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Semin Musculoskelet Radiol 2000; 4(4): 481-502
DOI: 10.1055/s-2000-13172
Copyright © 2000 by Thieme Medical Publishers, Inc., 333 Seventh Avenue, New York, NY 10001, USA. Tel.: +1(212) 584-4662

Clinical Utility of Muscle MR Spectroscopy

D. J. Taylor
  • Medical Research Council Scientist, MRC Biochemical and Clinical Magnetic Resonance Unit, John Radcliffe Hospital, Oxford, and Department of Biochemistry, University of Oxford, Oxford, UK
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Publication History

Publication Date:
31 December 2000 (online)

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ABSTRACT

31Phosphorus (31P) magnetic resonance spectroscopy (MRS) is well suited for gathering data on skeletal muscle energetics in vivo. The technique has evolved to the point where it has become an important tool in the study of the pathophysiology both of rare primary disorders of muscle such as the mitochondrial myopathies and of more common systemic diseases such as renal failure, which also influence muscle metabolism. 31P-MRS is used for providing information about the biochemical composition of tissue without invasive sampling, and it has the unique ability to measure intracellular pH. In some conditions it can be used as an aid to diagnosis. Because MRS is well tolerated and examinations are easily repeated, the technique can also be employed in longitudinal studies of disease progression or the effects of treatment. Magnetic resonance spectroscopy is being increasingly used in conjunction with other noninvasive technologies to investigate effects of gene function on metabolism.

KEYWORD

31Phosphorus magnetic resonance spectroscopy - myopathy - exercise - myalgia - muscles

REFERENCES

  • 1 Andrew E R, Bydder G, Griffiths J, Iles R, Styles P. Clinical Magnetic Resonance: Imaging and Spectroscopy.  Chichester: John Wiley and Sons; 1990
    Google Scholar
  • 2 Taylor D J, Kemp G J, Thompson C H, Radda G K. Ageing: effects on oxidative function of skeletal muscle in vivo.  Mol Cell Biochem . 1997;  174 321-324
    CrossrefPubMedGoogle Scholar
  • 3 Tarnopolsky M A, Parise G. Direct measurement of high-energy phosphate compounds in patients with neuromuscular disease.  Muscle Nerve . 1999;  22 1228-1233
    PubMedGoogle Scholar
  • 4 Arnold D L, Taylor D J, Radda G K. Investigation of human mitochondrial myopathies by phosphorus magnetic resonance spectroscopy.  Ann Neurol . 1985;  18 189-196
    CrossrefPubMedGoogle Scholar
  • 5 Gupta R K, Gupta P, Yushok W D, Rose Z B. On the noninvasive measurement of intracellular free magnesium by 31P NMR spectroscopy.  Physiol Chem Phys Med NMR . 1983;  15 265-280
    PubMedGoogle Scholar
  • 6 Lodi R, Montagna P, Soriani S. Deficit of brain and skeletal muscle bioenergetics and low brain magnesium in juvenile migraine: an in vivo 31P magnetic resonance spectroscopy interictal study.  Pediatr Res . 1997;  42 866-871
    PubMedGoogle Scholar
  • 7 Ward K M, Rajan S S, Wysong M, Radulovic D, Clauw D J. Phosphorus nuclear magnetic resonance spectroscopy: in vivo magnesium measurements in the skeletal muscle of normal subjects.  Magn Reson Med . 1996;  36 475-480
    PubMedGoogle Scholar
  • 8 Kemp G J, Radda G K. Quantitative interpretation of bioenergetic data from 31P and 1H magnetic resonance spectroscopic studies of skeletal muscle: an analytical review.  Magn Reson Q . 1994;  10 43-63
    PubMedGoogle Scholar
  • 9 Chance B, Bank W. Genetic disease of mitochondrial function evaluated by NMR and NIR spectroscopy of skeletal tissue.  Biochim Biophys Acta . 1995;  1271 7-14
    PubMedGoogle Scholar
  • 10 McCully K K, Iotti S, Kendrick K. Simultaneous in vivo measurements of HbO2 saturation and PCr kinetics after exercise in normal humans.  J Appl Physiol . 1994;  77 5-10
    PubMedGoogle Scholar
  • 11 Bendahan D, Badier M, Jammes Y. Metabolic and myoelectrical effects of acute hypoxaemia during isometric contraction of forearm muscles in humans: a combined 31P-magnetic resonance spectroscopy-surface electromyogram (MRS-SEMG) study.  Clin Sci (Colch) . 1998;  94 279-286
    PubMedGoogle Scholar
  • 12 Bendahan D, Jammes Y, Salvan A M. Combined electromyography-31P-magnetic resonance spectroscopy study of human muscle fatigue during static contraction.  Muscle Nerve . 1996;  19 715-721
