Skip to main content
Erschienen in: European Radiology 6/2019

17.12.2018 | Musculoskeletal

Muscle diffusion tensor imaging in glycogen storage disease V (McArdle disease)

verfasst von: R. Rehmann, L. Schlaffke, M. Froeling, R. A. Kley, E. Kühnle, M. De Marées, J. Forsting, M. Rohm, M. Tegenthoff, T. Schmidt-Wilcke, M. Vorgerd

Erschienen in: European Radiology | Ausgabe 6/2019

Einloggen, um Zugang zu erhalten

Abstract

Purpose

To evaluate differences in diffusion parameters in thigh muscles in patients with glycogen storage disease type V (McArdle disease) using muscle diffusion tensor imaging (mDTI) compared to healthy controls

Methods

In this prospective study, we evaluated thigh muscles from hip to knee of 10 McArdle patients (5 female, mean age 33.7 ± 14.4 years) and 10 healthy age- and gender-matched volunteers. MRI scans were performed at 3 T and comprised mDTI, T1-weighted and T2-weighted imaging between May 2015 and May 2017. Needle biopsy of the vastus lateralis muscle was performed in three McArdle patients. The muscle tissue was analyzed by using histochemical and enzyme-histochemical techniques for glycogen content and histopathological changes. Mean values of the eigenvalues (λ1λ3), fractional anisotropy (FA), and mean diffusivity (MD) were obtained for the vastus lateralis, vastus medialis, rectus femoris, biceps femoris, semitendinosus, and semimembranosus and compared between groups using Student’s t tests, as well as ANCOVA; significance level was set at p < 0.05.

Results

Needle biopsy showed intracellular glycogen accumulation in skeletal muscle fibers of three McArdle patients. Extracellular histopathological changes were not found. Muscle DTI analysis did not show statistically significant differences between patients and controls for any of the muscles.

Conclusion

Despite intracellular glycogen accumulation in the three biopsy samples, mDTI parameters were not altered in McArdle patients compared to controls. We conclude that the currently used mDTI acquisition and processing lack the sensitivity to detect intracellular changes due to accumulated glycogen in this cohort of McArdle patients.

