Effect of ischemic preconditioning in skeletal muscle measured by functional magnetic resonance imaging and spectroscopy: A randomized crossover trial

Journal of Cardiovascular Magnetic Resonance

Volumn 13, Issue 1, 2011, Pages

  Andreas, Martin ^a   Schmid, Albrecht I ^a,b   Keilani, Mohammad ^a   Doberer, Daniel ^a   Bartko, Johann ^a   Crevenna, Richard ^a   Moser, Ewald ^a,b   Wolzt, Michael ^a  

^a MEDICAL UNIVERSITY OF VIENNA   (Austria)

^b Christian Doppler Laboratory for Innovative Optical Imaging and its Translation to Medicine   (Austria)

Author keywords

[No Author keywords available]

Indexed keywords

ADENOSINE TRIPHOSPHATE; CREATINE PHOSPHATE; LACTATE DEHYDROGENASE; OXYGEN;

ADULT; AEROBIC METABOLISM; ARTICLE; BLOOD SAMPLING; CLINICAL PROTOCOL; CONTROLLED STUDY; CROSSOVER PROCEDURE; DYNAMOMETER; FUNCTIONAL MAGNETIC RESONANCE IMAGING; HUMAN; HUMAN EXPERIMENT; ISCHEMIC PRECONDITIONING; ISOMETRIC EXERCISE; LIMB ISCHEMIA; MALE; MITOCHONDRION; MUSCLE FORCE; MUSCLE METABOLISM; MUSCLE STRENGTH; NORMAL HUMAN; NUCLEAR MAGNETIC RESONANCE SPECTROSCOPY; OXYGEN CONSUMPTION; PHOSPHORUS NUCLEAR MAGNETIC RESONANCE; PRIORITY JOURNAL; RANDOMIZED CONTROLLED TRIAL; REPERFUSION; SKELETAL MUSCLE; WHOLE BODY SCANNER; AUSTRIA; BLOOD; BLOOD FLOW; CLINICAL TRIAL; CONTROLLED CLINICAL TRIAL; METABOLISM; METHODOLOGY; MUSCLE ISOMETRIC CONTRACTION; NUCLEAR MAGNETIC RESONANCE IMAGING; PATHOLOGY; PATHOPHYSIOLOGY; REPERFUSION INJURY; TIME; VASCULARIZATION;

ADULT; AUSTRIA; CROSS-OVER STUDIES; HUMANS; ISCHEMIC PRECONDITIONING; ISOMETRIC CONTRACTION; MAGNETIC RESONANCE IMAGING; MAGNETIC RESONANCE SPECTROSCOPY; MALE; MUSCLE STRENGTH; MUSCLE, SKELETAL; OXYGEN; OXYGEN CONSUMPTION; PHOSPHOCREATINE; REGIONAL BLOOD FLOW; REPERFUSION INJURY; TIME FACTORS; YOUNG ADULT;

EID: 80053521440     PISSN: 10976647     EISSN: 1532429X     Source Type: Journal    
DOI: 10.1186/1532-429X-13-32     Document Type: Article

References (44)