    PubMedGoogle Scholar
  • 13 Vestergaard-Poulsen P, Thomsen C, Sinkjaer T, Henriksen O. Simultaneous 31P NMR spectroscopy and EMG in exercising and recovering human skeletal muscle: technical aspects.  Magn Reson Med . 1994;  31 93-102
    PubMedGoogle Scholar
  • 14 Morvan D, Jehenson P, Duboc D, Syrota A. Discriminant factor analysis of 31P NMR spectroscopic data in myopathies.  Magn Reson Med . 1990;  13 216-227
    PubMedGoogle Scholar
  • 15 Taylor D J, Bore P J, Styles P, Gadian D G, Radda G K. Bioenergetics of intact human muscle. A 31P nuclear magnetic resonance study.  Mol Biol Med . 1983;  1 77-94
    PubMedGoogle Scholar
  • 16 Argov Z, Bank W J, Maris J, Peterson P, Chance B. Bioenergetic heterogeneity of human mitochondrial myopathies: phosphorus magnetic resonance spectroscopy study.  Neurology . 1987;  37 257-262
    PubMedGoogle Scholar
  • 17 Taylor D J, Kemp G J, Radda G K. Bioenergetics of skeletal muscle in mitochondrial myopathy.  J Neurol Sci . 1994;  127 198-206
    CrossrefPubMedGoogle Scholar
  • 18 Arnold D L, Matthews P M, Radda G K. Metabolic recovery after exercise and the assessment of mitochondrial function in vivo in human skeletal muscle by means of 31P NMR.  Magn Reson Med . 1984;  1 307-315
    CrossrefPubMedGoogle Scholar
  • 19 Bendahan D, Confort-Gouny S, Kozak-Reiss G, Cozzone P J. Heterogeneity of metabolic response to muscular exercise in humans. New criteria of invariance defined by in vivo phosphorus-31 NMR spectroscopy.  FEBS Lett . 1990;  272 155-158
    CrossrefPubMedGoogle Scholar
  • 20 Iotti S, Lodi R, Frassineti C, Zaniol P, Barbiroli B. In vivo assessment of mitochondrial functionality in human gastrocnemius muscle by 31P MRS. The role of pH in the evaluation of phosphocreatine and inorganic phosphate recoveries from exercise.  NMR Biomed . 1993;  6 248-253
    PubMedGoogle Scholar
  • 21 Taylor D J, Styles P, Matthews P M. Energetics of human muscle: exercise-induced ATP depletion.  Magn Reson Med . 1986;  3 44-54
    PubMedGoogle Scholar
  • 22 Park J H, Brown R L, Park C R. Functional pools of oxidative and glycolytic fibers in human muscle observed by 31P magnetic resonance spectroscopy during exercise.  Proc Natl Acad Sci U S A. 1987b;  84 8976-8980
    CrossrefPubMedGoogle Scholar
  • 23 Vandenborne K, McCully K, Kakihira H. Metabolic heterogeneity in human calf muscle during maximal exercise.  Proc Natl Acad Sci U S A . 1991;  88 5714-5718
    PubMedGoogle Scholar
  • 24 Fleckenstein J L, Bertocci L A, Nunnally R L, Parkey R W, Peshock R M. Exercise-enhanced MR imaging of variations in forearm muscle anatomy and use: importance in MR spectroscopy.  Am J Roentgenol . 1989;  153 693-698
    PubMedGoogle Scholar
  • 25 McCully K K, Forciea M A, Hack L M. Muscle metabolism in older subjects using 31P magnetic resonance spectroscopy.  Can J Physiol Pharmacol . 1991;  69 576-580
    PubMedGoogle Scholar
  • 26 Guthrie B M, Frostick S P, Goodman J. Endurance-trained and untrained skeletal muscle bioenergetics observed with magnetic resonance spectroscopy.  Can J Appl Physiol . 1996;  21 251-263
    PubMedGoogle Scholar
  • 27 Kent-Braun J A, McCully K K, Chance B. Metabolic effects of training in humans: a 31P-MRS study.  J Appl Physiol . 1990;  69 1165-1170
    PubMedGoogle Scholar
  • 28 Zochodne D W, Thompson R T, Driedger A A. Metabolic changes in human muscle denervation: topical 31P NMR spectroscopy studies.  Magn Reson Med . 1988;  7 373-383
    PubMedGoogle Scholar
  • 29 Frostick S P, Taylor D J, Dolecki M J, Radda G K. Human muscle cell denervation: the results of a 31-phosphorus magnetic resonance spectroscopy study.  J Hand Surg . 1992;  17 33-45
    CrossrefPubMedGoogle Scholar
  • 30 McCully K K, Kent J A, Chance B. Application of 31P magnetic resonance spectroscopy to the study of athletic performance.  Sports Med . 1988;  5 312-321
    PubMedGoogle Scholar
  • 31 Gupta R K, Mittal R D, Agarwal K N, Agarwal D K. Muscular sufficiency, serum protein, enzymes and bioenergetic studies (31-phosphorus magnetic resonance spectroscopy) in chronic malnutrition.  Acta Paediatr . 1994;  83 327-331
    PubMedGoogle Scholar
  • 32 Lodi R, Taylor D J, Tabrizi S J. In vivo skeletal muscle mitochondrial function in Leber's hereditary optic neuropathy assessed by 31P magnetic resonance spectroscopy.  Ann Neurol . 1997;  42 573-579