Key Points

Despite intracellular glycogen accumulation in three examined biopsy samples, mDTI parameters were not altered in McArdle patients compared to controls.
In its current form, diffusion MR does not provide additional information in quantifying intracellular glycogen accumulations within skeletal muscle fibers in McArdle patients.
Anhänge
Nur mit Berechtigung zugänglich
Literatur
1.
Zurück zum Zitat De Castro M, Johnston J, Biesecker L (2015) Determining the prevalence of McArdle disease from gene frequency by analysis of next generation sequencing data: McArdle prevalence by NGS data. Genet Med 17:1002–1006CrossRefPubMedPubMedCentral De Castro M, Johnston J, Biesecker L (2015) Determining the prevalence of McArdle disease from gene frequency by analysis of next generation sequencing data: McArdle prevalence by NGS data. Genet Med 17:1002–1006CrossRefPubMedPubMedCentral
2.
Zurück zum Zitat Quinlivan R, Buckley J, James M et al (2010) McArdle disease: a clinical review. J Neurol Neurosurg Psychiatry 81:1182–1188CrossRefPubMed Quinlivan R, Buckley J, James M et al (2010) McArdle disease: a clinical review. J Neurol Neurosurg Psychiatry 81:1182–1188CrossRefPubMed
3.
Zurück zum Zitat Lebo RV, Gorin F, Fletterick RJ et al (1984) High-resolution chromosome sorting and DNA spot-blot analysis assign McArdle’s syndrome to chromosome 11. Science (80- ) 225:57–59CrossRef Lebo RV, Gorin F, Fletterick RJ et al (1984) High-resolution chromosome sorting and DNA spot-blot analysis assign McArdle’s syndrome to chromosome 11. Science (80- ) 225:57–59CrossRef
4.
Zurück zum Zitat McArdle B (1951) Myopathy due to a defect in muscle glycogen breakdown. Clin Sci 10:13–35PubMed McArdle B (1951) Myopathy due to a defect in muscle glycogen breakdown. Clin Sci 10:13–35PubMed
5.
Zurück zum Zitat Preisler N, Haller RG, Vissing J (2015) Exercise in muscle glycogen storage diseases. J Inherit Metab Dis 38:551–563CrossRefPubMed Preisler N, Haller RG, Vissing J (2015) Exercise in muscle glycogen storage diseases. J Inherit Metab Dis 38:551–563CrossRefPubMed
6.
Zurück zum Zitat Godfrey R, Quinlivan R (2016) Skeletal muscle disorders of glycogenolysis and glycolysis. Nat Rev Neurol 12:393–402CrossRefPubMed Godfrey R, Quinlivan R (2016) Skeletal muscle disorders of glycogenolysis and glycolysis. Nat Rev Neurol 12:393–402CrossRefPubMed
7.
8.
Zurück zum Zitat Nogales-Gadea G, Santalla A, Ballester-Lopez A et al (2016) Exercise and preexercise nutrition as treatment for McArdle disease. Med Sci Sports Exerc 48:673–679CrossRefPubMed Nogales-Gadea G, Santalla A, Ballester-Lopez A et al (2016) Exercise and preexercise nutrition as treatment for McArdle disease. Med Sci Sports Exerc 48:673–679CrossRefPubMed
9.
Zurück zum Zitat Quinlivan R, Martinuzzi A, Schoser B (2014) Pharmacological and nutritional treatment for McArdle disease (Glycogen Storage Disease type V). Cochrane Database Syst Rev 12:CD003458 Quinlivan R, Martinuzzi A, Schoser B (2014) Pharmacological and nutritional treatment for McArdle disease (Glycogen Storage Disease type V). Cochrane Database Syst Rev 12:CD003458
10.
Zurück zum Zitat Vorgerd M, Zange J (2007) Treatment of glycogenosys type V (McArdle disease) with creatine and ketogenic diet with clinical scores and with 31P-MRS on working leg muscle. Acta Myol 26:61–63PubMedPubMedCentral Vorgerd M, Zange J (2007) Treatment of glycogenosys type V (McArdle disease) with creatine and ketogenic diet with clinical scores and with 31P-MRS on working leg muscle. Acta Myol 26:61–63PubMedPubMedCentral
11.
Zurück zum Zitat De Kerviler E, Leroy-Willig A, Duboc D, Eymard B, Syrota A (1996) MR quantification of muscle fatty replacement in McArdle’s disease. Magn Reson Imaging 14:1137–1141 De Kerviler E, Leroy-Willig A, Duboc D, Eymard B, Syrota A (1996) MR quantification of muscle fatty replacement in McArdle’s disease. Magn Reson Imaging 14:1137–1141
12.
Zurück zum Zitat Nadaj-Pakleza AA, Vincitorio CM, Laforêt P et al (2009) Permanent muscle weakness in McArdle disease. Muscle Nerve 40:350–357CrossRefPubMed Nadaj-Pakleza AA, Vincitorio CM, Laforêt P et al (2009) Permanent muscle weakness in McArdle disease. Muscle Nerve 40:350–357CrossRefPubMed
13.
Zurück zum Zitat Zange J, Grehl T, Disselhorst-Klug C et al (2003) Breakdown of adenine nucleotide pool in fatiguing skeletal muscle in McArdle’s disease: a noninvasive 31P-MRS and EMG study. Muscle Nerve 27:728–736CrossRefPubMed Zange J, Grehl T, Disselhorst-Klug C et al (2003) Breakdown of adenine nucleotide pool in fatiguing skeletal muscle in McArdle’s disease: a noninvasive 31P-MRS and EMG study. Muscle Nerve 27:728–736CrossRefPubMed
