Quantitative measurement of cerebral physiology using respiratory-calibrated MRI

NeuroImage

Volumn 60, Issue 1, 2012, Pages 582-591

  Bulte, D P ^a   Kelly, M ^a   Germuska, M ^a   Xie, J ^a   Chappell, M A ^a,b   Okell, T W ^a   Bright, M G ^a,c,d   Jezzard, P ^a  

^a UNIVERSITY OF OXFORD   (United Kingdom)

^b UNIVERSITY OF OXFORD   (United Kingdom)

^c NATIONAL INSTITUTE OF NEUROLOGICAL DISORDERS AND STROKE   (United States)

^d CARDIFF UNIVERSITY   (United Kingdom)

Author keywords

CMRO 2; FMRI; Hypercapnia; Hyperoxia

Indexed keywords

ADULT; ARTICLE; BLOOD VESSEL REACTIVITY; BRAIN BLOOD FLOW; BRAIN BLOOD VOLUME; BRAIN FUNCTION; CALIBRATION; CEREBRAL METABOLIC RATE OF OXYGEN; CLINICAL PROTOCOL; CONTROLLED STUDY; FEMALE; FUNCTIONAL MAGNETIC RESONANCE IMAGING; FUNCTIONAL NEUROIMAGING; HUMAN; HUMAN EXPERIMENT; HYPERCAPNIA; HYPEROXIA; IMAGE ANALYSIS; INTERMETHOD COMPARISON; MALE; NORMAL HUMAN; OXYGEN EXTRACTION FRACTION; POSITRON EMISSION TOMOGRAPHY; PRIORITY JOURNAL; QUANTITATIVE ANALYSIS;

ADULT; BRAIN; CALIBRATION; CEREBROVASCULAR CIRCULATION; FEMALE; HUMANS; MAGNETIC RESONANCE IMAGING; MALE; OXYGEN; REGIONAL BLOOD FLOW; RESPIRATION;

EID: 84856079508     PISSN: 10538119     EISSN: 10959572     Source Type: Journal    
DOI: 10.1016/j.neuroimage.2011.12.017     Document Type: Article

References (67)