1. Progression of myocardial necrosis during reperfusion of ischemic myocardium. Matsumura K, Jeremy RW, Schaper J, Becker LC, Circulation 1998 97 8 795 804 9498544 (Pubitemid 28135343)
2. Role of apoptosis in reperfusion injury. Eefting F, Rensing B, Wigman J, Pannekoek WJ, Liu WM, Cramer MJ, Lips DJ, Doevendans PA, Cardiovasc Res 2004 61 3 414 426 10.1016/j.cardiores.2003.12.023 14962473 (Pubitemid 38210148)
3. Preconditioning with ischemia: a delay of lethal cell injury in ischemic myocardium. Murry CE, Jennings RB, Reimer KA, Circulation 1986 74 5 1124 1136 10.1161/01.CIR.74.5.1124 3769170 (Pubitemid 17174962)
4. Ischemic preconditioning prevents endothelial injury and systemic neutrophil activation during ischemia-reperfusion in humans in vivo. Kharbanda RK, Peters M, Walton B, Kattenhorn M, Mullen M, Klein N, Vallance P, Deanfield J, MacAllister R, Circulation 2001 103 12 1624 1630 11273988 (Pubitemid 32246608)
5. Effect of remote ischaemic preconditioning on myocardial injury in patients undergoing coronary artery bypass graft surgery: a randomised controlled trial. Hausenloy DJ, Mwamure PK, Venugopal V, Harris J, Barnard M, Grundy E, Ashley E, Vichare S, Di Salvo C, Kolvekar S, et al. Lancet 2007 370 9587 575 579 10.1016/S0140-6736(07)61296-3 17707752 (Pubitemid 47247853)
6. Randomized controlled trial of the effects of remote ischemic preconditioning on children undergoing cardiac surgery: first clinical application in humans. Cheung MM, Kharbanda RK, Konstantinov IE, Shimizu M, Frndova H, Li J, Holtby HM, Cox PN, Smallhorn JF, Van Arsdell GS, et al. J Am Coll Cardiol 2006 47 11 2277 2282 10.1016/j.jacc.2006.01.066 16750696 (Pubitemid 43795071)
7. Remote ischemic preconditioning provides early and late protection against endothelial ischemia-reperfusion injury in humans: role of the autonomic nervous system. Loukogeorgakis SP, Panagiotidou AT, Broadhead MW, Donald A, Deanfield JE, MacAllister RJ, J Am Coll Cardiol 2005 46 3 450 456 10.1016/j.jacc.2005.04.044 16053957 (Pubitemid 41040285)
8. Cardiac stress protein elevation 24 hours after brief ischemia or heat stress is associated with resistance to myocardial infarction. Marber MS, Latchman DS, Walker JM, Yellon DM, Circulation 1993 88 3 1264 1272 8353888 (Pubitemid 23264047)
9. Transient limb ischemia induces remote ischemic preconditioning in vivo. Kharbanda RK, Mortensen UM, White PA, Kristiansen SB, Schmidt MR, Hoschtitzky JA, Vogel M, Sorensen K, Redington AN, MacAllister R, Circulation 2002 106 23 2881 2883 10.1161/01.CIR.0000043806.51912.9B 12460865 (Pubitemid 35424735)
10. Direct noninvasive quantification of lactate and high energy phosphates simultaneously in exercising human skeletal muscle by localized magnetic resonance spectroscopy. Meyerspeer M, Kemp GJ, Mlynarik V, Krssak M, Szendroedi J, Nowotny P, Roden M, Moser E, Magn Reson Med 2007 57 4 654 660 10.1002/mrm.21188 17390348 (Pubitemid 46731790)
11. Muscle [phosphocreatine] dynamics following the onset of exercise in humans: the influence of baseline work-rate. Jones AM, Wilkerson DP, Fulford J, J Physiol 2008 586 3 889 898 18063663 (Pubitemid 351194125)
12. Absolute quantification of phosphorus metabolite concentrations in human muscle in vivo by 31P MRS: a quantitative review. Kemp GJ, Meyerspeer M, Moser E, NMR Biomed 2007 20 6 555 565 10.1002/nbm.1192 17628042 (Pubitemid 47496897)
13. 31P MRS measurement of mitochondrial function in skeletal muscle: reliability, force-level sensitivity and relation to whole body maximal oxygen uptake. Larson-Meyer DE, Newcomer BR, Hunter GR, Hetherington HP, Weinsier RL, NMR Biomed 2000 13 1 14 27 10.1002/(SICI)1099-1492(200002)13:1<14::AID- NBM605>3.0.CO;2-0 10668050 (Pubitemid 30136998)
