2007;19(7):1081-1088. (Pubitemid 47026498)
53. Rees JH, Smirniotopoulos JG, Jones RV, Wong K. Glioblastoma multiforme: Radiologic-pathologic correlation. Radiographics. 1996;16(6): 1413-1438.
54. DeAngelis LM, Posner JB. Neurologic Complications of Cancer. 2nd ed. New York: Oxford University Press; 2009.
55. Steen RG, Tamargo RJ, McGovern KA, et al. In vivo 31P nuclear magnetic resonance spectroscopy of subcutaneous 9L gliosarcoma: Effects of tumor growth and treatment with 1,3-bis(2-chloroethyl)-1- nitrosourea on tumor bioenergetics and histology. Cancer Res. 1988;48(3):676-681. (Pubitemid 18056542)
56. Ross BD, Higgins RJ, Boggan JE, Knittel B, Garwood M. 31P NMR spectroscopy of the in vivo metabolism of an intracerebral glioma in the rat. Magn Reson Med. 1988;6(4):403-417.
57. Winter PM, Poptani H, Bansal N. Effects of chemotherapy by 1,3-bis(2-chloroethyl)-1-nitrosourea on single-quantum- and triple-quantum- filtered 23Na and 31P nuclear magnetic resonance of the subcutaneously implanted 9L glioma. Cancer Res. 2001;61(5):2002-2007. (Pubitemid 32692020)
58. Oh J, Cha S, Aiken AH, et al. Quantitative apparent diffusion coefficients and T2 relaxation times in characterizing contrast enhancing brain tumors and regions of peritumoral edema. J Magn Reson Imaging. 2005;21(6):701-708. (Pubitemid 40770861)
59. Schad LR, Brix G, Zuna I, Härle W, Lorenz WJ, Semmler W. Multiexponential proton spin-spin relaxation in MR imaging of human brain tumors. J Comput Assist Tomogr. 1989;13(4):577-587. (Pubitemid 19183899)
60. Damadian R. Tumor detection by nuclear magnetic resonance. Science. 1971;171(976):1151-1153.
61. Eis M, Els T, Hoehn-Berlage M. High resolution quantitative relaxation and diffusion MRI of three different experimental brain tumors in rat. Magn Reson Med. 1995;34(6):835-844.
62. van den Bent MJ, Vogelbaum MA,Wen PY, Macdonald DR, Chang SM. End point assessment in gliomas: Novel treatments limit usefulness of classical Macdonald's criteria. J Clin Oncol. 2009;27(18):2905-2908.
63. Ananthnarayan S, Bahng J, Roring J, et al. Time course of imaging changes of GBM during extended bevacizumab treatment. J Neurooncol. 2008;88(3):339-347.
64. Tozer GM, Griffiths JR. The contribution made by cell death and oxygenation to 31P MRS observations of tumour energy metabolism. NMR Biomed. 1992;5(5):279-289.
65. Pistollato F, Abbadi S, Rampazzo E, Persano L, et al. Intratumoral hypoxic gradient drives stem cells distribution and MGMT expression in glioblastoma. Stem Cells. 2010;28:851-862.
66. Wick W, Wick A, Weiler M, Weller M. Patterns of progression in malignant glioma following anti-VEGF therapy: Perceptions and evidence. Curr Neurol Neurosci Rep. 2011;11:305-312.
67. Chamberlain MC. Radiographic patterns of relapse in glioblastoma. J Neurooncol. 2011;101(2):319-323.
68. Poptani H, Puumalainen AM, Gröhn OH, et al. Monitoring thymidine kinase and ganciclovir-induced changes in rat malignant glioma in vivo by nuclear magnetic resonance imaging. Cancer Gene Ther. 1998;5(2):101-109. (Pubitemid 128639996)
69. Wu J, Gilbert MR, De Groot JF, Yung WA, Puduvalli VK. J Clin Oncol. 2010;28:15s. (suppl; abstr 2024).
70. Marincek B, Friedburg H. Calculated T1 and T2 MR images and 31P MR spectra in rabbit thigh V2 carcinoma to monitor the effect of steroid administration. Invest Radiol. 1985;20(7):701-707. (Pubitemid 16242110)
71. O'Shea JM, Williams SR, van Bruggen N, Gardner-Medwin AR. Apparent diffusion coefficient and MR relaxation during osmotic manipulation in isolated turtle cerebellum. Magn Reson Med. 2000;44(3):427-432.
