Importance of X-Nuclei for Broadening Uses of Ultrahigh Field MR Imaging in Humans

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1 UHF Funding Conference 2015, NIH, Washington DC Importance of X-Nuclei for Broadening Uses of Ultrahigh Field MR Imaging in Humans Keith R. Thulborn, MD, PhD Professor of Radiology, Physiology & Biophysics Center for Magnetic Resonance Research University of Illinois

2 Sensitivity Requirement: [X] & γ Most MRI (based on 1 H signals of water & fat) Spatially-resolved biochemistry with other elements 1 H 80M, 23 Na 35mM, 17 O 16mM, 39 K 100mM, 31 P 3mM gamma { 1 H = 4x 23 Na;; 8x 17 O;; 24x 39 K;; 2x 31 P}

3 Goal: Comprehensive Metabolic Model of Human Biochemistry ( 23 Na, 39 K, 17 O, 31 P 13 C) Workload ATP 31 ATP 31 + Cr P i + ADP Na 23 ADP + P 31 Cr High energy ~P bioenergetics K 39 Glucose Glucose Pyruvate Acetyl CoA Cell Membrane Resting Membrane Potential ~ - 70mV V m = const.ln(p i [K i ] / p o [K o ]) CO 2 Acetyl CoA H 2 O 17 Oxidative Phosphorylation O 2 17 >60% of brain energy used for Na + /K + pump Brain tissue has high cell density: cell volume fraction 80%

4 E"0*/,->($A1&,$ "1&*0$,2($'(>$ >"+2(>$1/*($ PCr/ATP ratio, NAD+/NADH ~P Bioenergetics / redox state!"#$%&%$'()&*+,'-).&*$-+/*0$"11$,2($ '()(/3/*0$)&/1+$!(4045$ :5;5<#4$62($ %=9$/*$,2($'(>$?&7$/+$;@4@!$ 9()&*+,'-),(>$ /B"0($ CMRO2 (17O enrichment) Cerebral oxygen consumption (brain / heart) 17O!?#$%&%$'()&*+,'-).&*$-+/*0$"11$,2($ '()(/3($)&/1+$(7)(A,$,2($&*($ B",)2(>$C/,2$,2($,'"*+B/,$)&/1$!(4045$67897:5;5<#4$62($%=9$/+$;<4D"$!)#$=(C$'()&*+,'-).&*$-+/*0$"11$,2($ '()(/3/*0$)&/1+$!(4045$ :5;5<#4$$62($ %=9$/+$<84:4$ Anatomy SERIAL Imaging 1H Vm? Resting membrane potential 39K PCr γ- ATP PCr/γ- ATP 31P Biochemistry MRI Toolbox 23Na Cell density (brain) / Fixed charge density (cartilage)

5 23 Na Cell Volume Fraction Bioscale (Endogenous) Intraparenchymal Voxel V m = - 60mV ATP Na Na Na 145mM 12mM 20% 80% Christensen et al., MRM Comparison of 23 Na MRI & 22 Na radioisotope dilution in normal rat brain: equivalent results Thulborn et al., MRM Comparison of 23 Na MRI & 22 Na radioisotope dilution in rat brain tumors: equivalent results Vascular: Na 140mM, 2% VF v, Interstitial: Na 145mM, 18% Vf i but C v ~ C i Intracellular: Na 12mM, 80% CVF TSC = CVF.C c + (1-CVF).C i < 40 mm CVF = (TSC - C i )/(C c - C i ) Increasing TSC implies decreasing cell volume fraction CVF

6 Quantitative Biochemisty

7 CVF with Normal Ageing N=49 Cell volume fraction is stable with normal ageing! Neurons become smaller & ECM decreases at same rate (volume loss is NOT from loss of neurons) Thulborn et al., NMR Biomed, 2015

8 A Relevant Medical Question? Normal Cognition MCI Dementia? Can CVF detect cell loss in early degenerative disease?

9 17 O MRI CMRO 2 Model (Enrichment) H 17 2 O H 17 2 O H 17 2 O Gain Creation Loss Voxel l H dm 17O 2 V (t) = 2 CMRO dt 2 A 17O H (t) K L M 17O 2 V (t) + K G B H 17O 2 (t) Rate constants summarize labeled water gain and loss l l l CMRO 2 : Creation of labeled water K G : Gain due to wash-in (labeled water in blood) K L : Loss due to wash-out and conversion Atkinson & Thulborn, Neuroimage 2010

10 17 O CMRO2 corrected for Tissue Mass CMRO 2 TSC Atkinson & Thulborn, Neuroimage 2010

11 17 O MRI of Glioblastoma: 7T Assess oxygen metabolism First 17 O 2 inhalation experiment in a tumor patient Geometric transfer matrix for correction of partial volume effects reduced CMRO2 in tumor compartments 1) Hoffmann, Radbruch, Semmler, Nagel. MAGMA 2014 (2014) 27: ) Rousset et al. J Nucl Med 39(5):

12 (Quantitative cognitive workload) Supplied by Wei Chen, 2015

13 31P MR Imaging PCr γ- ATP PCr/γ- ATP P PCr and ATP images over 23Na image PCr/γ- ATP ratios for 3 volunteers: 1.46 ± 0.27 Spectral selective RF pulse with flextpi readout = SIMPLE- TPI Lu, Atkinson, Zhou & Thulborn, MRM ± ± 0.31 SLE patient 1.54±0.3 Spectral selective RF pulse whole head spectrum

14 NAD + /NADH MRS Redox State in Human Brain 200 PCr Residual Xiao-Hong Zhu, Ming Lu, Byeong- Yeul Lee, Kamil Ugurbil and Wei Chen α-atp Original NAD + PNAS, 2015;;112: PME Pi PDE γ-atp Fitting NADH β-atp NAD + /NADH Redox Ratio Age (year) Chemical Shift (ppm) NAD Content (µmol/g) [NAD + ] 14 [NADH] Age (year) Demonstration of the in vivo 31 P MRS based NAD assay for quantifying cellular NAD + and NADH contents in human occipital lobe (highlighted in the brain anatomic image) at 7T. The results revealed a significant decline of NAD + /NADH redox state in healthy elderly people.

15 Human SERIAL 1 H Images SERIAL 2D FLASH Stria of Gennari Voxel size = 0.4 x 0.4 x 4 mm 3 2 minute acquisition

16 X-Nuclei Summary: Need for UHF Quantification of rates & concentrations is the new dimension, possibly enabling metabolic modeling of human biochemistry, possibly to predict health & illness and to measure longitudinal responses & development without ionizing radiation ( Man on Moon Mission statement ): Sensitivity enhancement of endogeneous X nuclei (low gamma, low concentration, e.g., 23 Na) Enrichment approaches (e.g., 17 O, 7 Li, 19 F,. etc) SAR increases at UHF but Quantification reduces duty cycle to avoid T 1 saturation except for very short T 1 species (e.g., 39 K) Partial Volume Effects due to spatial resolution limit accuracy of quantification

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