Three-dimensional mapping of the creatine kinase enzyme reaction rate in muscles of the lower leg

Phosphorus (31P) magnetization transfer (MT) techniques enable the non‐invasive measurement of metabolic turnover rates of important enzyme‐catalyzed reactions, such as the creatine kinase reaction (CK), a major transducing reaction involving adenosine triphosphate and phosphocreatine. Alteration in...

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Published inNMR in biomedicine Vol. 26; no. 9; pp. 1142 - 1151
Main Authors Parasoglou, Prodromos, Xia, Ding, Chang, Gregory, Convit, Antonio, Regatte, Ravinder R.
Format Journal Article
LanguageEnglish
Published England Blackwell Publishing Ltd 01.09.2013
Wiley Subscription Services, Inc
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Online AccessGet full text
ISSN0952-3480
1099-1492
1099-1492
DOI10.1002/nbm.2928

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Abstract Phosphorus (31P) magnetization transfer (MT) techniques enable the non‐invasive measurement of metabolic turnover rates of important enzyme‐catalyzed reactions, such as the creatine kinase reaction (CK), a major transducing reaction involving adenosine triphosphate and phosphocreatine. Alteration in the kinetics of the CK reaction rate appears to play a central role in many disease states. In this study, we developed and implemented at ultra‐high field (7T) a novel three‐dimensional 31P‐MT imaging sequence that maps the kinetics of CK in the entire volume of the lower leg at relatively high resolution (0.52 mL voxel size), and within acquisition times that can be tolerated by patients (below 60 min). We tested the sequence on five healthy and two clinically diagnosed type 2 diabetic subjects. Overall, we obtained measurements that are in close agreement with measurements reported previously using spectroscopic methods. Importantly, our spatially resolved method allowed us to measure local CK reaction rate constants and metabolic fluxes in individual muscles in a non‐invasive manner. Furthermore, it allowed us to detect variations of the CK rates of different muscles, which would not have been possible using unlocalized MRS methods. The results of this work suggest that 3D mapping of the CK reaction rates and metabolic fluxes can be achieved in the skeletal muscle in vivo at relatively high spatial resolution and with acquisition times well tolerated by patients. The ability to measure bioenergetics simultaneously in large areas of muscles will bring new insights into possible heterogeneous patterns of muscle metabolism associated with several diseases and serve as a valuable tool for monitoring the efficacy of interventions. Copyright © 2013 John Wiley & Sons, Ltd. In this study, we developed and implemented a novel three‐dimensional 31P‐MT imaging sequence that maps the kinetics of CK in the entire volume of the lower leg within acquisition times that can be tolerated by patients. We tested the sequence on five healthy and two clinically diagnosed type 2 diabetic subjects. Overall, we obtained measurements that are in close agreement with measurements reported previously using spectroscopic methods. Importantly, our spatially resolved method allowed us, in the case of diabetic patients, to detect variations of the CK rate of different calf muscles, which would not have been possible using unlocalized MRS methods.
AbstractList Phosphorous (31P) magnetization transfer (MT) techniques enable the non-invasive measurement of metabolic turnover rates of important enzyme catalyzed reactions, such as the creatine kinase reaction (CK), a major transducing reaction involving adenosine triphosphate and phosphocreatine. Alteration in the kinetics of the CK reaction rate appears to play a central role in many disease states. In this study, we developed and implemented at ultra-high field (7T), a novel three-dimensional 31P-MT imaging sequence that maps the kinetics of CK in the entire volume of the lower leg at relatively high resolution (0.52 mL voxel size), and within acquisition times that can be tolerated by patients (below 60 min). We tested the sequence on five healthy and two clinically diagnosed type 2-diabetic patients. Overall, we obtained measurements that are in close agreement with measurements reported previously using spectroscopic methods. Importantly, our spatially resolved method allowed us to measure local CK reaction rate constants and metabolic fluxes in individual muscles in healthy subjects. Furthermore, in the case of patients with diabetes, it allowed us to detect variations of the CK rate of different muscles, which would not have been possible using unlocalized MRS methods. The results of this work suggest that 3D-mapping of the CK reaction rates and metabolic fluxes can be achieved in the skeletal muscle in vivo at relatively high spatial resolution and with acquisition times well tolerated by patients. The ability to measure bioenergetics simultaneously in large areas of muscles will bring new insights into possible heterogeneous patterns of muscle metabolism associated with several diseases and serve as a valuable tool for monitoring the efficacy of interventions.
Phosphorus ((31) P) magnetization transfer (MT) techniques enable the non-invasive measurement of metabolic turnover rates of important enzyme-catalyzed reactions, such as the creatine kinase reaction (CK), a major transducing reaction involving adenosine triphosphate and phosphocreatine. Alteration in the kinetics of the CK reaction rate appears to play a central role in many disease states. In this study, we developed and implemented at ultra-high field (7T) a novel three-dimensional (31) P-MT imaging sequence that maps the kinetics of CK in the entire volume of the lower leg at relatively high resolution (0.52 mL voxel size), and within acquisition times that can be tolerated by patients (below 60 min). We tested the sequence on five healthy and two clinically diagnosed type 2 diabetic subjects. Overall, we obtained measurements that are in close agreement with measurements reported previously using spectroscopic methods. Importantly, our spatially resolved method allowed us to measure local CK reaction rate constants and metabolic fluxes in individual muscles in a non-invasive manner. Furthermore, it allowed us to detect variations of the CK rates of different muscles, which would not have been possible using unlocalized MRS methods. The results of this work suggest that 3D mapping of the CK reaction rates and metabolic fluxes can be achieved in the skeletal muscle in vivo at relatively high spatial resolution and with acquisition times well tolerated by patients. The ability to measure bioenergetics simultaneously in large areas of muscles will bring new insights into possible heterogeneous patterns of muscle metabolism associated with several diseases and serve as a valuable tool for monitoring the efficacy of interventions.
