Neuromuscular Disorders
Volume 20, Issue 8 , Pages 548-558 , August 2010

Investigating glycogenosis type III patients with multi-parametric functional NMR imaging and spectroscopy

  • Claire Wary

      Affiliations

    • Institute of Myology, Paris, France
    • CEA, I2BM, MIRCen, IdM NMR Laboratory, Paris, France
    • UPMC University Paris 06, Paris, France
    • Corresponding Author InformationCorresponding author. Address: NMR Laboratory AIM-CEA, Institut de Myologie, Bat Babinski, G.H. Pitie-Salpetriere, 75651 Paris Cedex 13, France. Tel.: +33 1 42 16 58 92; fax: +33 1 42 16 58 97.
    • ,
  • Aleksandra Nadaj-Pakleza

      Affiliations

    • East-Paris Reference Center for Neuromuscular Pathology, Pitié-Salpêtrière University Hospital, AP-HP, Paris, France
    • Department of Neurology, Angers University Hospital, Angers, France
    • ,
  • Pascal Laforêt

      Affiliations

    • Institute of Myology, Paris, France
    • East-Paris Reference Center for Neuromuscular Pathology, Pitié-Salpêtrière University Hospital, AP-HP, Paris, France
    • ,
  • Kristl G. Claeys

      Affiliations

    • Institute of Myology, Paris, France
    • East-Paris Reference Center for Neuromuscular Pathology, Pitié-Salpêtrière University Hospital, AP-HP, Paris, France
    • ,
  • Robert Carlier

      Affiliations

    • Institute of Myology, Paris, France
    • Medical Imaging Department and Center for Technological Innovation, Raymond Poincaré University Hospital, AP-HP, Garches, France
    • ,
  • Aurélien Monnet

      Affiliations

    • Institute of Myology, Paris, France
    • CEA, I2BM, MIRCen, IdM NMR Laboratory, Paris, France
    • UPMC University Paris 06, Paris, France
    • ,
  • Servanne Fleury

      Affiliations

    • Institute of Myology, Paris, France
    • CEA, I2BM, MIRCen, IdM NMR Laboratory, Paris, France
    • UPMC University Paris 06, Paris, France
    • ,
  • Céline Baligand

      Affiliations

    • Institute of Myology, Paris, France
    • CEA, I2BM, MIRCen, IdM NMR Laboratory, Paris, France
    • UPMC University Paris 06, Paris, France
    • ,
  • Bruno Eymard

      Affiliations

    • Institute of Myology, Paris, France
    • East-Paris Reference Center for Neuromuscular Pathology, Pitié-Salpêtrière University Hospital, AP-HP, Paris, France
    • ,
  • Philippe Labrune

      Affiliations

    • Department of Pediatrics, Antoine Béclère University Hospital, AP-HP, Clamart, France
    • ,
  • Pierre G. Carlier

      Affiliations

    • Institute of Myology, Paris, France
    • CEA, I2BM, MIRCen, IdM NMR Laboratory, Paris, France
    • UPMC University Paris 06, Paris, France

Received 23 February 2010 ,Revised 27 May 2010 ,Accepted 7 June 2010.