14. Linear dependence of muscle phosphocreatine kinetics on oxidative capacity. Paganini AT, Foley JM, Meyer RA, Am J Physiol 1997 272 2 Pt 1 501 510 9124293
15. Assessment of regional myocardial oxygenation changes in the presence of coronary artery stenosis with balanced SSFP imaging at 3.0 T: theory and experimental evaluation in canines. Dharmakumar R, Arumana JM, Tang R, Harris K, Zhang Z, Li D, J Magn Reson Imaging 2008 27 5 1037 1045 10.1002/jmri.21345 18425840 (Pubitemid 351614614)
16. Blood oxygenation level-dependent magnetic resonance imaging of the skeletal muscle in patients with peripheral arterial occlusive disease. Ledermann HP, Schulte AC, Heidecker HG, Aschwanden M, Jager KA, Scheffler K, Steinbrich W, Bilecen D, Circulation 2006 113 25 2929 2935 10.1161/ CIRCULATIONAHA.105.605717 16785340 (Pubitemid 44297234)
17. Effects of percutaneous transluminal angioplasty on muscle BOLD-MRI in patients with peripheral arterial occlusive disease: preliminary results. Huegli RW, Schulte AC, Aschwanden M, Thalhammer C, Kos S, Jacob AL, Bilecen D, Eur Radiol 2009 19 2 509 515 10.1007/s00330-008-1168-6 18795296
18. Oxygenation dependence of the transverse relaxation time of water protons in whole blood at high field. Thulborn KR, Waterton JC, Matthews PM, Radda GK, Biochim Biophys Acta 1982 714 2 265 270 6275909 (Pubitemid 12134309)
19. Brain magnetic resonance imaging with contrast dependent on blood oxygenation. Ogawa S, Lee TM, Kay AR, Tank DW, Proc Natl Acad Sci USA 1990 87 24 9868 9872 10.1073/pnas.87.24.9868 2124706 (Pubitemid 120016545)
20. Dynamic interleaved 1H/31P STEAM MRS at 3 Tesla using a pneumatic force-controlled plantar flexion exercise rig. Meyerspeer M, Krssak M, Kemp GJ, Roden M, Moser E, Magma 2005 18 5 257 262 10.1007/s10334-005-0014-y 16320091 (Pubitemid 41738413)
21. Improved method for accurate and efficient quantification of MRS data with use of prior knowledge. Vanhamme L, van den Boogaart A, Van Huffel S, J Magn Reson 1997 129 1 35 43 10.1006/jmre.1997.1244 9405214 (Pubitemid 127454051)
22. Java-based graphical user interface for the MRUI quantitation package. Naressi A, Couturier C, Devos JM, Janssen M, Mangeat C, de Beer R, Graveron-Demilly D, Magma 2001 12 2-3 141 152 10.1007/BF02668096 11390270 (Pubitemid 32510133)
23. PDL: The Perl Data Language. Glazebrook K, E F, The Perl Journal 1997 5 5
24. Reliability and validity of the Biodex system 3 pro isokinetic dynamometer velocity, torque and position measurements. Drouin JM, Valovich-mcLeod TC, Shultz SJ, Gansneder BM, Perrin DH, Eur J Appl Physiol 2004 91 1 22 29 10.1007/s00421-003-0933-0 14508689 (Pubitemid 38292346)
25. Reproducibility of an Isokinetic Strength-Testing Protocol of the Knee and Ankle in Older Adults. Hartmann A, Knols R, Murer K, de Bruin ED, Gerontology 2008
26. Relation between foot arch index and ankle strength in elite gymnasts: a preliminary study. Aydog ST, Ozcakar L, Tetik O, Demirel HA, Hascelik Z, Doral MN, Br J Sports Med 2005 39 3 13 10.1136/bjsm.2004.011627 15728681
27. Preconditioning improves energy metabolism during reperfusion but does not attenuate myocardial stunning in porcine hearts. Miyamae M, Fujiwara H, Kida M, Yokota R, Tanaka M, Katsuragawa M, Hasegawa K, Ohura M, Koga K, Yabuuchi Y, et al. Circulation 1993 88 1 223 234 8319337 (Pubitemid 23195453)
28. Mechanisms underlying acute protection from cardiac ischemia-reperfusion injury. Murphy E, Steenbergen C, Physiol Rev 2008 88 2 581 609 10.1152/physrev.00024.2007 18391174 (Pubitemid 351520088)
29. A hierarchy of ATP-consuming processes in mammalian cells. Buttgereit F, Brand MD, Biochem J 1995 312 Pt 1 163 167 7492307