Phosphorus ( 31 P) magnetization transfer (MT) techniques enable the non‐invasive measurement of metabolic turnover rates of important enzyme‐catalyzed reactions, such as the creatine kinase reaction (CK), a major transducing reaction involving adenosine triphosphate and phosphocreatine. Alteration in the kinetics of the CK reaction rate appears to play a central role in many disease states. In this study, we developed and implemented at ultra‐high field (7T) a novel three‐dimensional 31 P‐MT imaging sequence that maps the kinetics of CK in the entire volume of the lower leg at relatively high resolution (0.52 mL voxel size), and within acquisition times that can be tolerated by patients (below 60 min). We tested the sequence on five healthy and two clinically diagnosed type 2 diabetic subjects. Overall, we obtained measurements that are in close agreement with measurements reported previously using spectroscopic methods. Importantly, our spatially resolved method allowed us to measure local CK reaction rate constants and metabolic fluxes in individual muscles in a non‐invasive manner. Furthermore, it allowed us to detect variations of the CK rates of different muscles, which would not have been possible using unlocalized MRS methods. The results of this work suggest that 3D mapping of the CK reaction rates and metabolic fluxes can be achieved in the skeletal muscle in vivo at relatively high spatial resolution and with acquisition times well tolerated by patients. The ability to measure bioenergetics simultaneously in large areas of muscles will bring new insights into possible heterogeneous patterns of muscle metabolism associated with several diseases and serve as a valuable tool for monitoring the efficacy of interventions. Copyright © 2013 John Wiley & Sons, Ltd.
Phosphorus (31P) magnetization transfer (MT) techniques enable the non-invasive measurement of metabolic turnover rates of important enzyme-catalyzed reactions, such as the creatine kinase reaction (CK), a major transducing reaction involving adenosine triphosphate and phosphocreatine. Alteration in the kinetics of the CK reaction rate appears to play a central role in many disease states. In this study, we developed and implemented at ultra-high field (7T) a novel three-dimensional 31P-MT imaging sequence that maps the kinetics of CK in the entire volume of the lower leg at relatively high resolution (0.52 mL voxel size), and within acquisition times that can be tolerated by patients (below 60 min). We tested the sequence on five healthy and two clinically diagnosed type 2 diabetic subjects. Overall, we obtained measurements that are in close agreement with measurements reported previously using spectroscopic methods. Importantly, our spatially resolved method allowed us to measure local CK reaction rate constants and metabolic fluxes in individual muscles in a non-invasive manner. Furthermore, it allowed us to detect variations of the CK rates of different muscles, which would not have been possible using unlocalized MRS methods. The results of this work suggest that 3D mapping of the CK reaction rates and metabolic fluxes can be achieved in the skeletal muscle in vivo at relatively high spatial resolution and with acquisition times well tolerated by patients. The ability to measure bioenergetics simultaneously in large areas of muscles will bring new insights into possible heterogeneous patterns of muscle metabolism associated with several diseases and serve as a valuable tool for monitoring the efficacy of interventions. Copyright © 2013 John Wiley & Sons, Ltd. [PUBLICATION ABSTRACT]
Phosphorus (31P) magnetization transfer (MT) techniques enable the non‐invasive measurement of metabolic turnover rates of important enzyme‐catalyzed reactions, such as the creatine kinase reaction (CK), a major transducing reaction involving adenosine triphosphate and phosphocreatine. Alteration in the kinetics of the CK reaction rate appears to play a central role in many disease states. In this study, we developed and implemented at ultra‐high field (7T) a novel three‐dimensional 31P‐MT imaging sequence that maps the kinetics of CK in the entire volume of the lower leg at relatively high resolution (0.52 mL voxel size), and within acquisition times that can be tolerated by patients (below 60 min). We tested the sequence on five healthy and two clinically diagnosed type 2 diabetic subjects. Overall, we obtained measurements that are in close agreement with measurements reported previously using spectroscopic methods. Importantly, our spatially resolved method allowed us to measure local CK reaction rate constants and metabolic fluxes in individual muscles in a non‐invasive manner. Furthermore, it allowed us to detect variations of the CK rates of different muscles, which would not have been possible using unlocalized MRS methods. The results of this work suggest that 3D mapping of the CK reaction rates and metabolic fluxes can be achieved in the skeletal muscle in vivo at relatively high spatial resolution and with acquisition times well tolerated by patients. The ability to measure bioenergetics simultaneously in large areas of muscles will bring new insights into possible heterogeneous patterns of muscle metabolism associated with several diseases and serve as a valuable tool for monitoring the efficacy of interventions. Copyright © 2013 John Wiley & Sons, Ltd. In this study, we developed and implemented a novel three‐dimensional 31P‐MT imaging sequence that maps the kinetics of CK in the entire volume of the lower leg within acquisition times that can be tolerated by patients. We tested the sequence on five healthy and two clinically diagnosed type 2 diabetic subjects. Overall, we obtained measurements that are in close agreement with measurements reported previously using spectroscopic methods. Importantly, our spatially resolved method allowed us, in the case of diabetic patients, to detect variations of the CK rate of different calf muscles, which would not have been possible using unlocalized MRS methods.