    CrossrefPubMedGoogle Scholar
  • 33 Cortelli P, Montagna P, Avoni P. Leber's hereditary optic neuropathy: genetic, biochemical, and phosphorus magnetic resonance spectroscopy study in an Italian family.  Neurology . 1991;  41 1211-1215
    PubMedGoogle Scholar
  • 34 Barbiroli B, Montagna P, Cortelli P. Defective brain and muscle energy metabolism shown by in vivo 31P magnetic resonance spectroscopy in nonaffected carriers of 11778 mtDNA mutation.  Neurology . 1995;  45 1364-1369
    PubMedGoogle Scholar
  • 35 Carelli V, Ghelli A, Ratta M. Leber's hereditary optic neuropathy: biochemical effect of 11778/ND4 and 3460/ND1 mutations and correlation with the mitochondrial genotype.  Neurology . 1997;  48 1623-1632
    PubMedGoogle Scholar
  • 36 Cock H, Tabrizi S, Cooper J, Schapira A. The influence of nuclear background on the biochemical expression of 3460 Leber's hereditary optic neuropathy.  Ann Neurol . 1998;  44 187-193
    CrossrefPubMedGoogle Scholar
  • 37 Lodi R, Cooper J M, Bradley J L. Deficit of in vivo mitochondrial ATP production in patients with Friedreich ataxia.  Proc Nat Acad Sci U S A . 1999;  96 11492-11495
    PubMedGoogle Scholar
  • 38 Chinnery P, Taylor D J, Brown D T. Very low levels of the mt DNA A3243G mutation associated with mitochondrial dysfunction in vivo.  Annals Neurol . 2000;  47 381-384
    PubMedGoogle Scholar
  • 39 Matthews P M, Allaire C, Shoubridge E A. In vivo muscle magnetic resonance spectroscopy in the clinical investigation of mitochondrial disease.  Neurology . 1991;  41 114-120
    PubMedGoogle Scholar
  • 40 Eleff S, Kennaway N, Buist N. 31P NMR study of improvement in oxidative phosphorylation by vitamins K3 and C in a patient with a defect in electron transportb at complex III in skeletal muscle.  Proc Natl Acad Sci . 1984;  81 3529-3533
    PubMedGoogle Scholar
  • 41 Penn A M, Lee J W, Thuillier P. MELAS syndrome with mitochondrial tRNA(Leu)(UUR) mutation: correlation of clinical state, nerve conduction, and muscle 31P magnetic resonance spectroscopy during treatment with nicotinamide and riboflavin.  Neurology . 1992;  42 2147-2152
    PubMedGoogle Scholar
  • 42 Matthews P M, Ford B, Dandurand R J. Coenzyme Q10 with multiple vitamins is generally ineffective in treatment of mitochondrial disease.  Neurology . 1993;  43 884-890
    PubMedGoogle Scholar
  • 43 Bendahan D, Desnuelle C, Vanuxem D. 31P NMR spectroscopy and ergometer exercise test as evidence for muscle oxidative performance improvement with coenzyme Q in mitochondrial myopathies.  Neurology . 1992;  42 1203-1208
    PubMedGoogle Scholar
  • 44 Barbiroli B, Frassineti C, Martinelli P. Coenzyme Q10 improves mitochondrial respiration in patients with mitochondrial cytopathies. An in vivo study on brain and skeletal muscle by phosphorous magnetic resonance spectroscopy.  Cell Mol Biol . 1997;  43 741-749
    PubMedGoogle Scholar
  • 45 De Stefano N, Matthews P M, Ford B. Short-term dichloroacetate treatment improves indices of cerebral metabolism in patients with mitochondrial disorders.  Neurology . 1995;  45 1193-1198
    PubMedGoogle Scholar
  • 46 Taivassalo T, De Stefano N, Argov Z. Effects of aerobic training in patients with mitochondrial myopathies.  Neurology . 1998;  50 1055-1060
    PubMedGoogle Scholar
  • 47 Ross B D, Radda G K, Gadian D G. Examination of a case of suspected McArdle's syndrome by 31P nuclear magnetic resonance.  N Engl J Med . 1981;  304 1338-1342
    CrossrefPubMedGoogle Scholar
  • 48 Argov Z, Bank W J, Maris J, Chance B. Muscle energy metabolism in McArdle's syndrome by in vivo phosphorus magnetic resonance spectroscopy.  Neurology . 1987;  37 1720-1724
    PubMedGoogle Scholar
  • 49 Duboc D, Jehenson P, Tran-Dinh S. Phosphourus NMR spectroscopy study of muscular enzyme deficiencies involving glycogenolysis and glycolysis.  Neurology . 1987;  37 663-671
    PubMedGoogle Scholar
  • 50 Radda G K, Rajagopalan B, Taylor D J. Biochemistry in vivo: an appraisal of clinical magnetic resonance spectroscopy.  Magn Reson Q . 1989;  5 122-151
    PubMedGoogle Scholar
  • 51 Bendahan D, Confort-Gouny S, Kozak-Ribbens G, Cozzone P J. 31-P characterization of the metabolic anomalies associated with the lack of glycogen phosphorylase activity in human forearm muscle.  Biochem Biophys Res Comm . 1992;  185 16-21