14.
Zurück zum Zitat Heinicke K, Dimitrov IE, Romain N et al (2014) Reproducibility and absolute quantification of muscle glycogen in patients with glycogen storage disease by 13C NMR spectroscopy at 7 tesla. PLoS One 9:e108706 Heinicke K, Dimitrov IE, Romain N et al (2014) Reproducibility and absolute quantification of muscle glycogen in patients with glycogen storage disease by 13C NMR spectroscopy at 7 tesla. PLoS One 9:e108706
15.
Zurück zum Zitat Lewis SF, Haller RG, Cook JD, Nunnally RL (1985) Muscle fatigue in McArdle’s disease studied by 31P-NMR: effect of glucose infusion. J Appl Physiol (1985) 59:1991–1994 Lewis SF, Haller RG, Cook JD, Nunnally RL (1985) Muscle fatigue in McArdle’s disease studied by 31P-NMR: effect of glucose infusion. J Appl Physiol (1985) 59:1991–1994
16.
Zurück zum Zitat Gruetter R, Kaelin P, Boesch C, Martin E, Werner B (1990) Non-invasive31P magnetic resonance spectroscopy revealed McArdle disease in an asymptomatic child. Eur J Pediatr 149:483–486 Gruetter R, Kaelin P, Boesch C, Martin E, Werner B (1990) Non-invasive31P magnetic resonance spectroscopy revealed McArdle disease in an asymptomatic child. Eur J Pediatr 149:483–486
17.
Zurück zum Zitat de Kerviler E, Leroy-Willig A, Jehenson P, Duboc D, Eymard B, Syrota A (1991) Exercise-induced muscle modifications: study of healthy subjects and patients with metabolic myopathies with MR imaging and P-31 spectroscopy. Radiology 181:259–264 de Kerviler E, Leroy-Willig A, Jehenson P, Duboc D, Eymard B, Syrota A (1991) Exercise-induced muscle modifications: study of healthy subjects and patients with metabolic myopathies with MR imaging and P-31 spectroscopy. Radiology 181:259–264
18.
Zurück zum Zitat Ai T, Yu K, Gao L et al (2014) Diffusion tensor imaging in evaluation of thigh muscles in patients with polymyositis and dermatomyositis. Br J Radiol 87:20140261CrossRefPubMedPubMedCentral Ai T, Yu K, Gao L et al (2014) Diffusion tensor imaging in evaluation of thigh muscles in patients with polymyositis and dermatomyositis. Br J Radiol 87:20140261CrossRefPubMedPubMedCentral
19.
Zurück zum Zitat Budzik JF, Balbi V, Verclytte S, Pansini V, Le Thuc V, Cotten A (2014) Diffusion tensor imaging in musculoskeletal disorders. Radiographics 34:E56–E72 Budzik JF, Balbi V, Verclytte S, Pansini V, Le Thuc V, Cotten A (2014) Diffusion tensor imaging in musculoskeletal disorders. Radiographics 34:E56–E72
20.
Zurück zum Zitat Damon BM, Froeling M, Buck AKW et al (2016) Skeletal muscle diffusion tensor-MRI fiber tracking: rationale, data acquisition and analysis methods, applications and future directions. NMR Biomed 30:1–13 Damon BM, Froeling M, Buck AKW et al (2016) Skeletal muscle diffusion tensor-MRI fiber tracking: rationale, data acquisition and analysis methods, applications and future directions. NMR Biomed 30:1–13
21.
Zurück zum Zitat Froeling M, Oudeman J, Strijkers GJ et al (2015) Muscle changes detected with diffusion-tensor imaging after long-distance running. Radiology 274:548–562CrossRefPubMed Froeling M, Oudeman J, Strijkers GJ et al (2015) Muscle changes detected with diffusion-tensor imaging after long-distance running. Radiology 274:548–562CrossRefPubMed
23.
Zurück zum Zitat Ponrartana S, Ramos-Platt L, Wren TA et al (2015) Effectiveness of diffusion tensor imaging in assessing disease severity in Duchenne muscular dystrophy: preliminary study. Pediatr Radiol 45:582–589CrossRefPubMed Ponrartana S, Ramos-Platt L, Wren TA et al (2015) Effectiveness of diffusion tensor imaging in assessing disease severity in Duchenne muscular dystrophy: preliminary study. Pediatr Radiol 45:582–589CrossRefPubMed
24.
Zurück zum Zitat Bergström J (1975) Percutaneous needle biopsy of skeletal muscle in physiological and clinical research. Scand J Clin Lab Invest 35:609–616CrossRefPubMed Bergström J (1975) Percutaneous needle biopsy of skeletal muscle in physiological and clinical research. Scand J Clin Lab Invest 35:609–616CrossRefPubMed
25.
Zurück zum Zitat Ekblom B (2017) The muscle biopsy technique. Historical and methodological considerations. Scand J Med Sci Sports 27:458–461CrossRefPubMed Ekblom B (2017) The muscle biopsy technique. Historical and methodological considerations. Scand J Med Sci Sports 27:458–461CrossRefPubMed
26.
Zurück zum Zitat Shanely RA, Zwetsloot KA, Triplett NT, Meaney MP, Farris GE, Nieman DC (2014) Human skeletal muscle biopsy procedures using the modified Bergström technique. J Vis Exp 10:51812 Shanely RA, Zwetsloot KA, Triplett NT, Meaney MP, Farris GE, Nieman DC (2014) Human skeletal muscle biopsy procedures using the modified Bergström technique. J Vis Exp 10:51812