Phosphorus ((31) P) magnetization transfer (MT) techniques enable the non-invasive measurement of metabolic turnover rates of important enzyme-catalyzed reactions, such as the creatine kinase reaction (CK), a major transducing reaction involving adenosine triphosphate and phosphocreatine. Alteration in the kinetics of the CK reaction rate appears to play a central role in many disease states. In this study, we developed and implemented at ultra-high field (7T) a novel three-dimensional (31) P-MT imaging sequence that maps the kinetics of CK in the entire volume of the lower leg at relatively high resolution (0.52 mL voxel size), and within acquisition times that can be tolerated by patients (below 60 min). We tested the sequence on five healthy and two clinically diagnosed type 2 diabetic subjects. Overall, we obtained measurements that are in close agreement with measurements reported previously using spectroscopic methods. Importantly, our spatially resolved method allowed us to measure local CK reaction rate constants and metabolic fluxes in individual muscles in a non-invasive manner. Furthermore, it allowed us to detect variations of the CK rates of different muscles, which would not have been possible using unlocalized MRS methods. The results of this work suggest that 3D mapping of the CK reaction rates and metabolic fluxes can be achieved in the skeletal muscle in vivo at relatively high spatial resolution and with acquisition times well tolerated by patients. The ability to measure bioenergetics simultaneously in large areas of muscles will bring new insights into possible heterogeneous patterns of muscle metabolism associated with several diseases and serve as a valuable tool for monitoring the efficacy of interventions.Phosphorus ((31) P) magnetization transfer (MT) techniques enable the non-invasive measurement of metabolic turnover rates of important enzyme-catalyzed reactions, such as the creatine kinase reaction (CK), a major transducing reaction involving adenosine triphosphate and phosphocreatine. Alteration in the kinetics of the CK reaction rate appears to play a central role in many disease states. In this study, we developed and implemented at ultra-high field (7T) a novel three-dimensional (31) P-MT imaging sequence that maps the kinetics of CK in the entire volume of the lower leg at relatively high resolution (0.52 mL voxel size), and within acquisition times that can be tolerated by patients (below 60 min). We tested the sequence on five healthy and two clinically diagnosed type 2 diabetic subjects. Overall, we obtained measurements that are in close agreement with measurements reported previously using spectroscopic methods. Importantly, our spatially resolved method allowed us to measure local CK reaction rate constants and metabolic fluxes in individual muscles in a non-invasive manner. Furthermore, it allowed us to detect variations of the CK rates of different muscles, which would not have been possible using unlocalized MRS methods. The results of this work suggest that 3D mapping of the CK reaction rates and metabolic fluxes can be achieved in the skeletal muscle in vivo at relatively high spatial resolution and with acquisition times well tolerated by patients. The ability to measure bioenergetics simultaneously in large areas of muscles will bring new insights into possible heterogeneous patterns of muscle metabolism associated with several diseases and serve as a valuable tool for monitoring the efficacy of interventions.
Phosphorus ( super(31)P) magnetization transfer (MT) techniques enable the non-invasive measurement of metabolic turnover rates of important enzyme-catalyzed reactions, such as the creatine kinase reaction (CK), a major transducing reaction involving adenosine triphosphate and phosphocreatine. Alteration in the kinetics of the CK reaction rate appears to play a central role in many disease states. In this study, we developed and implemented at ultra-high field (7T) a novel three-dimensional super(31)P-MT imaging sequence that maps the kinetics of CK in the entire volume of the lower leg at relatively high resolution (0.52 mL voxel size), and within acquisition times that can be tolerated by patients (below 60 min). We tested the sequence on five healthy and two clinically diagnosed type 2 diabetic subjects. Overall, we obtained measurements that are in close agreement with measurements reported previously using spectroscopic methods. Importantly, our spatially resolved method allowed us to measure local CK reaction rate constants and metabolic fluxes in individual muscles in a non-invasive manner. Furthermore, it allowed us to detect variations of the CK rates of different muscles, which would not have been possible using unlocalized MRS methods. The results of this work suggest that 3D mapping of the CK reaction rates and metabolic fluxes can be achieved in the skeletal muscle in vivo at relatively high spatial resolution and with acquisition times well tolerated by patients. The ability to measure bioenergetics simultaneously in large areas of muscles will bring new insights into possible heterogeneous patterns of muscle metabolism associated with several diseases and serve as a valuable tool for monitoring the efficacy of interventions. Copyright copyright 2013 John Wiley & Sons, Ltd. In this study, we developed and implemented a novel three-dimensional super(31)P-MT imaging sequence that maps the kinetics of CK in the entire volume of the lower leg within acquisition times that can be tolerated by patients. We tested the sequence on five healthy and two clinically diagnosed type 2 diabetic subjects. Overall, we obtained measurements that are in close agreement with measurements reported previously using spectroscopic methods. Importantly, our spatially resolved method allowed us, in the case of diabetic patients, to detect variations of the CK rate of different calf muscles, which would not have been possible using unlocalized MRS methods.