    CrossrefPubMedGoogle Scholar
  • 52 Siciliano G, Rossi B, Martini A. Myophosphorylase deficiency affects muscle mitochondrial respiration as shown by 31P-MR spectroscopy in a case with associated multifocal encephalopathy.  J Neurol Sci . 1995;  128 84-91
    CrossrefPubMedGoogle Scholar
  • 53 De Stefano N, Argov Z, Matthews P M, Karpati G, Arnold D L. Impairment of muscle mitochondrial oxidative metabolism in McArdles's disease.  Muscle Nerve . 1996;  19 764-769
    CrossrefPubMedGoogle Scholar
  • 54 Chance B, Eleff S, Leigh J, Sokolov D, Sapega A. Mitochondrial regulation of phosphocreatine/inorganic phosphate ratios in exercising human muscle: A gated 31P NMR study.  Proc Natl Acad Sci . 1981;  78 6714-6718
    PubMedGoogle Scholar
  • 55 Edwards R HT, Dawson M J, Wilkie D R, Gordon R E, Shaw D. Clinical use of nuclear magnetic resonance in the investigation of myopathy.  Lancet . 1982;  1 725-731
    PubMedGoogle Scholar
  • 56 Argov Z, Bank W J, Maris J, Leigh Jr S J, Chance B. Muscle energy metabolism in human phosphofructokinase deficiency as recorded by 31P nuclear magnetic resonance spectroscopy.  Ann Neurol . 1987;  22 46-51
    CrossrefPubMedGoogle Scholar
  • 57 Grehl T, Muller K, Vorgerd M. Impaired aerobic glycolysis in muscle phosphofructokinase deficiency results in biphasic post-exercise phosphocreatine recovery in 31P magnetic resonance spectroscopy.  Neuromuscul Disord . 1998;  8 480-488
    PubMedGoogle Scholar
  • 58 Bertocci L A, Haller R G, Lewis S F. Muscle metabolism during lactate infusion in human phosphofructokinase deficiency.  J Appl Physiol . 1993;  74 1342-1347
    PubMedGoogle Scholar
  • 59 Lewis S F, Haller R G. Skeletal muscle disorders and associated factors that limit exercise performance.  Exerc Sport Sci Rev . 1989;  61 67-113
    PubMedGoogle Scholar
  • 60 Sivakumar K, Vasconcelos O, Goldfarb L, Dalakas M C. Late-onset muscle weakness in partial phosphofructokinase deficiency: a unique myopathy with vacuoles, abnormal mitochondria, and absence of the common exon 5/intron 5 junction point mutation.  Neurology . 1996;  46 1337-1342
    PubMedGoogle Scholar
  • 61 Massa R, Lodi R, Barbiroli B, Servidei S, Sancesario G, Manfredi G, Zaniol P, Bernardi G. Partial block of glycolysis in late-onset phosphofructokinase deficiency myopathy.  Acta Neuropathol . 1996;  91 322-329
    CrossrefPubMedGoogle Scholar
  • 62 Vora S, DiMauro S, Spear D, Harker D, Danon M. Characterization of the enzymatic defect in late-onset muscle phosphofructokinase deficiency. New subtype of glycogen storage disease type VII.  J Clin Invest . 1987;  80 1479-1485
    PubMedGoogle Scholar
  • 63 Argov Z, Bank W J, Boden B, Ro Y I, Chance B. Phosphorus magnetic resonance spectroscopy of partially blocked muscle glycolysis. An in vivo study of phosphoglycerate mutase deficiency.  Arch Neurol . 1987;  44 614-617
    PubMedGoogle Scholar
  • 64 Vita G, Toscano A, Bresolin N. Muscle phosphoglycerate mutase (PGAM) deficiency in the first Caucasian patient: biochemistry, muscle culture and 31P-MR spectroscopy.  J Neurol . 1994;  241 289-294
    PubMedGoogle Scholar
  • 65 Jensen K E, Jakobsen J, Thomsen C, Henriksen O. Improved energy kinetics following high protein diet in McArdle's syndrome. A 31P magnetic resonance spectroscopy study.  Acta Neurol Scand . 1990;  81 499-503
    PubMedGoogle Scholar
  • 66 Vorgerd M, Grehl T, Jager M. A placebo-controlled crossover trial of creatine therapy in myophosphorylase deficiency (McArdle's disease).  Archives Neurol . 2000;  57 956-963
    PubMedGoogle Scholar
  • 67 Barbiroli B, Funicello R, Iotti S. 31P-NMR spectroscopy of skeletal muscle in Becker dystrophy and DMD/BMD carriers. Altered rate of phosphate transport.  J Neurol Sci . 1992;  109 188-195
    CrossrefPubMedGoogle Scholar
  • 68 Edwards R H, Griffiths R D, Cady E B. Topical magnetic resonance for the study of muscle metabolism in human myopathy.  Clin Physiol . 1985;  5 93-109
    PubMedGoogle Scholar
  • 69 Kemp G J, Taylor D J, Dunn J F, Frostick S P, Radda G K. Cellular energetics of dystrophic muscle.  J Neurol Sci. 1993a;  116 201-206
    CrossrefPubMedGoogle Scholar
  • 70 Newman R J, Bore P J, Chan L. Nuclear magnetic resonance studies of forearm muscle in Duchenne dystrophy.  Br Med J . 1982;  284 1072-1074
