Blood oxygenation level dependent, blood volume, and blood flow responses to carbogen and hypoxic hypoxia in 9L rat gliomas as measured by MRI

Journal of Magnetic Resonance Imaging

Volumn 39, Issue 1, 2014, Pages 110-119

  Jerome, Neil P ^a   Hekmatyar, S Khan ^a   Kauppinen, Risto A ^a,b,c  

^a DARTMOUTH COLLEGE   (United States)

^b INSTITUTE OF CANCER RESEARCH   (United Kingdom)

^c UNIVERSITY OF GEORGIA   (United States)

Author keywords

9L glioma; blood flow; blood oxygenation level dependent signal; blood volume; hypercarbia; hypoxia; MRI; vessel size

Indexed keywords

CARBOGEN; GADODIAMIDE; ULTRASMALL SUPERPARAMAGNETIC IRON OXIDE;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTHROPOMETRIC PARAMETERS; ARTICLE; BLOOD OXYGENATION; BLOOD VESSEL REACTIVITY; BOLD SIGNAL; BRAIN BLOOD VOLUME; BRAIN CORTEX; BREATHING; CONTROLLED STUDY; ECHO PLANAR IMAGING; GLIOMA; HISTOPATHOLOGY; HYPERCAPNIA; HYPOXIA; NONHUMAN; NUCLEAR MAGNETIC RESONANCE IMAGING; NUCLEAR MAGNETIC RESONANCE SCANNER; PRIORITY JOURNAL; PROSPECTIVE STUDY; PULSE OXIMETER; RAT; SPIN LABELING; TUMOR BLOOD FLOW; VESSEL SIZE INDEX;

9L GLIOMA; BLOOD FLOW; BLOOD OXYGENATION LEVEL DEPENDENT SIGNAL; BLOOD VOLUME; HYPERCARBIA; HYPOXIA; MRI; VESSEL SIZE;

ANIMALS; ANOXIA; BLOOD VESSELS; CARBON DIOXIDE; CELL LINE, TUMOR; CONTRAST MEDIA; DIFFUSION; GLIOMA; HEMODYNAMICS; HYPERCAPNIA; MAGNETIC RESONANCE IMAGING; MALE; NEOPLASM TRANSPLANTATION; OXYGEN; PROSPECTIVE STUDIES; RATS; RATS, INBRED F344; SPIN LABELS;

EID: 84890467784     PISSN: 10531807     EISSN: 15222586     Source Type: Journal    
DOI: 10.1002/jmri.24097     Document Type: Article

References (43)