Author Chang, Gregory
Xia, Ding
Regatte, Ravinder R.
Convit, Antonio
Parasoglou, Prodromos
AuthorAffiliation 2 Departments of Psychiatry and Medicine, New York University Langone Medical Center, New York, NY, USA
1 Quantitative Multinuclear Musculoskeletal Imaging Group (QMMIG), Department of Radiology, Center for Biomedical Imaging, New York University Langone Medical Center, New York, NY, USA
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  email: Correspondence to: Prodromos Parasoglou, PhD, Center of Biomedical Imaging, Department of Radiology, NYU Langone Medical Center, 660 First Avenue (4th floor), New York, NY 10016, USA., prodromos.parasoglou@nyumc.org
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Issue 9
Keywords phosphorus MRI
magnetization transfer
muscle metabolism
creatine kinase
Language English
License http://onlinelibrary.wiley.com/termsAndConditions#vor
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PublicationDate September 2013
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  text: September 2013
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PublicationTitle NMR in biomedicine
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PublicationYear 2013
Publisher Blackwell Publishing Ltd
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– name: Wiley Subscription Services, Inc
References Kemp GJ, Radda GK. Quantitative interpretation of bioenergetic data from 31P and 1H magnetic resonance spectroscopic studies of skeletal muscle. Magn. Reson. Q. 1994; 10(1): 43-63.
Chao H, Bowers JL, Holtzman D, Mulkern RV. RARE imaging of PCr in human forearm muscles. J. Magn. Reson. Imaging 1997; 7(6): 1048-1055.
Bogner W, Chmelik M, Schmid AI, Moser E, Trattnig S, Gruber S. Assessment of (31)P relaxation times in the human calf muscle: a comparison between 3 T and 7 T in vivo. Magn. Reson. Med. 2009; 62(3): 574-582.
Johnson MA, Polgar J, Weightma D, Appleton D. Data on distribution of fiber types in 36 human muscles. Autopsy study. J. Neurol. Sci. 1973; 18(1): 111-129.
Du F, Zhu X-H, Qiao H, Zhang X, Chen W. Efficient in vivo P-31 magnetization transfer approach for noninvasively determining multiple kinetic parameters and metabolic fluxes of ATP metabolism in the human brain. Magn. Reson. Med. 2007; 57(1): 103-114.
Kupce E, Freeman R. Adiabatic pulses for wide-band inversion and broad-band decoupling. J. Magn. Reson. Ser. A 1995; 115(2): 273-276.
Hetherington HP, Spencer DD, Vaughan JT, Pan JW. Quantitative P-31 spectroscopic imaging of human brain at 4 tesla: assessment of gray and white matter differences of phosphocreatine and ATP. Magn. Reson. Med. 2001; 45(1): 46-52.
Bottomley PA, Ouwerkerk R, Lee RF, Weiss RG. Four-angle saturation transfer (FAST) method for measuring creatine kinase reaction rates in vivo. Magn. Reson. Med. 2002; 47(5): 850-863.
Kholmovski EG, Parker DL, Alexander AL. A generalized k-sampling scheme for 3D fast spin echo. J. Magn. Reson. Imaging 2000; 11(5): 549-558.
Parasoglou P, Xia D, Chang G, Regatte RR. Dynamic imaging of phosphocreatine recovery kinetics in the human lower leg muscles at 3T and 7T: a preliminary study. NMR Biomed. 2013; 26(3): 348-356.
Duncan BB, Schmidt MI, Pankow JS, Ballantyne CM, Couper D, Vigo A, Hoogeveen R, Folsom AR, Heiss G. Low-grade systemic inflammation and the development of type 2 diabetes - the Atherosclerosis Risk in Communities Study. Diabetes 2003; 52(7): 1799-1805.
Taylor DJ. Clinical utility of muscle MR spectroscopy. Semin. Musculoskeletal Radiol. 2000; 4(4): 481-502.
Greenman RL, Axel L, Ferrari VA, Lenkinski RE. Fast imaging of phosphocreatine in the normal human myocardium using a three-dimensional RARE pulse sequence at 4 tesla. J. Magn. Reson. Imaging 2002; 15(4): 467-472.
Greenman RL, Elliott MA, Vandenborne K, Schnall MD, Lenkinski RE. Fast imaging of phosphocreatine using a RARE pulse sequence. Magn. Reson. Med. 1998; 39(5): 851-854.
Jennings RB, Reimer KA. Lethal myocardial ischemic-injury. Am. J. Pathol. 1981; 102(2): 241-255.
Chao H, Bowers JL, Holtzman D, Mulkern RV. Multi-echo 31P spectroscopic imaging of ATP: a scan time reduction strategy. J. Magn. Reson. Imaging 1997; 7(2): 425-433.
Kelley DE, He J, Menshikova EV, Ritov VB. Dysfunction of mitochondria in human skeletal muscle in type 2 diabetes. Diabetes 2002; 51(10): 2944-2950.
Degani H, Laughlin M, Campbell S, Shulman RG. Kinetics of creatine kinase in heart - a P31 saturation-transfer and inversion-transfer study. Biochemistry 1985; 24(20): 5510-5516.