    PubMedGoogle Scholar
  • 71 Younkin D P, Berman P, Sladky J. 31P NMR studies in Duchenne muscular dystrophy: age-related metabolic changes.  Neurology . 1987;  37 165-169
    PubMedGoogle Scholar
  • 72 Barnes P R, Kemp G J, Taylor D J, Radda G K. Skeletal muscle metabolism in myotonic dystrophy A 31P magnetic resonance spectroscopy study.  Brain . 1997;  120 1699-1711
    CrossrefPubMedGoogle Scholar
  • 73 Barbiroli B, McCully K K, Iotti S. Further impairment of muscle phosphate kinetics by lengthening exercise in DMD/BMD carriers. An in vivo 31P-NMR spectroscopy study.  J Neurol Sci . 1993;  119 65-73
    CrossrefPubMedGoogle Scholar
  • 74 Lodi R, Kemp G J, Muntoni F. Reduced cytosolic acidification during exercise suggests defective glycolytic activity in skeletal muscle of patients with Becker muscular dystrophy. An in vivo 31P magnetic resonance spectroscopy study.  Brain . 1999;  122 121-130
    CrossrefPubMedGoogle Scholar
  • 75 Lodi R, Muntoni F, Taylor J. Correlative MR imaging and 31P-MR spectroscopy study in sarcoglycan deficient limb girdle muscular dystrophy.  Neuromuscul Disord . 1997;  7 505-511
    PubMedGoogle Scholar
  • 76 Zochodne D W, Koopman W J, Witt N J. Forearm P-31 nuclear magnetic resonance spectroscopy studies in oculopharyngeal muscular dystrophy.  Can J Neurol Sci . 1992;  19 174-179
    PubMedGoogle Scholar
  • 77 Kemp G J, Taylor D J, Thompson C H, Hands L J, Rajagopalan B, Styles P, Radda G K. Quantitative analysis by 31P magnetic resonance spectroscopy of abnormal mitochondrial oxidation in skeletal muscle during recovery from exercise.  NMR Biomed. 1993b;  6 302-310
    CrossrefPubMedGoogle Scholar
  • 78 Letellier T, Malgat M, Mazat J P. Control of oxidative phosphorylation in rat muscle mitochondria: implications for mitochondrial myopathies.  Biochim Biophys Acta . 1993;  1141 58-64
    PubMedGoogle Scholar
  • 79 Pagliaro L. Gylcolysis revisited. News Physiol Sci .  1993;  8 219-223
    PubMedGoogle Scholar
  • 80 Taylor D J, Kemp G J, Woods C G, Edwards J H, Radda G K. Skeletal muscle bioenergetics in myotonic dystrophy.  J Neurol Sci . 1993;  116 193-200
    CrossrefPubMedGoogle Scholar
  • 81 Jansen G, Mahadevan M, Amemiya C. Characterization of the myotonic dystrophy region predicts multiple protein isoform-encoding mRNAs.  Nat Genet . 1992;  1 261-266
    PubMedGoogle Scholar
  • 82 Mahadevan M S, Amemiya C, Jansen G. Structure and genomic sequence of the myotonic dystrophy (DM kinase) gene.  Hum Mol Genet . 1993;  2 299-304
    PubMedGoogle Scholar
  • 83 Monsieurs K, Heytens L, Kloeck C. Slower recovery of muscle phosphocreatine in malignant hyperthermia-susceptible individuals assessed by 31P-MR spectroscopy.  J Neurol . 1997;  244 651-656
    PubMedGoogle Scholar
  • 84 Bendahan D, Kozak-Ribbens G, Rodet L, Confort-Gouny S, Cozzone P J. 31Phosphorus magnetic resonance spectroscopy characterization of muscular metabolic anomalies in patients with malignant hyperthermia: application to diagnosis.  Anesthesiology . 1998;  88 96-107
    CrossrefPubMedGoogle Scholar
  • 85 Webster D W, Thompson R T, Gravelle D R, Laschuk M J, Driedger A A. Metabolic response to exercise in malignant hyperthermia-sensitive patients measured by 31P magnetic resonance spectroscopy.  Magn Reson Med . 1990;  15 81-89
    PubMedGoogle Scholar
  • 86 Olgin J, Rosenberg H, Allen G, Seestedt R, Chance B. A blinded comparison of noninvasive, in vivo phosphorus nuclear magnetic resonance spectroscopy and the in vitro halothane/caffeine contracture test in the evaluation of malignant hyperthermia susceptibility.  Anesth Analg . 1991;  72 36-47
    PubMedGoogle Scholar
  • 87 Payen J F, Bosson J L, Bourdon L. Improved noninvasive diagnostic testing for malignant hyperthermia susceptibility from a combination of metabolites determined in vivo with 31P-magnetic resonance spectroscopy.  Anesthesiology . 1993;  78 848-855
    PubMedGoogle Scholar
  • 88 Payen J F, Fouilhe N, Sam-Lai E, Remy C, Dupeyre R, Mezin P, Halsall J, Stieglitz P. In vitro 31P-magnetic resonance spectroscopy of muscle extracts in malignant hyperthermia-susceptible patients.  Anesthesiology . 1996;  84 1077-1082
    PubMedGoogle Scholar