1. Jain RK, di Tomaso E, Duda DG, Loeffler JS, Sorensen AG, Batchelor TT,. Angiogenesis in brain tumours. Nat Rev Neurosci 2007; 8: 610-622.
2. Jouanneau E,. Angiogenesis and gliomas: current issues and development of surrogate markers. Neurosurgery 2008; 62: 31-52.
3. Wong ET, Brem S,. Antiangiogenesis treatment for glioblastoma multiforme: challenges and opportunities. J Natl Compr Canc Netw 2008; 6: 515-522.
4. Heldin CH, Rubin K, Pietras K, Ostman A,. High interstitial fluid pressure-an obstacle in cancer therapy. Nat Rev Cancer 2004; 4: 806-813.
5. Bergers G, Brekken R, McMahon G, et al. Matrix metalloproteinase-9 triggers the angiogenic switch during carcinogenesis. Nat Cell Biol 2000; 2: 737-744.
6. Shweiki D, Itin A, Soffer D, Keshet E,. Vascular endothelial growth factor induced by hypoxia may mediate hypoxia-initiated angiogenesis. Nature 1992; 359: 843-845.
7. Vredenburgh JJ, Desjardins A, Herndon JE Jr, et al. Bevacizumab plus irinotecan in recurrent glioblastoma multiforme. J Clin Oncol 2007; 25: 4722-4729.
8. Parker GJM, Padhani AR,. T1-w DCE-MRI: T1-weighted dynamic contrast-enhanced MRI. In:, Tofts PS, editor. Quantitative MRI of the brain. Chippenham: John Wiley and Son; 2004. p 341-364.
9. Kennan RP, Jager HR,. T2- and T2*-w DCE-MRI: blood perfusion and volume estimation using bolus tracking. In:, Tofts PB, editor. Quantitative MRI of the brain. Chippenham: John Wiley and Son; 2004. p 365-412.
10. Dennie J, Mandeville JB, Boxerman JL, Packard SD, Rosen BR, Weisskoff RM,. NMR imaging of changes in vascular morphology due to tumor angiogenesis. Magn Reson Med 1998; 40: 793-799.
11. Tropres I, Lamalle L, Peoc'h M, et al. In vivo assessment of tumoral angiogenesis. Magn Reson Med 2004; 51: 533-541.
12. Claes A, Gambarota G, Hamans B, et al. Magnetic resonance imaging-based detection of glial brain tumors in mice after antiangiogenic treatment. Int J Cancer 2008; 122: 1981-1986.
13. Howe FA, Robinson SP, McIntyre DJ, Stubbs M, Griffiths JR,. Issues in flow and oxygenation dependent contrast (FLOOD) imaging of tumours. NMR Biomed 2001; 14: 497-506.
14. Kauppinen RA, Peet AC,. Using magnetic resonance imaging and spectroscopy in cancer diagnostics and monitoring: preclinical and clinical approaches. Cancer Biol Ther 2011; 12: 665-679.
15. Cosgrove D, Lassau N,. Imaging of perfusion using ultrasound. Eur J Nucl Med Mol Imaging 2010; 37 (Suppl 1): S65-S85.
16. Herholz K, Coope D, Jackson A,. Metabolic and molecular imaging in neuro-oncology. Lancet Neurol 2007; 6: 711-724.
17. Rauscher A, Sedlacik J, Fitzek C, et al. High resolution susceptibility weighted MR-imaging of brain tumors during the application of a gaseous agent. Rofo 2005; 177: 1065-1069.
18. Remmele S, Dahnke H, Flacke S, et al. Quantification of the magnetic resonance signal response to dynamic CO2-enhanced imaging in the brain at 3 T: R2* BOLD vs. balanced SSFP. J Magn Reson Imaging 2010; 31: 1300-1310.
19. Barth RF, Kaur B,. Rat brain tumor models in experimental neuro-oncology: the C6, 9L, T9, RG2, F98, BT4C, RT-2 and CNS-1 gliomas. J Neurooncol 2009; 94: 299-312.
20. Sicard KM, Duong TQ,. Effects of hypoxia, hyperoxia, and hypercapnia on baseline and stimulus-evoked BOLD, CBF, and CMRO2 in spontaneously breathing animals. Neuroimage 2005; 25: 850-858.
21. Julien C, Payen JF, Tropres I, et al. Assessment of vascular reactivity in rat brain glioma by measuring regional blood volume during graded hypoxic hypoxia. Br J Cancer 2004; 91: 374-380.
22. Mori S, van Zijl PCM,. Diffusion weighting by the trace of the diffusion tensor within a single scan. Magn Reson Med 1995; 33: 41-52.
23. Williams DS, Detre JA, Leigh JS, Koretsky AP,. Magnetic resonance imaging of perfusion using spin inversion of arterial water. Proc Natl Acad Sci U S A 1992; 89: 212-216.
24. Benga G,. Water exchange through the erythrocyte membrane. Int Rev Cytol 1989; 114: 273-316.
25. Dunn JF, Roche MA, Springett R, et al. Monitoring angiogenesis in brain using steady-state quantification of DeltaR2 with MION infusion. Magn Reson Med 2004; 51: 55-61.
26. Thomas DL,. Arterial spin labeling in small animals: methods and applications to experimental cerebral ischemia. J Magn Reson Imaging 2005; 22: 741-744.
27. Herscovitch P, Raichle ME,. What is the correct value for the brain-blood partition coefficient for water. J Cereb Blood Flow Metab 1985; 5: 65-69.
28. Tropres I, Grimault S, Vaeth A, et al. Vessel size imaging. Magn Reson Med 2001; 45: 397-408.
29. Mandeville JB, Leite FP, Marota JJ,. Spin-echo MRI underestimates functional changes in microvascular cerebral blood plasma volume using exogenous contrast agent. Magn Reson Med 2007; 58: 769-776.
30. Dunn JF, O'Hara JA, Zaim-Wadghiri Y, et al. Changes in oxygenation of intracranial tumors with carbogen: a BOLD MRI and EPR oximetry study. J Magn Reson Imaging 2002; 16: 511-521.
31. Hekmatyar SK, Liimatainen T, Jerome N, Khan N, Swartz HM, Kauppinen RA,. 1H MRS detected mobile lipids in rodent gliomas: correlation with EPR determined tumour oxygenation. Proc Intl Soc Magn Reson Med 2009; 17: 1016.
32. Zoula S, Rijken PF, Peters JP, et al. Pimonidazole binding in C6 rat brain glioma: relation with lipid droplet detection. Br J Cancer 2003; 88: 1439-1444.
33. Matsumoto S, Hyodo F, Subramanian S, et al. Low-field paramagnetic resonance imaging of tumor oxygenation and glycolytic activity in mice. J Clin Invest 2008; 118: 1965-1973.
34. Poptani H, Puumalainen A-M, Grohn OHJ, 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: 101-109.
35. Gambarota G, Leenders W, Maass C, et al. Characterisation of tumour vasculature in mouse brain by USPIO contrast-enhanced MRI. Br J Cancer 2008; 98: 1784-1789.
36. Bernsen HJ, Rijken PF, Hagemeier NE, van der Kogel AJ,. A quantitative analysis of vascularization and perfusion of human glioma xenografts at different implantation sites. Microvasc Res 1999; 57: 244-257.
37. Yacoub E, Van De Moortele PF, Shmuel A, Ugurbil K,. Signal and noise characteristics of Hahn SE and GE BOLD fMRI at 7 T in humans. Neuroimage 2005; 24: 738-750.
38. Silva AC, Zhang W, Williams DS, Koretsky AP,. Estimation of water extraction fractions in rat brain using magnetic resonance measurement of perfusion with arterial spin labeling. Magn Reson Med 1997; 37: 58-68.
39. Moffat BA, Chenevert TL, Hall DE, Rehemtulla A, Ross BD,. Continuous arterial spin labeling using a train of adiabatic inversion pulses. J Magn Reson Imaging 2005; 21: 290-296.
40. Broux C, Tropres I, Montigon O, Julien C, Decorps M, Payen JF,. The effects of sustained hyperventilation on regional cerebral blood volume in thiopental-anesthetized rats. Anesth Analg 2002; 95: 1746-1751.
41. Packard SD, Mandeville JB, Ichikawa T, et al. Functional response of tumor vasculature to PaCO2: determination of total and microvascular blood volume by MRI. Neoplasia 2003; 5: 330-338.
42. Meng Y, Wang P, Kim SG,. Simultaneous measurement of cerebral blood flow and transit time with turbo dynamic arterial spin labeling (Turbo-DASL): application to functional studies. Magn Reson Med 2012; 68: 762-771.
43. Sommers MG, van Egmond J, Booij LH, Heerschap A,. Isoflurane anesthesia is a valuable alternative for alpha-chloralose anesthesia in the forepaw stimulation model in rats. NMR Biomed 2009; 22: 414-418.