Greenman RL, Wang X, Smithline HA. Simultaneous acquisition of phosphocreatine and inorganic phosphate images for Pi:PCr ratio mapping using a RARE sequence with chemically selective interleaving. Magn. Reson. Imaging 2011; 29(8): 1138-1144.
Alger JR, Shulman RG. NMR-studies of enzymatic rates in vitro and in vivo by magnetization transfer. Q. Rev. Biophys. 1984; 17(1): 83-124.
Ingwall JS. Is cardiac-failure a consequence of decreased energy reserve? Circulation 1993; 87(6): 58-62.
Parasoglou P, Feng L, Xia D, Otazo R, Regatte RR. Rapid 3D-imaging of phosphocreatine recovery kinetics in the human lower leg muscles with compressed sensing. Magn. Reson. Med. 2012; 68(6): 1738-1746.
Parasoglou P, Xia D, Regatte RR. Spectrally selective 3D TSE imaging of phosphocreatine in the human calf muscle at 3 T. Magn. Reson. Med. 2012. DOI: 10.1002/mrm.24288
Forsen S, Hoffman RA. Study of moderately rapid chemical exchange reactions by means of nuclear magnetic double resonance. J. Chem. Phys. 1963; 39(11): 2892-2901.
Sun PZ, Benner T, Kumar A, Sorensen AG. Investigation of optimizing and translating pH-sensitive pulsed-chemical exchange saturation transfer (CEST) imaging to a 3T clinical scanner. Magn. Reson. Med. 2008; 60(4): 834-841.
Bottomley PA, Ouwerkerk R. Optimum flip-angles for exciting NMR uncertain T1 values. Magn. Reson. Med. 1994; 32(1): 137-141.
Marjanska M, Eberly LE, Adriany G, Verdoliva SN, Garwood M, Chow L. Influence of foot orientation on the appearance and quantification of (1) H magnetic resonance muscle spectra obtained from the soleus and the vastus lateralis. Magn. Reson. Med. 2012; 68(6): 1731-1737.
Kemp GJ, Meyerspeer M, Moser E. Absolute quantification of phosphorus metabolite concentrations in human muscle in vivo by P-31 MRS: a quantitative review. NMR Biomed. 2007; 20(6): 555-565.
Lanza IR, Larsen RG, Kent-Braun JA. Effects of old age on human skeletal muscle energetics during fatiguing contractions with and without blood flow. J. Physiol. (Lond.) 2007; 583(3): 1093-1105.
Radda GK. The use of NMR spectroscopy for the understanding of disease. Science 1986; 233(4764): 640-645.
Valkovic L, Chmelik M, Kukurova IJ, Krssak M, Gruber S, Frollo I, Trattnig S, Bogner W. Time-resolved phosphorus magnetization transfer of the human calf muscle at 3 T and 7 T: a feasibility study. Eur. J. Radiol. DOI: 10.1016/j.ejrad.2011.09.024
Prompers JJ, Jeneson JAL, Drost MR, Oomens CCW, Strijkers GJ, Nicolay K. Dynamic MRS and MRI of skeletal muscle function and biomechanics. NMR Biomed. 2006; 19(7): 927-953.
Yarnykh VL. Actual flip-angle imaging in the pulsed steady state: a method for rapid three-dimensional mapping of the transmitted radiofrequency field. Magn. Reson. Med. 2007; 57(1): 192-200.
Karampinos DC, Baum T, Nardo L, Alizai H, Yu H, Carballido-Gamio J, Yap P, Shimakawa A, Link TM, Majumdar S. Characterization of the regional distribution of skeletal muscle adipose tissue in type 2 diabetes using chemical shift-based water/fat separation. J. Magn. Reson. Imaging 2012; 35(4): 899-907.
Hood DA. Plasticity in skeletal, cardiac, and smooth muscle - invited review: contractile activity-induced mitochondrial biogenesis in skeletal muscle. J. Appl. Physiol. 2001; 90(3): 1137-1157.
Collewet G, Davenel A, Toussaint C, Akoka S. Correction of intensity nonuniformity in spin-echo T(1)-weighted images. Magn. Reson. Imaging 2002; 20(4): 365-373.
Schar M, El-Sharkawy A-MM, Weiss RG, Bottomley PA. Triple repetition time saturation transfer (TRiST) (31)P spectroscopy for measuring human creatine kinase reaction kinetics. Magn. Reson. Med. 2010; 63(6): 1493-1501.
Greenman RL, Smithline HA. The feasibility of measuring phosphocreatine recovery kinetics in muscle using a single-shot (31)P RARE MRI sequence. Acad. Radiol. 2011; 18(7): 917-923.
Hands LJ, Bore PJ, Galloway G, Morris PJ, Radda GK. Muscle metabolism in patients with peripheral vascular-disease investigated by 31P nuclear-magnetic resonance spectroscopy. Clin. Sci. 1986; 71(3): 283-290.
Befroy DE, Shulman GI. Magnetic resonance spectroscopy studies of human metabolism. Diabetes 2011; 60(5): 1361-1369.