  • 89 Park J, Vital T, Ryder N. Magnetic resonance imaging and P-31 magnetic resonance spectroscopy provide unique quantitative data useful in the longitudinal management of patients with dermatomyositis.  Arthritis Rheum . 1994;  37 736-746
    PubMedGoogle Scholar
  • 90 Cea G, Bendahan D, Manners D. MRI and 31P MRS demonstrate abnormal muscle efficiency and mitochondrial function in inflammatory myopathies, 4th International Congress of the World Muscle Society. Antalya, Turkey, Neuromuscular Disorders, 1999 9: 475-476
    Google Scholar
  • 91 Park J H, Olsen N J, King Jr L. Use of magnetic resonance imaging and P-31 magnetic resonance spectroscopy to detect and quantify muscle dysfunction in the amyopathic and myopathic variants of dermatomyositis.  Arthritis Rheum . 1995;  38 68-77
    PubMedGoogle Scholar
  • 92 Park J H, Vansant J P, Kumar N G. Dermatomyositis: correlative MR imaging and P-31 MR spectroscopy for quantitative characterization of inflammatory disease.  Radiology . 1990;  177 473-479
    PubMedGoogle Scholar
  • 93 Emslie-Smith A M, Engel A G. Microvascular changes in early and advanced dermatomyositis: a quantitative study.  Ann Neurol . 1990;  27 343-356
    CrossrefPubMedGoogle Scholar
  • 94 Dalakas M C. Polymyositis, dermatomyositis, and inclusion-body myositis.  N Engl J Med . 1991;  325 1487-1498
    PubMedGoogle Scholar
  • 95 Griggs R C, Askanas V, DiMauro S. Inclusion body myositis and myopathies.  Ann Neurol . 1995;  38 705-713
    CrossrefPubMedGoogle Scholar
  • 96 Oldfors A, Larsson N G, Lindberg C, Holme E. Mitochondrial DNA deletions in inclusion body myositis.  Brain . 1993;  116 325-336
    PubMedGoogle Scholar
  • 97 Santorelli F M, Sciacco M, Tanji K. Multiple mitochondrial DNA deletions in sporadic inclusion body myositis: a study of 56 patients.  Ann Neurol . 1996;  39 789-795
    CrossrefPubMedGoogle Scholar
  • 98 Lodi R, Taylor D J, Tabrizi S J. Normal in vivo skeletal muscle oxidative metabolism in sporadic inclusion body myositis assessed by 31P-magnetic resonance spectroscopy.  Brain . 1998;  121 2119-2126
    CrossrefPubMedGoogle Scholar
  • 99 Argov Z, Taivassalo T, De Stefano N. Intracellular phosphates in inclusion body myositis-a 31P magnetic resonance spectroscopy study.  Muscle Nerve . 1998;  21 1523-1525
    PubMedGoogle Scholar
  • 100 Park J H, Kari S, King L E, Olsen N J. Analysis of 31P MR spectroscopy data using artificial neural networks for longitudinal evaluation of muscle diseases: dermatomyositis.  NMR Biomed . 1998;  11 245-256
    CrossrefPubMedGoogle Scholar
  • 101 Thompson C H, Kemp G J, Barnes P R. Uraemic muscle metabolism at rest and during exercise.  Nephrol Dial Transplant . 1994;  9 1600-1605
    PubMedGoogle Scholar
  • 102 Thompson C H, Irish A B, Kemp G J, Taylor D J, Radda G K. The effect of propionyl L-carnitine on skeletal muscle metabolism in renal failure.  Clin Nephrol . 1997;  47 372-378
    PubMedGoogle Scholar
  • 103 Thompson C H, Kemp G J, Taylor D J, Radda G K. Bioenergetic effects of erythropoietin in skeletal muscle.  Nephron . 1996;  74 239(letter)-240(letter)
    PubMedGoogle Scholar
  • 104 Thompson C H, Irish A, Kemp G J, Taylor D J, Radda G K. Skeletal muscle metabolism before and after gemfibrozil treatment in dialysed patients with chronic renal failure.  Clin Nephrol . 1996;  45 386-389
    PubMedGoogle Scholar
  • 105 Wilson J R, Fink L, Maris J. Evaluation of energy metabolism in skeletal muscle of patients with heart failure with gated phosphorus-31 nuclear magnetic resonance.  Circulation . 1985;  71 57-62
    PubMedGoogle Scholar
  • 106 Massie B, Conway M, Yonge R. Skeletal muscle metabolism in patients with congestive heart failure: relation to clinical severity and blood flow.  Circulation . 1987;  76 1009-1019
    PubMedGoogle Scholar
  • 107 Kemp G J, Thompson C H, Stratton J R. Abnormalities in exercising skeletal muscle in congestive heart failure can be explained in terms of decreased mitochondrial ATP synthesis, reduced metabolic efficiency, and increased glycogenolysis.  Heart . 1996;  76 35-41
    PubMedGoogle Scholar
  • 108 Toussaint J F, Kwong K K, M'Kparu F, Weisskoff R M, La Raia J P, Kantor H L. Interrelationship of oxidative metabolism and local perfusion demonstrated by NMR in human skeletal muscle.  J Appl Physiol . 1996;  81 2221-2228
    PubMedGoogle Scholar