References 

  1. Forbes GB. Glycogen storage disease; report of a case with abnormal glycogen structure in liver and skeletal muscle. J Pediatr. 1953;42:645–653
  2. Illingworth B, Cori GT, Cori CF. Amylo-1,6-glucosidase in muscle tissue in generalized glycogen storage disease. J Biol Chem. 1956;218:123–129
  3. Coleman RA, Winter HS, Wolf B, Gilchrist JM, Chen YT. Glycogen storage disease type III (glycogen debranching enzyme deficiency): correlation of biochemical defects with myopathy and cardiomyopathy. Ann Intern Med. 1992;116:896–900
  4. Kiechl S, Willeit J, Vogel W, Kohlendorfer U, Poewe W. Reversible severe myopathy of respiratory muscles due to adult-onset type III glycogenosis. Neuromuscul Disord. 1999;9:408–410
  5. Momoi T, Sano H, Yamanaka C, Sasaki H, Mikawa H. Glycogen storage disease type III with muscle involvement: reappraisal of phenotypic variability and prognosis. Am J Med Genet. 1992;42:696–699
  6. Shen J, Bao Y, Liu HM, Lee P, Leonard JV, Chen YT. Mutations in exon 3 of the glycogen debranching enzyme gene are associated with glycogen storage disease type III that is differentially expressed in liver and muscle. J Clin Invest. 1996;98:352–357
  7. Lucchiari S, Pagliarani S, Salani S, Filocamo M, Di Rocco M, Melis D, et al. Hepatic and neuromuscular forms of glycogenosis type III: nine mutations in AGL. Hum Mutat. 2006;27:600–601
  8. Shaiu WL, Kishnani PS, Shen J, Liu HM, Chen YT. Genotype–phenotype correlation in two frequent mutations and mutation update in type III glycogen storage disease. Mol Genet Metab. 2000;69:16–23
  9. Walton J, Rowland L. Clinical examination, differential diagnosis and classification. In:  Walton J,  Karpati G,  Hilton-Jones D editor. Disorders of Voluntary Muscle. sixth ed.. New York: Churchill Livingstone; 1994;p. 1771
  10. Raynaud JS, Carlier PG, Wary C, Duteil S, Leroy-Willig A, Vaughan JT, et al. Improved methodology for dynamic studies of muscle oxygen metabolism using 1H/31P imaging/spectroscopy protocols (Abstract). MAGMA. 1999;9:150
  11. Wary C, Carlier PG, Laforet P, Eymard B, Fardeau M, Leroy-Willig A. T1-weighted interleaved acquisitions of glycogen and creatine spectra for improved clinical characterisation of glycogenoses by 13C NMR spectroscopy. MAGMA. 2000;11:153
  12. Jehenson P, Duboc D, Bloch G, Fardeau M, Syrota A. Diagnosis of muscular glycogenosis by in vivo natural abundance 13C NMR spectroscopy. Neuromuscul Disord. 1991;1:99–101
  13. Wary C, Laforet P, Eymard B, Fardeau M, Leroy-Willig A, Bassez G, et al. Evaluation of muscle glycogen content by 13C NMR spectroscopy in adult-onset acid maltase deficiency. Neuromuscul Disord. 2003;13:545–553
  14. Mercuri E, Pichiecchio A, Allsop J, Messina S, Pane M, Muntoni F. Muscle MRI in inherited neuromuscular disorders: past, present, and future. J Magn Reson Imaging. 2007;25:433–440
  15. Taylor DJ, Bore PJ, Styles P, Gadian DG, Radda GK. Bioenergetics of intact human muscle. A 31P nuclear magnetic resonance study. Mol Biol Med. 1983;1:77–94
  16. Laforet P, Wary C, Duteil S, de Kerviler E, Carlier PG, Lombes A, et al. Exploration of exercise intolerance by 31P NMR spectroscopy of calf muscles coupled with MRI and ergometry. Rev Neurol (Paris). 2003;159:56–67
  17. 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
  18. Raynaud JS, Duteil S, Vaughan JT, Hennel F, Wary C, Leroy-Willig A, et al. Determination of skeletal muscle perfusion using arterial spin labeling NMRI: validation by comparison with venous occlusion plethysmography. Magn Reson Med. 2001;46:305–311
  19. Brillault-Salvat C, Giacomini E, Wary C, Peynsaert J, Jouvensal L, Bloch G, et al. An interleaved heteronuclear NMRI–NMRS approach to non-invasive investigation of exercising human skeletal muscle. Cell Mol Biol (Noisy-le-grand). 1997;43:751–762