Bogner W, Chmelik M, Andronesi OC, Sorensen AG, Trattnig S, Gruber S. In vivo (31)P spectroscopy by fully adiabatic extended image selected in vivo spectroscopy: a comparison between 3 T and 7 T. Magn. Reson. Med. 2011; 66(4): 923-930.
Boesch C, Kreis R. Dipolar coupling and ordering effects observed in magnetic resonance spectra of skeletal muscle. NMR Biomed. 2001; 14(2): 140-148.
Reeder SB, McKenzie CA, Pineda AR, Yu H, Shimakawa A, Brau AC, Hargreaves BA, Gold GE, Brittain JH. Water-fat separation with IDEAL gradient-echo imaging. J. Magn. Reson. Imaging 2007; 25(3): 644-652.
Parry A, Matthews PM. Roles for imaging in understanding the pathophysiology, clinical evaluation, and management of patients with mitochondrial disease. J. Neuroimaging 2003; 13(4): 293-302.
Moller HE, Wiedermann D. Magnetization-transfer P-31 NMR of biochemical exchange in vivo: application to creatine kinase kinetics. J. Spectrosc. 2002; 16(3/4): 207-216.
Oberbach A, Bossenz Y, Lehmann S, Niebauer J, Adams V, Paschke R, Schon MR, Bluher M, Punkt K. Altered fiber distribution and fiber-specific glycolytic and oxidative enzyme activity in skeletal muscle of patients with type 2 diabetes. Diabetes Care 2006; 29(4): 895-900.
Boesch C, Machann J, Vermathen P, Schick F. Role of proton MR for the study of muscle lipid metabolism. NMR Biomed. 2006; 19(7): 968-988.
Lu A, Atkinson IC, Zhou XJ, Thulborn KR. PCr/ATP ratio mapping of the human head by simultaneously imaging of multiple spectral peaks with interleaved excitations and flexible twisted projection imaging readout trajectories at 9.4 T. Magn. Reson. Med. 2012. DOI: 10.1002/mrm.24281
Greenman RL. Quantification of the P-31 metabolite concentration in human skeletal muscle from RARE image intensity. Magn. Reson. Med. 2004; 52(5): 1036-1042.
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References_xml – reference: Greenman RL, Wang X, Smithline HA. Simultaneous acquisition of phosphocreatine and inorganic phosphate images for Pi:PCr ratio mapping using a RARE sequence with chemically selective interleaving. Magn. Reson. Imaging 2011; 29(8): 1138-1144.
– reference: Greenman RL, Elliott MA, Vandenborne K, Schnall MD, Lenkinski RE. Fast imaging of phosphocreatine using a RARE pulse sequence. Magn. Reson. Med. 1998; 39(5): 851-854.
– reference: Boesch C, Machann J, Vermathen P, Schick F. Role of proton MR for the study of muscle lipid metabolism. NMR Biomed. 2006; 19(7): 968-988.
– reference: Du F, Zhu X-H, Qiao H, Zhang X, Chen W. Efficient in vivo P-31 magnetization transfer approach for noninvasively determining multiple kinetic parameters and metabolic fluxes of ATP metabolism in the human brain. Magn. Reson. Med. 2007; 57(1): 103-114.
– reference: Bottomley PA, Ouwerkerk R. Optimum flip-angles for exciting NMR uncertain T1 values. Magn. Reson. Med. 1994; 32(1): 137-141.
– reference: Schar M, El-Sharkawy A-MM, Weiss RG, Bottomley PA. Triple repetition time saturation transfer (TRiST) (31)P spectroscopy for measuring human creatine kinase reaction kinetics. Magn. Reson. Med. 2010; 63(6): 1493-1501.
– reference: Kelley DE, He J, Menshikova EV, Ritov VB. Dysfunction of mitochondria in human skeletal muscle in type 2 diabetes. Diabetes 2002; 51(10): 2944-2950.
– reference: Oberbach A, Bossenz Y, Lehmann S, Niebauer J, Adams V, Paschke R, Schon MR, Bluher M, Punkt K. Altered fiber distribution and fiber-specific glycolytic and oxidative enzyme activity in skeletal muscle of patients with type 2 diabetes. Diabetes Care 2006; 29(4): 895-900.
– reference: Reeder SB, McKenzie CA, Pineda AR, Yu H, Shimakawa A, Brau AC, Hargreaves BA, Gold GE, Brittain JH. Water-fat separation with IDEAL gradient-echo imaging. J. Magn. Reson. Imaging 2007; 25(3): 644-652.
– reference: Ingwall JS. Is cardiac-failure a consequence of decreased energy reserve? Circulation 1993; 87(6): 58-62.
– reference: Chao H, Bowers JL, Holtzman D, Mulkern RV. RARE imaging of PCr in human forearm muscles. J. Magn. Reson. Imaging 1997; 7(6): 1048-1055.
– reference: Boesch C, Kreis R. Dipolar coupling and ordering effects observed in magnetic resonance spectra of skeletal muscle. NMR Biomed. 2001; 14(2): 140-148.
– reference: Moller HE, Wiedermann D. Magnetization-transfer P-31 NMR of biochemical exchange in vivo: application to creatine kinase kinetics. J. Spectrosc. 2002; 16(3/4): 207-216.
– reference: Collewet G, Davenel A, Toussaint C, Akoka S. Correction of intensity nonuniformity in spin-echo T(1)-weighted images. Magn. Reson. Imaging 2002; 20(4): 365-373.