30. Phosphocreatine recovery overshoot after high intensity exercise in human skeletal muscle is associated with extensive muscle acidification and a significant decrease in phosphorylation potential. Zoladz JA, Korzeniewski B, Kulinowski P, Zapart-Bukowska J, Majerczak J, Jasinski A, J Physiol Sci 60 5 331 341
31. Some factors determining the PCr recovery overshoot in skeletal muscle. Korzeniewski B, Zoladz JA, Biophys Chem 2005 116 2 129 136 10.1016/j.bpc.2005. 03.004 15950825 (Pubitemid 40799382)
32. Simultaneous measurement of perfusion and oxygenation changes using a multiple gradient-echo sequence: application to human muscle study. Lebon V, Carlier PG, Brillault-Salvat C, Leroy-Willig A, Magn Reson Imaging 1998 16 7 721 729 10.1016/S0730-725X(98)00088-5 9811138 (Pubitemid 28496569)
33. Perfusion changes in human skeletal muscle during reactive hyperemia measured by echo-planar imaging. Toussaint JF, Kwong KK, Mkparu FO, Weisskoff RM, LaRaia PJ, Kantor HL, Magn Reson Med 1996 35 1 62 69 10.1002/mrm.1910350109 8771023 (Pubitemid 26017920)
34. Influence of vascular filling and perfusion on BOLD contrast during reactive hyperemia in human skeletal muscle. Duteil S, Wary C, Raynaud JS, Lebon V, Lesage D, Leroy-Willig A, Carlier PG, Magn Reson Med 2006 55 2 450 454 10.1002/mrm.20760 16342333 (Pubitemid 43238115)
35. BOLD magnetic resonance imaging of skeletal muscle. Noseworthy MD, Bulte DP, Alfonsi J, Semin Musculoskelet Radiol 2003 7 4 307 315 14735429 (Pubitemid 38056267)
36. Evidence of muscle BOLD effect revealed by simultaneous interleaved gradient-echo NMRI and myoglobin NMRS during leg ischemia. Lebon V, Brillault-Salvat C, Bloch G, Leroy-Willig A, Carlier PG, Magn Reson Med 1998 40 4 551 558 10.1002/mrm.1910400408 9771572 (Pubitemid 28440023)
37. Simultaneous gradient-echo/spin-echo EPI of graded ischemia in human skeletal muscle. Donahue KM, Van Kylen J, Guven S, El-Bershawi A, Luh WM, Bandettini PA, Cox RW, Hyde JS, Kissebah AH, J Magn Reson Imaging 1998 8 5 1106 1113 10.1002/jmri.1880080516 9786149 (Pubitemid 28481797)
38. Calf muscles at blood oxygen level-dependent MR imaging: aging effects at postocclusive reactive hyperemia. Schulte AC, Aschwanden M, Bilecen D, Radiology 2008 247 2 482 489 10.1148/radiol.2472070828 18372453
39. Human soleus muscle: a comparison of fiber composition and enzyme activities with other leg muscles. Gollnick PD, Sjodin B, Karlsson J, Jansson E, Saltin B, Pflugers Arch 1974 348 3 247 255 10.1007/BF00587415 4275915
40. Transient limb ischemia induces remote preconditioning and remote postconditioning in humans by a K(ATP)-channel dependent mechanism. Loukogeorgakis SP, Williams R, Panagiotidou AT, Kolvekar SK, Donald A, Cole TJ, Yellon DM, Deanfield JE, MacAllister RJ, Circulation 2007 116 12 1386 1395 10.1161/CIRCULATIONAHA.106.653782 17724264 (Pubitemid 47417565)
41. Role of creatine kinase isoenzymes on muscular and cardiorespiratory endurance: genetic and molecular evidence. Echegaray M, Rivera MA, Sports Med 2001 31 13 919 934 10.2165/00007256-200131130-00003 11708401
42. Direct evidence that initial oxidative stress triggered by preconditioning contributes to second window of protection by endogenous antioxidant enzyme in myocytes. Zhou X, Zhai X, Ashraf M, Circulation 1996 93 6 1177 1184 8653839 (Pubitemid 26087021)
43. Control of glycolysis in contracting skeletal muscle. II. Turning it off. Crowther GJ, Kemper WF, Carey MF, Conley KE, Am J Physiol Endocrinol Metab 2002 282 1 74 79 11739086
44. In vivo ATP production during free-flow and ischaemic muscle contractions in humans. Lanza IR, Wigmore DM, Befroy DE, Kent-Braun JA, J Physiol 2006 577 Pt 1 353 367 16945975 (Pubitemid 44698261)