  20. Carlier PG, Brillault-Salvat C, Giacomini E, Wary C, Bloch G. How to investigate oxygen supply, uptake, and utilization simultaneously by interleaved NMR imaging and spectroscopy of the skeletal muscle. Magn Reson Med. 2005;54:1010–1013
  21. Toussaint JF, Kwong KK, Mkparu FO, Weisskoff RM, LaRaia PJ, Kantor HL. Perfusion changes in human skeletal muscle during reactive hyperemia measured by echo-planar imaging. Magn Reson Med. 1996;35:62–69
  22. Lebon V, Brillault-Salvat C, Bloch G, Leroy-Willig A, Carlier PG. Evidence of muscle BOLD effect revealed by simultaneous interleaved gradient-echo NMRI and myoglobin NMRS during leg ischemia. Magn Reson Med. 1998;40:551–558
  23. Duteil S, Wary C, Raynaud JS, Lebon V, Lesage D, Leroy-Willig A, et al. Influence of vascular filling and perfusion on BOLD contrast during reactive hyperemia in human skeletal muscle. Magn Reson Med. 2006;55:450–454
  24. Damon BM, Wadington MC, Hornberger JL, Lansdown DA. Absolute and relative contributions of BOLD effects to the muscle functional MRI signal intensity time course: effect of exercise intensity. Magn Reson Med. 2007;58:335–345
  25. Meyer RA, Prior BM. Functional magnetic resonance imaging of muscle. Exerc Sport Sci Rev. 2000;28:89–92
  26. Richardson RS, Newcomer SC, Noyszewski EA. Skeletal muscle intracellular PO(2) assessed by myoglobin desaturation: response to graded exercise. J Appl Physiol. 2001;91:2679–2685
  27. Duteil S, Bourrilhon C, Raynaud JS, Wary C, Richardson RS, Leroy-Willig A, et al. Metabolic and vascular support for the role of myoglobin in humans: a multiparametric NMR study. Am J Physiol Regul Integr Comp Physiol. 2004;287:R1441–1449
  28. Dubowitz V, Sewry CA. Muscle Biopsy: A Practical Approach. 3rd ed.. London: Saunders Elsevier; 2007;
  29. Monnet A, Wary C, Wuyam B, Verges S, Duteil S, Carlier PG. Influence of workload on human calf muscle following dynamic aerobic exercise: BOLD effect, perfusion, oxygenation and energetics assessed by mpf-NMR. MAGMA. 2008;21(Suppl. 1):92
  30. Edwards RH, Dawson MJ, Wilkie DR, Gordon RE, Shaw D. Clinical use of nuclear magnetic resonance in the investigation of myopathy. Lancet. 1982;1:725–731
  31. Chan WP, Liu GC. MR imaging of primary skeletal muscle diseases in children. AJR Am J Roentgenol. 2002;179:989–997
  32. Kuo GP, Carrino JA. Skeletal muscle imaging and inflammatory myopathies. Curr Opin Rheumatol. 2007;19:530–535
  33. Lovitt S, Moore SL, Marden FA. The use of MRI in the evaluation of myopathy. Clin Neurophysiol. 2006;117:486–495
  34. Ozsarlak O, Schepens E, Parizel PM, Van Goethem JW, Vanhoenacker F, De Schepper AM, et al. Hereditary neuromuscular diseases. Eur J Radiol. 2001;40:184–197
  35. de Kerviler E, Leroy-Willig ALW, Duboc D, Eymard B, Syrota A. MR quantification of muscle fatty replacement in McArdle’s disease. Magn Reson Imaging. 1996;14:1137–1141
  36. Pichiecchio A, Uggetti C, Ravaglia S, Egitto MG, Rossi M, Sandrini G, et al. Muscle MRI in adult-onset acid maltase deficiency. Neuromuscul Disord. 2004;14:51–55
  37. Brooke MH, Fenichel GM, Griggs RC, Mendell JR, Moxley R, Miller JP, et al. Clinical investigation in Duchenne dystrophy: 2. Determination of the “power” of therapeutic trials based on the natural history. Muscle Nerve. 1983;6:91–103
  38. Lord JP, Lieberman JS, Portwood MM, Fowler WM, Carson R. Functional ability and equipment use among patients with neuromuscular disease. Arch Phys Med Rehabil. 1987;68:348–352
  39. Seelig J, Burlina AP. Carbon-13 magnetic resonance in biology and medicine. Clin Chim Acta. 1992;206:125–136
