Principles of EPR and Image Acquisition
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1 The University of Chicago Center for EPR Imaging in Vivo Physiology Principles of EPR and Image Acquisition Boris Epel
2 Outline Electron Paramagnetic Resonance (EPR) Oxygen Partial Tension Measuring using EPR What EPR can measure Imaging Instrumentation overview
3 The University of Chicago Center for EPR Imaging in Vivo Physiology Electron Paramagnetic Resonance
4 Electron Paramagnetic Resonance (EPR) Resonance of Unpaired Electron e - has magnetic moment µ B 0 in the absence of B 0 µ s are oriented arbitrarily in the absence of B 0 µ s are oriented arbitrarily
5 e - in the Magnetic Field Zeeman effect - splitting of energy levels into several components in the presence of a static magnetic field Quantum mechanics dictates that electron can be in one of two states: parallel or antiparallel to the magnetic field those have different energy
6 Boltzmann distribution A probability to find a particle in a state with energy E pp~ee EE kkkk Population difference pp dddd pp uuuu pp dddd = ee EE kkkk at 20 0 C Only small fraction of electrons can be observed Thermal equilibrium
7 EPR Signal (Quantum Mechanics) An unpaired electron can be moved between its two energy states through absorbing/emission of the alternating magnetic field energy hν = γβ 0 γ - gyromagnetic ratio, ν - alternating magnetic field frequency h Planck constant
8 EPR experiment approach 1 The uncertainty principle and magnetic interactions of e - with other magnetic particles (e - or nuclei) result in resonance line broadening (signal is observed at the field slightly different from Β 0 ) Electron paramagnetic resonance absorption is observed Alternating magnetic field at ν frequency is applied Magnetic field is scanned
9 EPR experiment approach 2 Electron paramagnetic resonance emission is observed from all spins at the same time Fourier transform of the signal gives EPR line Alternating magnetic field at all frequencies is applied Magnetic field is fixed A very short pulse at frequency ν generates a broad range of frequencies
10 Electron Paramagnetic Resonance Eugene Zavoyski First observation of EPR (1944) 133 MHz (4.75 mt) Zavoyski laboratory journal -> Kazan State University, Russia Zavoyski experimental setup RF amplifier from B-17
11 EPR Signal Anatomy Amplitude Integral of the spectrum Center field A 1,2,3 Line width Number of lines A Distance between lines Line shape Relaxation Kinetics
12 The University of Chicago Center for EPR Imaging in Vivo Physiology Oxygen partial tension (po2) measurement
13 Relaxation Relaxation - return of a perturbed system into equilibrium Irreversible loss of excitation energy T1 Longitudinal relaxation Spin-lattice relaxation Signal SS tt = SS 0 ee tttttttt TT 1 time
14 Relaxation Relaxation without the loss of total energy multiple spin effect Loss of the coherence T2 Transverse relaxation Spin-spin relaxation For large number of particles: SS tt = SS 0 ee tttttttt TT 2 Signal time
15 Relaxation rate It is convenient to define relaxation rate RR 1 = 1 TT 1 SS tt = SS 0 ee tttttttt TT 1 SS tt = SS 0 ee tttttttt RR 1
16 Relaxation sources T1 loss of the energy to the media (lattice) T2 loss of signal due to the loss of coherence. T1 contributes to T2 T2* - T2 observed in some experiments which do not correct for reversible loss of the coherence, T2 can be extracted EPR line shape T2* Interaction with other electrons (no energy transfer) - T2 Interaction with other electrons (energy transfer) T1, T2 Interaction with nuclei on the same molecule (reversible coherence loss) - T2*, T1 Interaction with media nuclei (irreversible coherence loss) T2, T1