1. Ances B.M., Leontiev O., Perthen J.E., Liang C., Lansing A.E., Buxton R.B. Regional differences in the coupling of cerebral blood flow and oxygen metabolism changes in response to activation: Implications for BOLD-fMRI. Neuroimage 2008, 39:1510-1521.
2. Ances B.M., Liang C.L., Leontiev O., Perthen J.E., Fleisher A.S., Lansing A.E., Buxton R.B. Effects of aging on cerebral blood flow, oxygen metabolism, and blood oxygenation level dependent responses to visual stimulation. Hum. Brain Mapp. 2009, 30:1120-1132.
3. Aslan S., Xu F., Wang P.L., Uh J., Yezhuvath U.S., Van Osch M., Lu H. Estimation of labeling efficiency in pseudocontinuous arterial spin labeling. Magn. Reson. Med. 2010, 63:765-771.
4. Bolar D.S., Rosen B.R., Sorensen A.G., Adalsteinsson E. QUantitative Imaging of eXtraction of oxygen and TIssue Consumption (QUIXOTIC) using venular-targeted velocity-selective spin labeling. Magn. Reson. Med. 2011, 66:1550-1562.
5. Bulte D.P., Chiarelli P.A., Wise R., Jezzard P. Measurement of cerebral blood volume in humans using hyperoxic MRI contrast. J. Magn. Reson. Imaging 2007, 26:894-899.
6. Bulte D.P., Chiarelli P.A., Wise R.G., Jezzard P. Cerebral perfusion response to hyperoxia. J. Cereb. Blood Flow Metab. 2007, 27:69-75.
7. Bulte D.P., Drescher K., Jezzard P. Comparison of hypercapnia-based calibration techniques for measurement of cerebral oxygen metabolism with MRI. Magn. Reson. Med. 2009, 61:391-398.
8. Buxton R.B., Frank L.R., Wong E.C., Siewert B., Warach S., Edelman R.R. A general kinetic model for quantitative perfusion imaging with arterial spin labeling. Magn. Reson. Med. 1998, 40:383-396.
9. Buxton R.B., Uludag K., Dubowitz D.J., Liu T.T. Modeling the hemodynamic response to brain activation. Neuroimage 2004, 23:S220-S233.
10. Chappell M.A., Groves A.R., Whitcher B., Woolrich M.W. Variational Bayesian inference for a nonlinear forward model. IEEE Trans. Signal Process. 2009, 57:223-236.
11. Chen Y., Parrish T.B. Caffeine dose effect on activation-induced BOLD and CBF responses. Neuroimage 2009, 46:577-583.
12. Chen J.J., Pike G.B. MRI measurement of the BOLD-specific flow-volume relationship during hypercapnia and hypocapnia in humans. Neuroimage 2010, 53:383-391.
13. Chiarelli P.A., Bulte D.P., Piechnik S., Jezzard P. Sources of systematic bias in hypercapnia-calibrated functional MRI estimation of oxygen metabolism. Neuroimage 2007, 34:35-43.
14. Chiarelli P.A., Bulte D.P., Wise R., Gallichan D., Jezzard P. A calibration method for quantitative BOLD fMRI based on hyperoxia. Neuroimage 2007, 37:808-820.
15. Dai W., Garcia D., De Bazelaire C., Alsop D.C. Continuous flow-driven inversion for arterial spin labeling using pulsed radio frequency and gradient fields. Magn. Reson. Med. 2008, 60:1488-1497.
16. Davis T.L., Kwong K.K., Weisskoff R.M., Rosen B.R. Calibrated functional MRI: mapping the dynamics of oxidative metabolism. Proc. Natl. Acad. Sci. U. S. A. 1998, 95:1834-1839.
17. Gauthier C.J., Madjar C., Tancredi F.B., Stefanovic B., Hoge R.D. Elimination of visually evoked BOLD responses during carbogen inhalation: implications for calibrated MRI. Neuroimage 2011, 54:1001-1011.
18. Griffeth V.E.M., Buxton R.B. A theoretical framework for estimating cerebral oxygen metabolism changes using the calibrated-BOLD method: modeling the effects of blood volume distribution, hematocrit, oxygen extraction fraction, and tissue signal properties on the BOLD signal. Neuroimage 2011, 58:198-212.
19. Grubb R.L., Raichle M.E., Eichling J.O., Ter Pogossian M.M. The effects of changes in PaCO2 on cerebral blood volume, blood flow, and vascular mean transit time. Stroke 1974, 5:630-639.
20. He X., Yablonskiy D.A. Quantitative BOLD: mapping of human cerebral deoxygenated blood volume and oxygen extraction fraction: default state. Magn. Reson. Med. 2007, 57:115-126.
21. Herscovitch P., Raichle M.E. What is the correct value for the brain-blood partition coefficient for water?. J. Cereb. Blood Flow Metab. 1985, 5:65-69.
22. Hoge R.D., Atkinson J., Gill B., Crelier G.R., Marrett S., Pike G.B. Investigation of BOLD signal dependence on cerebral blood flow and oxygen consumption: the deoxyhemoglobin dilution model. Magn. Reson. Med. 1999, 42:849-863.