– reference: Valkovic L, Chmelik M, Kukurova IJ, Krssak M, Gruber S, Frollo I, Trattnig S, Bogner W. Time-resolved phosphorus magnetization transfer of the human calf muscle at 3 T and 7 T: a feasibility study. Eur. J. Radiol. DOI: 10.1016/j.ejrad.2011.09.024
– reference: Johnson MA, Polgar J, Weightma D, Appleton D. Data on distribution of fiber types in 36 human muscles. Autopsy study. J. Neurol. Sci. 1973; 18(1): 111-129.
– reference: Karampinos DC, Baum T, Nardo L, Alizai H, Yu H, Carballido-Gamio J, Yap P, Shimakawa A, Link TM, Majumdar S. Characterization of the regional distribution of skeletal muscle adipose tissue in type 2 diabetes using chemical shift-based water/fat separation. J. Magn. Reson. Imaging 2012; 35(4): 899-907.
– reference: Parasoglou P, Xia D, Regatte RR. Spectrally selective 3D TSE imaging of phosphocreatine in the human calf muscle at 3 T. Magn. Reson. Med. 2012. DOI: 10.1002/mrm.24288
– reference: Bogner W, Chmelik M, Schmid AI, Moser E, Trattnig S, Gruber S. Assessment of (31)P relaxation times in the human calf muscle: a comparison between 3 T and 7 T in vivo. Magn. Reson. Med. 2009; 62(3): 574-582.
– reference: Hood DA. Plasticity in skeletal, cardiac, and smooth muscle - invited review: contractile activity-induced mitochondrial biogenesis in skeletal muscle. J. Appl. Physiol. 2001; 90(3): 1137-1157.
– reference: Taylor DJ. Clinical utility of muscle MR spectroscopy. Semin. Musculoskeletal Radiol. 2000; 4(4): 481-502.
– reference: Bottomley PA, Ouwerkerk R, Lee RF, Weiss RG. Four-angle saturation transfer (FAST) method for measuring creatine kinase reaction rates in vivo. Magn. Reson. Med. 2002; 47(5): 850-863.
– reference: Greenman RL, Smithline HA. The feasibility of measuring phosphocreatine recovery kinetics in muscle using a single-shot (31)P RARE MRI sequence. Acad. Radiol. 2011; 18(7): 917-923.
– reference: Parasoglou P, Xia D, Chang G, Regatte RR. Dynamic imaging of phosphocreatine recovery kinetics in the human lower leg muscles at 3T and 7T: a preliminary study. NMR Biomed. 2013; 26(3): 348-356.
– reference: Kupce E, Freeman R. Adiabatic pulses for wide-band inversion and broad-band decoupling. J. Magn. Reson. Ser. A 1995; 115(2): 273-276.
– reference: Bogner W, Chmelik M, Andronesi OC, Sorensen AG, Trattnig S, Gruber S. In vivo (31)P spectroscopy by fully adiabatic extended image selected in vivo spectroscopy: a comparison between 3 T and 7 T. Magn. Reson. Med. 2011; 66(4): 923-930.
– reference: Kemp GJ, Meyerspeer M, Moser E. Absolute quantification of phosphorus metabolite concentrations in human muscle in vivo by P-31 MRS: a quantitative review. NMR Biomed. 2007; 20(6): 555-565.
– reference: Radda GK. The use of NMR spectroscopy for the understanding of disease. Science 1986; 233(4764): 640-645.
– reference: Yarnykh VL. Actual flip-angle imaging in the pulsed steady state: a method for rapid three-dimensional mapping of the transmitted radiofrequency field. Magn. Reson. Med. 2007; 57(1): 192-200.
– reference: Befroy DE, Shulman GI. Magnetic resonance spectroscopy studies of human metabolism. Diabetes 2011; 60(5): 1361-1369.
– reference: Prompers JJ, Jeneson JAL, Drost MR, Oomens CCW, Strijkers GJ, Nicolay K. Dynamic MRS and MRI of skeletal muscle function and biomechanics. NMR Biomed. 2006; 19(7): 927-953.
– reference: Duncan BB, Schmidt MI, Pankow JS, Ballantyne CM, Couper D, Vigo A, Hoogeveen R, Folsom AR, Heiss G. Low-grade systemic inflammation and the development of type 2 diabetes - the Atherosclerosis Risk in Communities Study. Diabetes 2003; 52(7): 1799-1805.
– reference: Kholmovski EG, Parker DL, Alexander AL. A generalized k-sampling scheme for 3D fast spin echo. J. Magn. Reson. Imaging 2000; 11(5): 549-558.
– reference: Sun PZ, Benner T, Kumar A, Sorensen AG. Investigation of optimizing and translating pH-sensitive pulsed-chemical exchange saturation transfer (CEST) imaging to a 3T clinical scanner. Magn. Reson. Med. 2008; 60(4): 834-841.
– reference: Parry A, Matthews PM. Roles for imaging in understanding the pathophysiology, clinical evaluation, and management of patients with mitochondrial disease. J. Neuroimaging 2003; 13(4): 293-302.
– reference: Forsen S, Hoffman RA. Study of moderately rapid chemical exchange reactions by means of nuclear magnetic double resonance. J. Chem. Phys. 1963; 39(11): 2892-2901.