17 What EPR can measure collision T2* Heisenberg spin exchange Low O 2 High O 2 T1, T2 Oxygen, po 2 Redox status Acidosis, ph Cell viability Viscosity etc
18 Molecular oxygen 18 Two unpaired electrons Very fast relaxation time: 1-10 ps Heisenberg exchange Electron of spin probe feels relaxing environment of the oxygen molecule during short time of the interaction More oxygen more interactions faster the relaxation σ* 2p MO π* 2p 2p π 2p 2p σ 2p 2s σ* 2s σ 2s 2s Both spin-spin and spin-lattice relation rates exhibit linear relations with p[o 2 ] O O
19 EPR oximetry Both spin-spin and spin-lattice relation rates exhibit linear relations with p[o 2 ]
20 Oxygen spin probes Soluble spin probes A Nitroxides B Trityl radicals Concentration of oxygen dissolved in a fluid Particulate (insoluble) spin probes C Lithium phthalocyanine and its derivatives Concentration of oxygen in material pores
21 Trityls Synthesized ~1996 by Nicomed Innovations, Sweden, currently GE Healthcare Longer relaxation: Symmetric shape, fast motion. At physiologic conditions and no O 2 T 1 T µs At 21% O 2 (blood saturated with O 2 ) T 1 T µs High sensitivity to O 2 and still measureable using pulse EPR Narrow EPR line high image resolution Clearance from a mouse: 5-20 minutes Non toxic, Well tolerated by animals The carbon based radical is sterically protected from environment - biostable Polar (3+): Does not enter cells. Locates in the extracellular volume. Bowman et al. J Mag Res 2004
22 The University of Chicago Center for EPR Imaging in Vivo Physiology What EPR can measure
23 What EPR can measure The redox state of the glutathione (GSH)/glutathione disulfide (GSSG) couple is considered to be the major intracellular redox buffer Roshchupkina, G. I., et al. (2008). Free Radical Biology and Medicine 45(3): Oxygen, po 2 Redox status Acidosis, ph Cell viability Viscosity etc
24 What EPR can measure Bobko, A. A., et al. (2012) Analytical Chemistry 84(14): Oxygen, po 2 Redox status Acidosis, ph Cell viability Viscosity etc
25 The University of Chicago Center for EPR Imaging in Vivo Physiology EPR in vivo Imaging
26 Magnetic Resonance Imaging Paul Lauterbur method (1973) Frequency encoding by application of the magnetic field gradients The inverse Radon transform was used for image reconstruction We use a similar method expanded to 3D and 4D 26
27 Magnetic Field Gradient The direction of B is always the same The direction of the magnetic field gradient can be changed BB = BB 0 + GG rr Homogeneous field, B 0 Linear gradient Linear gradient, GG ν ν ν ν B 0 ν
28 Imaging: Projections G=0 B = B 0 +Gr B 0 Gradient isocenter (B is always equal to B 0 ) G B 1 B 2 r Lauterbur PC. Nature 1973;242(5394): B r Rotation of the gradient direction is mathematically equivalent to rotation of the projection direction in Radon transformation original object can be restored
29 Image Dimensionality One dimensional Two dimensional Three-dimensional
30 Amplitude Imaging Distribution of spin-probe
31 Projection: Gradient Vector EPR spectrum collected under a gradient is called a projection 1D one gradient is sufficient GG 2D a plane of gradients is required G x GG G y G z GG 3D a sphere of gradients is necessary G x G y
32 Imaging Protocol Imaging protocol for 3D object Each point represents a gradient vector Vector starts at the coordinate origin and finished on the surface of a sphere Gradient vector length is the same for each orientation Only half of the sphere is required for the image For each gradient EPR spectrum is acquired
33 Parametric Imaging method 1 Low O 2 Slow relax. EPR spectral shape in every point of the sample should be imaged High O 2 Fast relax.