23. Huppert T.J., Allen M.S., Diamond S.G., Boas D.A. Estimating cerebral oxygen metabolism from fMRI with a dynamic multicompartment windkessel model. Hum. Brain Mapp. 2009, 30:1548-1567.
24. Ito H., Ibaraki M., Kanno I., Fukuda H., Miura S. Changes in cerebral blood flow and cerebral oxygen metabolism during neural activation measured by positron emission tomography: comparison with blood oxygenation level-dependent contrast measured by functional magnetic resonance imaging. J. Cereb. Blood Flow Metab. 2005, 25:371-377.
25. 15O-labelled carbon dioxide or water, carbon monoxide and oxygen: a multicentre study in Japan. Eur. J. Nucl. Med. Mol. Imaging 2004, 31:635-643.
26. Jain V., Langham M.C., Wehrli F.W. MRI estimation of global brain oxygen consumption rate. J. Cereb. Blood Flow Metab. 2010, 30:1598-1607.
27. Jenkinson M., Smith S. A global optimisation method for robust affine registration of brain images. Med. Image Anal. 2001, 5:143-156.
28. Kastrup A., Krüger G., Glover G.H., Moseley M.E. Assessment of cerebral oxidative metabolism with breath holding and fMRI. Magn. Reson. Med. 1999, 42:608-611.
29. 2 and breath holding. Magn. Reson. Imaging 2001, 19:13-20.
30. Kingsnorth A., Bowley D. Fundamentals of Surgical Practice 2011, Cambridge University Press.
31. Knutsson L., van Westen D., Petersen E.T., Bloch K.M., Holtås S., Ståhlberg F., Wirestam R. Absolute quantification of cerebral blood flow: correlation between dynamic susceptibility contrast MRI and model-free arterial spin labeling. Magn. Reson. Imaging 2010, 28:1-7.
32. Leontiev O., Buxton R.B. Reproducibility of BOLD, perfusion, and CMRO2 measurements with calibrated-BOLD fMRI. Neuroimage 2007, 35:175-184.
33. Lin A.L., Fox P.T., Yang Y., Lu H., Tan L.H., Gao J.H. Evaluation of MRI models in the measurement of CMRO2 and its relationship with CBF. Magn. Reson. Med. 2008, 60:380-389.
34. Lu H., Ge Y. Quantitative evaluation of oxygenation in venous vessels using T2-relaxation-under-spin-tagging MRI. Magn. Reson. Med. 2008, 60:357-363.
35. Lu H., Golay X., Pekar J.J., Van Zijl P.C.M. Sustained poststimulus elevation in cerebral oxygen utilization after vascular recovery. J. Cereb. Blood Flow Metab. 2004, 24:764-770.
36. Lu H., Van Zijl P.C.M. Experimental measurement of extravascular parenchymal BOLD effects and tissue oxygen extraction fractions using multi-echo VASO fMRI at 1.5 and 3.0 T. Magn. Reson. Med. 2005, 53:808-816.
37. MacIntosh B.J., Filippini N., Chappell M.A., Woolrich M.W., Mackay C.E., Jezzard P. Assessment of arterial arrival times derived from multiple inversion time pulsed arterial spin labeling MRI. Magn. Reson. Med. 2010, 63:641-647.
38. Mandell D.M., Han J.S., Poublanc J., Crawley A.P., Stainsby J.A., Fisher J.A., Mikulis D.J. Mapping cerebrovascular reactivity using blood oxygen level-dependent MRI in patients with arterial steno-occlusive disease: comparison with arterial spin labeling MRI. Stroke 2008, 39:2021-2028.
39. Mark C.I., Fisher J.A., Pike G.B. Improved fMRI calibration: precisely controlled hyperoxic versus hypercapnic stimuli. Neuroimage 2011, 54:1102-1111.
40. Mark C.I., Slessarev M., Ito S., Han J., Fisher J.A., Pike G.B. Precise control of end-tidal carbon dioxide and oxygen improves BOLD and ASL cerebrovascular reactivity measures. Magn. Reson. Med. 2010, 64:749-756.
41. Mazziotta J., Toga A., Evans A., Fox P., Lancaster J., Zilles K., Woods R., Paus T., Simpson G., Pike B., Holmes C., Collins L., Thompson P., MacDonald D., Iacoboni M., Schormann T., Amunts K., Palomero-Gallagher N., Geyer S., Parsons L., Narr K., Kabani N., Le Goualher G., Boomsma D., Cannon T., Kawashima R., Mazoyer B. A probabilistic atlas and reference system for the human brain: International Consortium for Brain Mapping (ICBM). Philos. Trans. R. Soc. Lond. B Biol. Sci. 2001, 356:1293-1322.
42. Mellon E.A., Beesam R.S., Elliott M.A., Reddy R. Mapping of cerebral oxidative metabolism with MRI. Proc. Natl. Acad. Sci. U. S. A. 2010, 107:11787-11792.
43. Mugler J.P., Brookeman J.R. Three-dimensional magnetization-prepared rapid gradient-echo imaging (3D MP RAGE). Magn. Reson. Med. 1990, 15:152-157.
44. * MRI. J. Cereb. Blood Flow Metab. 2006, 26:760-770.