  40. Jehenson P, Duboc D, Labrune P, Fardeau M, Odievre M, Syrota A. Diagnostic value of the evaluation of the glycogen content in muscle diseases by carbon 13 nuclear magnetic resonance. J Chim Phys. 1995;92:1797–1800
  41. Wary C, Bloch G, Jehenson P, Carlier PG. 13C NMR spectroscopy of lipids: a simple method for absolute quantitation. Anticancer Res. 1996;16:1479–1484
  42. Tarnopolsky MA, Parise G. Direct measurement of high-energy phosphate compounds in patients with neuromuscular disease. Muscle Nerve. 1999;22:1228–1233
  43. Cornelio F, Bresolin N, Singer PA, DiMauro S, Rowland LP. Clinical varieties of neuromuscular disease in debrancher deficiency. Arch Neurol. 1984;41:1027–1032
  44. Kiechl S, Kohlendorfer U, Thaler C, Skladal D, Jaksch M, Obermaier-Kusser B, et al. Different clinical aspects of debrancher deficiency myopathy. J Neurol Neurosurg Psychiatry. 1999;67:364–368
  45. Griffin JL. Infantile acid maltase deficiency. I. Muscle fiber destruction after lysosomal rupture. Virchows Arch B Cell Pathol Incl Mol Pathol. 1984;45:23–36
  46. Raben N, Danon M, Gilbert AL, Dwivedi S, Collins B, Thurberg BL, et al. Enzyme replacement therapy in the mouse model of Pompe disease. Mol Genet Metab. 2003;80:159–169
  47. Itoh M, Iio M, Kawai M, Takizawa O, Yoshikawa K, Minami M, et al. 31P NMR spectroscopy of myopathies: clinical application of whole-body MR. Radiat Med. 1986;4:41–45
  48. Duboc D, Jehenson P, Tran Dinh S, Marsac C, Syrota A, Fardeau M. Phosphorus NMR spectroscopy study of muscular enzyme deficiencies involving glycogenolysis and glycolysis. Neurology. 1987;37:663–671
  49. Bell JD, Cox IJ, Sargentoni J, Peden CJ, Menon DK, Foster CS, et al. A 31P and 1H NMR investigation in vitro of normal and abnormal human liver. Biochim Biophys Acta. 1993;1225:71–77
  50. Chance B, Eleff S, Bank W, Leigh JS, Warnell R. 31P NMR studies of control of mitochondrial function in phosphofructokinase-deficient human skeletal muscle. Proc Natl Acad Sci USA. 1982;79:7714–7718
  51. Roach PJ. Glycogen and its metabolism. Curr Mol Med. 2002;2:101–120
  52. Lomako J, Lomako WM, Kirkman BR, Whelan WJ. The role of phosphate in muscle glycogen. Biofactors. 1994;4:167–171
  53. Tagliabracci VS, Turnbull J, Wang W, Girard JM, Zhao X, Skurat AV, et al. Laforin is a glycogen phosphatase, deficiency of which leads to elevated phosphorylation of glycogen in vivo. Proc Natl Acad Sci USA. 2007;104:19262–19266
  54. Argov Z, Lofberg M, Arnold DL. Insights into muscle diseases gained by phosphorus magnetic resonance spectroscopy. Muscle Nerve. 2000;23:1316–1334
  55. De Stefano N, Argov Z, Matthews PM, Karpati G, Arnold DL. Impairment of muscle mitochondrial oxidative metabolism in McArdles’s disease. Muscle Nerve. 1996;19:764–769
  56. Lewis SF, Haller RG, Cook JD, Nunnally RL. Muscle fatigue in McArdle’s disease studied by 31P-NMR: effect of glucose infusion. J Appl Physiol. 1985;59:1991–1994
  57. Carlier PG, Bertoldi D, Baligand C, Wary C, Fromes Y. Muscle blood flow and oxygenation measured by NMR imaging and spectroscopy. NMR Biomed. 2006;19:954–967
  58. Ismail H. Glycogen storage disease type III presenting with secondary diabetes and managed with insulin: a case report. Cases J. 2009;2:6891
  59. Spengos K, Michelakakis H, Vontzalidis A, Zouvelou V, Manta P. Diabetes mellitus associated with glycogen storage disease type III. Muscle Nerve. 2009;39:876–877
  60. Oki Y, Okubo M, Tanaka S, Nakanishi K, Kobayashi T, Murase T. Diabetes mellitus secondary to glycogen storage disease type III. Diabet Med. 2000;17:810–812

PII: S0960-8966(10)00265-8

doi: 10.1016/j.nmd.2010.06.011

Neuromuscular Disorders
Volume 20, Issue 8 , Pages 548-558 , August 2010

Article Tools

* Image Usage & Resolution