34 Method 1 - Spectral-Spatial Imaging Sampling gradient space by use of different gradients orientations and amplitudes Gradient vectors fill the volume of the unit sphere As a result EPR spectrum shape can be obtained in every image voxel This method collects ALL information about EPR spectra in the image Lower signal-to-noise ratio Longer acquisition T2 can be extracted from line shape T1 imaging is possible but rather complicated G z GG G x G y
35 in an Animal Spectral spatial (2D) image of a murine tumor
36 Verification: Oxylite TM probe A B
37 Pulse imaging Method 2 In some cases it is possible to simplify acquisition protocol by extracting only some information Pulse imaging allows to image the relaxation times using 3D imaging approach T 2 *, T 2 and T 1 are measured directly 3D imaging approach This dramatically improves image signal-tonoise ratio Higher precision and accuracy Limited to slowly relaxing spin-probes For in vivo oxymetry there are spin-probes that allow pulse acquisition (trityls) Pulse imaging is the method of choice for the oxymetry
38 The University of Chicago Center for EPR Imaging in Vivo Physiology Pulse EPR in vivo Oxygen Imaging
39 EPR experiment approach 2 Electron paramagnetic resonance emission is observed from all spins at the same time Fourier transform of the signal gives EPR line Alternating magnetic field at all frequencies is applied Magnetic field is fixed A very short pulse at frequency ν generates a broad range of frequencies
40 Pulse methods FID Free induction decay T2* Echo τ τ Spin echo sequences T2 IRESE T τ τ Inversion recovery T1
41 Relaxation time measurement Inversion recovery (IRESE) T 1 imaging T τ τ 3D images T τ τ T τ τ
42 Pulse po 2 image: T 1 ESE imaging Inversion recovery (IRESE) T 1 imaging T τ τ T τ τ T τ τ
43 po 2 images: T2 vs T1 Relaxation
44 ESE (T 2 ) vs. IRESE (T 1 ) Areas of tumor and normal tissues are resolved Red contours outline the borders of tumor identified in the registered T 2 -weigted MRI image. The po 2 histogram of tumor voxels is shown in red. 44
45 Partial Volume Effect C = N / V Excluded volume C = 4, C REAL = 4 C = 4, C REAL = 16 45
46 T1 imaging T 1 imaging shows only weak dependence on spin probe concentration and thus much more accurate T 1 based EPR imaging is the perfect method for precise oxygen imaging Image parameters spatial resolution temporal resolution po 2 resolution po 2 accuracy ~1 mm 1-10 min 1 torr 1-3 torr
47 EPRI vs MRI MRI EPR Magnetic field at 250 MHz 5.9 T 9 mt Radiofrequency pulse width μsec msec nsec Relaxation rates msec sec nsec - μsec Endogenous probes Water protons Exogenous probes - Nitroxides, trityl Concentration >60 M < 1 mm Stability Stable Minutes Line width Hz khz 100 khz - MHz -
48 Methods of Oxygen Measurement
49 49 Operational frequency Workshop 2014, Chicago 7/30/2014-7/31/2014 Signal to noise ratio grows with imager frequency However Biological samples contain large proportion of water. They are aqueous and highly dielectric. This results in (i) non-resonant absorption of energy (sample heating) and (ii) poor penetration of samples. These get worse with frequency What is the optimum frequency? - depends on sample size Frequenc y ~250 MHz ~750 MHz 1-2 GHz Penetration > 10 cm 6-8 cm cm Object Mouse, rat, rabbit Mouse, full body Mouse part
50 In Vivo Trityl iv line Bladder flushing line Resonator Mouse cradle Fiducials Gas anesthesia mask Cutaneous thermocouple Tumor in the cast
51 250 MHz Pulse EPR Imager Control SpecMan4EPR: Arbitrary pulse sequences Arbitrary gradient sequences Arbitrary pulse shapes (in development) Epel B. et al., Concepts in Magnetic Resonance, 33B (2008) Quine R.W. et al., Concepts in Magnetic Resonance, 15B (2002)
52 Acknowledgements University of Chicago NIH University of Denver University of Maryland University of Illinois in Urbana Champaign EB CA98575 People who worked in our lab and contributed to EPR imaging
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