45. Obata T., Liu T.T., Miller K.L., Luh W.M., Wong E.C., Frank L.R., Buxton R.B. Discrepancies between BOLD and flow dynamics in primary and supplementary motor areas: application of the balloon model to the interpretation of BOLD transients. Neuroimage 2004, 21:144-153.
46. Ogawa S., Lee T.M., Kay A.R., Tank D.W. Brain magnetic resonance imaging with contrast dependent on blood oxygenation. Proc. Natl. Acad. Sci. U. S. A. 1990, 87:9868-9872.
47. Ogawa S., Menon R.S., Tank D.W., Kim S.-G., Merkle H., Ellermann J.M., Ugurbil K. Functional brain mapping by blood oxygenation level-dependent contrast magnetic resonance imaging. A comparison of signal characteristics with a biophysical model. Biophys. J. 1993, 64:803-812.
48. Perthen J.E., Lansing A.E., Liau J., Liu T.T., Buxton R.B. Caffeine-induced uncoupling of cerebral blood flow and oxygen metabolism: A calibrated BOLD fMRI study. Neuroimage 2008, 40:237-247.
49. Pilkinton D.T., Gaddam S.R., Reddy R. Characterization of paramagnetic effects of molecular oxygen on blood oxygenation level-dependent-modulated hyperoxic contrast studies of the human brain. Magn. Reson. Med. 2011, 66:794-801.
50. Poulin M.J., Liang P.J., Robbins P.A. Dynamics of the cerebral blood flow response to step changes in end-tidal PCO2 and PO2 in humans. J. Appl. Physiol. 1996, 81:1084-1095.
51. Qin Q., Grgac K., Van Zijl P.C.M. Determination of whole-brain oxygen extraction fractions by fast measurement of blood T2 in the jugular vein. Magn. Reson. Med. 2011, 65:471-479.
52. 2 dissociation computations. J. Appl. Physiol. 1979, 46:599-602.
53. 2 concentrations. J. Physiol. 2007, 581:1207-1219.
54. Smielewski P., Coles J.P., Fryer T.D., Minhas P.S., Menon D.K., Pickard J.D. Integrated image analysis solutions for PET datasets in damaged brain. J. Clin. Monit. Comput. 2002, 17:427-440.
55. Smith S.M., Jenkinson M., Woolrich M.W., Beckmann C.F., Behrens T.E.J., Johansen-Berg H., Bannister P.R., De Luca M., Drobnjak I., Flitney D.E., Niazy R.K., Saunders J., Vickers J., Zhang Y., De Stefano N., Brady J.M., Matthews P.M. Advances in functional and structural MR image analysis and implementation as FSL. Neuroimage 2004, 23:S208-S219.
56. Stephan K.E., Weiskopf N., Drysdale P.M., Robinson P.A., Friston K.J. Comparing hemodynamic models with DCM. Neuroimage 2007, 38:387-401.
57. Tak S., Jang J., Lee K., Ye J.C. Quantification of CMRO(2) without hypercapnia using simultaneous near-infrared spectroscopy and fMRI measurements. Phys. Med. Biol. 2010, 55:3249-3269.
58. Van Zijl P.C.M., Eleff S.M., Ulatowski J.A., Oja J.M.E., Ulug A.M., Traystman R.J., Kauppinen R.A. Quantitative assessment of blood flow, blood volume and blood oxygenation effects in functional magnetic resonance imaging. Nat. Med. 1998, 4:159-167.
59. Wong E.C., Buxton R.B., Frank L.R. Implementation of quantitative perfusion imaging techniques for functional brain mapping using pulsed arterial spin labeling. NMR Biomed. 1997, 10:237-249.
60. Wong E.C., Buxton R.B., Frank L.R. Quantitative imaging of perfusion using a single subtraction (QUIPSS and QUIPSS II). Magn. Reson. Med. 1998, 39:702-708.
61. Xie J., Gallichan D., Gunn R.N., Jezzard P. Optimal design of pulsed arterial spin labeling MRI experiments. Magn. Reson. Med. 2008, 59:826-834.
62. Xu F., Ge Y., Lu H. Noninvasive quantification of whole-brain cerebral metabolic rate of oxygen (CMRO2) by MRI. Magn. Reson. Med. 2009, 62:141-148.
63. 2 challenge on vascular and metabolic parameters. ISMRM 2011, 19:765.
64. Xu F., Uh J., Brier M.R., Hart J., Yezhuvath U.S., Gu H., Yang Y., Lu H. The influence of carbon dioxide on brain activity and metabolism in conscious humans. J. Cereb. Blood Flow Metab. 2011, 31:58-67.
65. Zappe A.C., Uludag K., Oeltermann A., Ugurbil K., Logothetis N.K. The influence of moderate hypercapnia on neural activity in the anesthetized nonhuman primate. Cereb. Cortex 2008, 18:2666-2673.
66. Zhang Y.Y., Brady M., Smith S. Segmentation of brain MR images through a hidden Markov random field model and the expectation-maximization algorithm. IEEE Trans. Med. Imaging 2001, 20:45-57.
67. Zhu X.H., Zhang N., Zhang Y., Ugurbil K., Chen W. New insights into central roles of cerebral oxygen metabolism in the resting and stimulus-evoked brain. J. Cereb. Blood Flow Metab. 2009, 29:10-18.