72. Kamman RL, Go KG, Brouwer W, Berendsen HJ. Nuclear magnetic resonance relaxation in experimental brain edema: Effects of water concentration, protein concentration, and temperature. Magn Reson Med. 1988;6(3):265-274. (Pubitemid 18093951)
73. Tofts, P. ed. Quantitative MRI of the brain: Measuring changes caused by disease. Chichester: John Wiley; 2003.
74. Ringelstein A, Turowski B, Gizewski ER, et al. [Evaluation of ADC mapping as an early predictor for tumor response to chemotherapy in recurrent glioma treated with bevacizumab/irinotecan: Proof of principle]. Rofo. 2010;182(10):868-872.
75. Nowosielski M, Recheis W, Goebel G, et al. ADC histograms predict response to anti-angiogenic therapy in patients with recurrent high-grade glioma. Neuroradiology. 2011;53(4):291-302.
76. Oberhaensli RD, Hilton-Jones D, Bore PJ, Hands LJ, Rampling RP, Radda GK. Biochemical investigation of human tumours in vivo with phosphorus-31 magnetic resonance spectroscopy. Lancet. 1986;2(8497):8-11. (Pubitemid 16095612)
77. Hubesch B, Sappey-Marinier D, Roth K, Meyerhoff DJ, Matson GB, Weiner MW. P-31 MR spectroscopy of normal human brain and brain tumors. Radiology. 1990;174(2):401-409. (Pubitemid 20038598)
78. Rutter A, Hugenholtz H, Saunders JK, Smith IC. One-dimensional phosphorus-31 chemical shift imaging of human brain tumors. Invest Radiol. 1995;30(6):359-366.
79. Maintz D, Heindel W, Kugel H, Jaeger R, Lackner KJ. Phosphorus-31 MR spectroscopy of normal adult human brain and brain tumours. NMR Biomed. 2002;15(1):18-27. (Pubitemid 34177164)
80. Martínez-Zaguilán R, Seftor EA, Seftor RE, Chu YW, Gillies RJ, Hendrix MJ. Acidic pH enhances the invasive behavior of human melanoma cells. Clin Exp Metastasis. 1996;14(2):176-186. (Pubitemid 26074280)
81. Fukumura D, Xu L, Chen Y, Gohongi T, Seed B, Jain RK. Hypoxia and acidosis independently up-regulate vascular endothelial growth factor transcription in brain tumors in vivo. Cancer Res. 2001;61(16):6020-6024. (Pubitemid 32762531)
82. Valonen PK, Griffin JL, Lehtimäki KK, et al. High-resolution magic-angle-spinning 1H NMR spectroscopy reveals different responses in choline-containing metabolites upon gene therapy-induced programmed cell death in rat brain glioma. NMR Biomed. 2005;18(4):252-259. (Pubitemid 40936445)
83. Mancuso A, Zhu A, Beardsley NJ, Glickson JD, Wehrli S, Pickup S. Artificial tumor model suitable for monitoring 31P and 13C NMR spectroscopic changes during chemotherapy-induced apoptosis in human glioma cells. Magn Reson Med. 2005;54(1):67-78. (Pubitemid 40898398)
84. Gillies RJ, Barry JA, Ross BD. In vitro and in vivo 13C and 31P NMR analyses of phosphocholine metabolism in rat glioma cells. Magn Reson Med. 1994;32(3):310-318. (Pubitemid 24274909)
85. Maris JM, Evans AE, McLaughlin AC, et al. 31P nuclear magnetic resonance spectroscopic investigation of human neuroblastoma in situ. N Engl J Med. 1985;312(23):1500-1505. (Pubitemid 15059237)
86. Negendank WG, Padavic-Shaller KA, Li CW, et al. Metabolic characterization of human non-Hodgkin's lymphomas in vivo with the use of proton-decoupled phosphorus magnetic resonance spectroscopy. Cancer Res. 1995;55(15):3286-3294.
87. Mintz A, Wang L, Ponde DE. Comparison of radiolabeled choline and ethanolamine as probe for cancer detection. Cancer Biol Ther. 2008;7(5):742-747.
88. Luyten PR, Bruntink G, Sloff FM, et al. Broadband proton decoupling in human 31P NMR spectroscopy. NMR Biomed. 1989;1(4):177-183.
89. Murphy-Boesch J, Stoyanova R, Srinivasan R, et al. Proton-decoupled 31P chemical shift imaging of the human brain in normal volunteers. NMR Biomed. 1993;6(3):173-180.
90. Potwarka JJ, Drost DJ, Williamson PC. Quantifying 1H decoupled in vivo 31P brain spectra. NMR Biomed. 1999;12(1):8-14. (Pubitemid 29135404)
91. Jensen JE, Drost DJ, Menon RS, Williamson PC. In vivo brain (31)P-MRS: Measuring the phospholipid resonances at 4 Tesla from small voxels. NMR Biomed. 2002;15(5):338-347. (Pubitemid 34960101)