28.
29.
Zurück zum Zitat Froeling M, Nederveen AJ, Nicolay K, Strijkers GJ (2013) DTI of human skeletal muscle: the effects of diffusion encoding parameters, signal-to-noise ratio and T2 on tensor indices and fiber tracts. NMR Biomed 26:1339–1352 Froeling M, Nederveen AJ, Nicolay K, Strijkers GJ (2013) DTI of human skeletal muscle: the effects of diffusion encoding parameters, signal-to-noise ratio and T2 on tensor indices and fiber tracts. NMR Biomed 26:1339–1352
30.
Zurück zum Zitat Froeling M, Nederveen AJ, Heijtel DF et al (2012) Diffusion-tensor MRI reveals the complex muscle architecture of the human forearm. J Magn Reson Imaging 36:237–248CrossRefPubMed Froeling M, Nederveen AJ, Heijtel DF et al (2012) Diffusion-tensor MRI reveals the complex muscle architecture of the human forearm. J Magn Reson Imaging 36:237–248CrossRefPubMed
31.
Zurück zum Zitat Veraart J, Novikov DS, Christiaens D, Ades-Aron B, Sijbers J, Fieremans E (2016) Denoising of diffusion MRI using random matrix theory. Neuroimage 142:394–406 Veraart J, Novikov DS, Christiaens D, Ades-Aron B, Sijbers J, Fieremans E (2016) Denoising of diffusion MRI using random matrix theory. Neuroimage 142:394–406
32.
Zurück zum Zitat Leemans A, Jones DK (2009) The B-matrix must be rotated when correcting for subject motion in DTI data. Magn Reson Med 61:1336–1349CrossRefPubMed Leemans A, Jones DK (2009) The B-matrix must be rotated when correcting for subject motion in DTI data. Magn Reson Med 61:1336–1349CrossRefPubMed
33.
Zurück zum Zitat Veraart J, Sijbers J, Sunaert S, Leemans A, Jeurissen B (2013) Weighted linear least squares estimation of diffusion MRI parameters: strengths, limitations, and pitfalls. Neuroimage 81:335–346 Veraart J, Sijbers J, Sunaert S, Leemans A, Jeurissen B (2013) Weighted linear least squares estimation of diffusion MRI parameters: strengths, limitations, and pitfalls. Neuroimage 81:335–346
34.
Zurück zum Zitat Froeling M, Tax CMW, Vos SB, Luijten PR, Leemans A (2017) “MASSIVE” brain dataset: multiple acquisitions for standardization of structural imaging validation and evaluation. Magn Reson Med 77:1797–1809 Froeling M, Tax CMW, Vos SB, Luijten PR, Leemans A (2017) “MASSIVE” brain dataset: multiple acquisitions for standardization of structural imaging validation and evaluation. Magn Reson Med 77:1797–1809
35.
Zurück zum Zitat Li GD, Liang YY, Xu P, Ling J, Chen YM (2016) Diffusion-tensor imaging of thigh muscles in Duchenne muscular dystrophy: correlation of apparent diffusion coefficient and fractional anisotropy values with fatty infiltration. AJR Am J Roentgenol 206:867–870 Li GD, Liang YY, Xu P, Ling J, Chen YM (2016) Diffusion-tensor imaging of thigh muscles in Duchenne muscular dystrophy: correlation of apparent diffusion coefficient and fractional anisotropy values with fatty infiltration. AJR Am J Roentgenol 206:867–870
36.
Zurück zum Zitat Scheel M, Winkler T, Scheel M et al (2013) Fiber type characterization in skeletal muscle by diffusion tensor imaging. NMR Biomed 26:1220–1224 Scheel M, Winkler T, Scheel M et al (2013) Fiber type characterization in skeletal muscle by diffusion tensor imaging. NMR Biomed 26:1220–1224
37.
Zurück zum Zitat Berry DB, Regner B, Galinsky V, Ward SR, Frank LR (2018) Relationships between tissue microstructure and the diffusion tensor in simulated skeletal muscle. Magn Reson Med 80:317–329 Berry DB, Regner B, Galinsky V, Ward SR, Frank LR (2018) Relationships between tissue microstructure and the diffusion tensor in simulated skeletal muscle. Magn Reson Med 80:317–329
38.
Zurück zum Zitat Jehenson P, Leroy-Willig A, de Kerviler E, Duboc D, Syrota A (1993) MR imaging as a potential diagnostic test for metabolic myopathies: importance of variations in the T2 of muscle with exercise. Am J Roentgenol 161:347–351 Jehenson P, Leroy-Willig A, de Kerviler E, Duboc D, Syrota A (1993) MR imaging as a potential diagnostic test for metabolic myopathies: importance of variations in the T2 of muscle with exercise. Am J Roentgenol 161:347–351
Metadaten
Titel
Muscle diffusion tensor imaging in glycogen storage disease V (McArdle disease)
verfasst von
R. Rehmann
L. Schlaffke
M. Froeling
R. A. Kley
E. Kühnle
M. De Marées
J. Forsting
M. Rohm
M. Tegenthoff
T. Schmidt-Wilcke
M. Vorgerd
Publikationsdatum
17.12.2018
Verlag
Springer Berlin Heidelberg
Erschienen in
European Radiology / Ausgabe 6/2019
Print ISSN: 0938-7994
Elektronische ISSN: 1432-1084
DOI
https://doi.org/10.1007/s00330-018-5885-1

Weitere Artikel der Ausgabe 6/2019

European Radiology 6/2019 Zur Ausgabe

Update Radiologie

Bestellen Sie unseren Fach-Newsletter und bleiben Sie gut informiert.