  • 109 Toussaint J F, Koelling T M, Schmidt C J. Local relation between oxidative metabolism and perfusion in leg muscles of patients with heart failure studied by magnetic resonance imaging and spectroscopy.  J Heart Lung Transplant . 1998;  17 892-900
    PubMedGoogle Scholar
  • 110 Duboc D, Jehenson P, Tamby J F, Payen J F, Syrota A, Guerin F. [Abnormalities of the skeletal muscle in hypertrophic cardiomyopathy. Spectroscopy using phosphorus-31 nuclear magnetic resonance].  Arch Mal Coeur Vaiss . 1991;  84 185-188
    PubMedGoogle Scholar
  • 111 Thompson C H, Kemp G J, Taylor D J. Abnormal skeletal muscle bioenergetics in familial hypertrophic cardiomyopathy.  Heart . 1997;  78 177-181
    PubMedGoogle Scholar
  • 112 Minotti J R, Johnson E C, Hudson T L. Skeletal muscle response to exercise training in congestive heart failure.  J Clin Invest . 1990;  86 751-758
    PubMedGoogle Scholar
  • 113 Adamopoulos S, Coats A J, Brunotte F. Physical training improves skeletal muscle metabolism in patients with chronic heart failure.  J Am Coll Cardiol . 1993;  21 1101-1106
    CrossrefPubMedGoogle Scholar
  • 114 Maillefert J F, Eicher J C, Walker P. Effects of low-frequency electrical stimulation of quadriceps and calf muscles in patients with chronic heart failure.  J Cardiopulm Rehabil . 1998;  18 277-282
    PubMedGoogle Scholar
  • 115 Kemp G J, Hands L J, Ramaswami G. Calf muscle mitochondrial and glycogenolytic ATP synthesis in patients with claudication due to peripheral vascular disease analysed using 31P magnetic resonance spectroscopy.  Clin Sci . 1995;  89 581-590
    PubMedGoogle Scholar
  • 116 Taylor D J, Amato A, Hands L J. Changes in energy metabolism of calf muscle in patients with intermittent claudication assessed by 31P magnetic resonance spectroscopy: a phase II open study.  Vasc Med . 1996;  1 241-245
    PubMedGoogle Scholar
  • 117 Kutsuzawa T, Shioya S, Kurita D. Muscle energy metabolism and nutritional status in patients with chronic obstructive pulmonary disease. A 31P magnetic resonance study.  Am J Respir Crit Care Med . 1995;  152 647-652
    PubMedGoogle Scholar
  • 118 Thompson C H, Davies R J, Kemp G J. Skeletal muscle metabolism during exercise and recovery in patients with respiratory failure.  Thorax . 1993;  48 486-490
    PubMedGoogle Scholar
  • 119 Payen J F, Wuyam B, Reutenauer H. Impairment of muscular metabolism in chronic respiratory failure. A human 31P MRS study.  NMR Biomed . 1991;  4 41-45
    PubMedGoogle Scholar
  • 120 Wuyam B, Payen J F, Levy P. Metabolism and aerobic capacity of skeletal muscle in chronic respiratory failure related to chronic obstructive pulmonary disease.  Eur Respir J . 1992;  5 157-162
    PubMedGoogle Scholar
  • 121 Levy P, Wuyam B, Pepin J L, Reutenauer H, Payen J F. Skeletal muscle abnormalities in chronic obstructive lung disease with respiratory insufficiency. Value of P31 magnetic resonance spectroscopy.  Rev Mal Respir . 1997;  14 183-191
    PubMedGoogle Scholar
  • 122 Taylor D J, Rajagopalan B, Radda G K. Cellular energetics in hypothyroid muscle.  Eur J Clin Invest . 1992;  22 358-365
    PubMedGoogle Scholar
  • 123 Kaminsky P, Robin-Lherbier B, Brunotte F. Energetic metabolism in hypothyroid skeletal muscle, as studied by phosphorus magnetic resonance spectroscopy.  J Clin Endocrinol Metab . 1992;  74 124-129
    CrossrefPubMedGoogle Scholar
  • 124 Argov Z, Renshaw P F, Boden B, Winokur A, Bank W J. Effects of thyroid hormones on skeletal muscle bioenergetics. In vivo phosphorus-31 magnetic resonance spectroscopy study of humans and rats.  J Clin Invest . 1988;  81 1695-1701
    PubMedGoogle Scholar
  • 125 Erkintalo M, Bendahan D, Mattei J P. Reduced metabolic efficiency of skeletal muscle energetics in hyperthyroid patients evidenced quantitatively by in vivo phosphorus-31 magnetic resonance spectroscopy.  Metabolism . 1998;  47 769-776
    CrossrefPubMedGoogle Scholar
  • 126 Reeves R R. Effects of thyroid hormone treatment on 31P-NMR spectroscopy of muscle and on nerve conduction studies in a patient with long-standing severe hypothyroidism.  J Am Osteopath Assoc . 1996;  96 424-428
    PubMedGoogle Scholar
  • 127 Dudley C R, Taylor D J, Ng L L. Evidence for abnormal Na+/H+ antiport activity detected by phosphorus nuclear magnetic resonance spectroscopy in exercising skeletal muscle of patients with essential hypertension.  Clin Sci . 1990;  79 491-497