– reference: Chao H, Bowers JL, Holtzman D, Mulkern RV. Multi-echo 31P spectroscopic imaging of ATP: a scan time reduction strategy. J. Magn. Reson. Imaging 1997; 7(2): 425-433.
– reference: Alger JR, Shulman RG. NMR-studies of enzymatic rates in vitro and in vivo by magnetization transfer. Q. Rev. Biophys. 1984; 17(1): 83-124.
– reference: Jennings RB, Reimer KA. Lethal myocardial ischemic-injury. Am. J. Pathol. 1981; 102(2): 241-255.
– reference: Parasoglou P, Feng L, Xia D, Otazo R, Regatte RR. Rapid 3D-imaging of phosphocreatine recovery kinetics in the human lower leg muscles with compressed sensing. Magn. Reson. Med. 2012; 68(6): 1738-1746.
– reference: Hands LJ, Bore PJ, Galloway G, Morris PJ, Radda GK. Muscle metabolism in patients with peripheral vascular-disease investigated by 31P nuclear-magnetic resonance spectroscopy. Clin. Sci. 1986; 71(3): 283-290.
– reference: Greenman RL. Quantification of the P-31 metabolite concentration in human skeletal muscle from RARE image intensity. Magn. Reson. Med. 2004; 52(5): 1036-1042.
– reference: Greenman RL, Axel L, Ferrari VA, Lenkinski RE. Fast imaging of phosphocreatine in the normal human myocardium using a three-dimensional RARE pulse sequence at 4 tesla. J. Magn. Reson. Imaging 2002; 15(4): 467-472.
– reference: Hetherington HP, Spencer DD, Vaughan JT, Pan JW. Quantitative P-31 spectroscopic imaging of human brain at 4 tesla: assessment of gray and white matter differences of phosphocreatine and ATP. Magn. Reson. Med. 2001; 45(1): 46-52.
– reference: Marjanska M, Eberly LE, Adriany G, Verdoliva SN, Garwood M, Chow L. Influence of foot orientation on the appearance and quantification of (1) H magnetic resonance muscle spectra obtained from the soleus and the vastus lateralis. Magn. Reson. Med. 2012; 68(6): 1731-1737.
– reference: Degani H, Laughlin M, Campbell S, Shulman RG. Kinetics of creatine kinase in heart - a P31 saturation-transfer and inversion-transfer study. Biochemistry 1985; 24(20): 5510-5516.
– reference: Lu A, Atkinson IC, Zhou XJ, Thulborn KR. PCr/ATP ratio mapping of the human head by simultaneously imaging of multiple spectral peaks with interleaved excitations and flexible twisted projection imaging readout trajectories at 9.4 T. Magn. Reson. Med. 2012. DOI: 10.1002/mrm.24281
– reference: Kemp GJ, Radda GK. Quantitative interpretation of bioenergetic data from 31P and 1H magnetic resonance spectroscopic studies of skeletal muscle. Magn. Reson. Q. 1994; 10(1): 43-63.
– reference: Lanza IR, Larsen RG, Kent-Braun JA. Effects of old age on human skeletal muscle energetics during fatiguing contractions with and without blood flow. J. Physiol. (Lond.) 2007; 583(3): 1093-1105.
– volume: 63
  start-page: 1493
  issue: 6
  year: 2010
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Snippet Phosphorus (31P) magnetization transfer (MT) techniques enable the non‐invasive measurement of metabolic turnover rates of important enzyme‐catalyzed...
Phosphorus ( 31 P) magnetization transfer (MT) techniques enable the non‐invasive measurement of metabolic turnover rates of important enzyme‐catalyzed...
Phosphorus ((31) P) magnetization transfer (MT) techniques enable the non-invasive measurement of metabolic turnover rates of important enzyme-catalyzed...
Phosphorus (31P) magnetization transfer (MT) techniques enable the non-invasive measurement of metabolic turnover rates of important enzyme-catalyzed...
Phosphorus ( super(31)P) magnetization transfer (MT) techniques enable the non-invasive measurement of metabolic turnover rates of important enzyme-catalyzed...
Phosphorous (31P) magnetization transfer (MT) techniques enable the non-invasive measurement of metabolic turnover rates of important enzyme catalyzed...
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StartPage 1142
SubjectTerms Adult
ATP
Computer Simulation
creatine kinase
Creatine Kinase - metabolism
Diabetes Mellitus, Type 2 - enzymology
Diabetes Mellitus, Type 2 - metabolism
Energy Metabolism
Female
Humans
Imaging, Three-Dimensional
Kinetics
Leg
Magnetic Resonance Spectroscopy
magnetization transfer
Male
Metabolic Flux Analysis
muscle metabolism
Muscle, Skeletal - enzymology
Phosphorus - metabolism
phosphorus MRI
Spin Labels
Title Three-dimensional mapping of the creatine kinase enzyme reaction rate in muscles of the lower leg
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https://onlinelibrary.wiley.com/doi/abs/10.1002%2Fnbm.2928
https://www.ncbi.nlm.nih.gov/pubmed/23436474
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https://www.proquest.com/docview/1424325782
https://www.proquest.com/docview/1492613687
https://pubmed.ncbi.nlm.nih.gov/PMC3744626
Volume 26
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