    PubMedGoogle Scholar
  • 128 Arnold D L, Bore P J, Radda G K, Styles P, Taylor D J. Excessive intracellular acidosis of skeletal muscle on exercise in a patient with a post-viral exhaustion/fatigue syndrome. A 31P nuclear magnetic resonance study.  Lancet . 1984;  1 1367-1369
    PubMedGoogle Scholar
  • 129 Barnes P R, Taylor D J, Kemp G J, Radda G K. Skeletal muscle bioenergetics in the chronic fatigue syndrome.  J Neurol Neurosurg Psychiatry . 1993;  56 679-683
    PubMedGoogle Scholar
  • 130 Lodi R, Taylor D J, Radda G K. Chronic fatigue syndrome and skeletal muscle mitochondrial function.  Muscle Nerve . 1997;  20 765-766
    PubMedGoogle Scholar
  • 131 McCully K K, Natelson B H, Iotti S, Sisto S, Leigh Jr S J. Reduced oxidative muscle metabolism in chronic fatigue syndrome.  Muscle Nerve . 1996;  19 621-625
    PubMedGoogle Scholar
  • 132 Lane R J, Barrett M C, Taylor D J, Kemp G J, Lodi R. Heterogeneity in chronic fatigue syndrome: evidence from magnetic resonance spectroscopy of muscle.  Neuromuscul Disord . 1998;  8 204-209
    CrossrefPubMedGoogle Scholar
  • 133 Simms R, Roy S, Hrovat M. Lack of association between fibromyalgia syndrome and abnormalities in muscle energy metabolism.  Arthritis Rheum . 1994;  37 794-800
    PubMedGoogle Scholar
  • 134 Vestergaard-Poulsen P, Thomsen C, Norregaard J. 31P NMR spectroscopy and electromyography during exercise and recovery in patients with fibromyalgia.  J Rheumatol . 1995;  22 1544-1551
    PubMedGoogle Scholar
  • 135 de Blecourt C A, Wolf R F, van Rijswijk H M. In vivo 31P magnetic resonance spectroscopy (MRS) of tender points in patients with primary fibromyalgia syndrome.  Rheumatol Int . 1991;  11 51-54
    CrossrefPubMedGoogle Scholar
  • 136 Park J H, Phothimat P, Oates C T, Hernanz-Schulman M, Olsen N J. Use of P-31 magnetic resonance spectroscopy to detect metabolic abnormalities in muscles of patients with fibromyalgia.  Arthritis Rheum . 1998;  41 406-413
    CrossrefPubMedGoogle Scholar
  • 137 Philip P A, Thompson C H, Carmichael J. A phase I study of the left-shifting agent BW12C79 plus mitomycin-C and the effect on the skeletal muscle metabolism using P31 magnetic resonance spectroscopy.  Cancer Res . 1993;  53 5649-5653
    PubMedGoogle Scholar
  • 138 Hickman P F, Kemp G J, Thompson C H. Bryostatin 1, a novel antineoplastic agent and protein kinase C activator, induces human myalgia and muscle metabolic defects: a 31P magnetic resonance spectroscopic study.  Br J Cancer . 1995;  72 998-1003
    PubMedGoogle Scholar
  • 139 Thompson C H, Macaulay V M, O'Byrne K J. Modulation of bryostatin 1 muscle toxicity by nifedipine: effects on muscle metabolism and oxygen supply.  Br J Cancer . 1996;  73 1161-1165
    PubMedGoogle Scholar
  • 140 Propper D J, Braybrooke J P, Taylor D J. Phase I trial of the selective mitochondrial toxin MKT 077 in chemo-resistant solid tumours.  Annals of Oncology . 1999;  10 923-927
    CrossrefPubMedGoogle Scholar
  • 141 Weissman J D, Constantinitis I, Hudgins P, Wallace D C. 31P magnetic resonance spectroscopy suggests impaired mitochondrial function in AZT-treated HIV-infected patients.  Neurology . 1992;  42 619-623
    PubMedGoogle Scholar
  • 142 Sinnwell T M, Sivakumar K, Soueidan K, Frank J A, McLaughlin A C, Dalakas M C. Metabolic abnormalities in skeletal muscle of patients receiving zidovudine therapy observed by 31P in vivo magnetic resonance spectroscopy.  J Clin Invest . 1995;  95 126-131
    PubMedGoogle Scholar
  • 143 Simpson M V, Chin C D, Keilbaugh S A, Lin T S, Prusoff W H. Studies on the inhibition of mitochondrial DNA replication by 3′-azido-3′-deoxythymidine and other dideoxynucleoside analogs which inhibit HIV-1 replication.  Biochem Pharmacol . 1989;  38 1033-1036
    CrossrefPubMedGoogle Scholar
  • 144 Bollaert P E, Robin-Lherbier B, Escanye J M. Phosphorus nuclear magnetic resonance evidence of abnormal skeletal muscle metabolism in chronic alcoholics.  Neurology . 1989;  39 821-824
    PubMedGoogle Scholar
  • 145 Taylor D, Fleckenstein J L, Lodi R. Imaging and spectroscopy of muscle. In: Karpati G, Hilton-Jones D, Griggs R, eds. Disorders of Voluntary Muscle. In press Cambridge, UK: Cambridge University Press 2001
    Google Scholar
      >