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Review

Diagnostic challenges in metabolic myopathies

, , &
Pages 1287-1298 | Received 25 Jun 2020, Accepted 16 Sep 2020, Published online: 04 Oct 2020

References

  • Finsterer J. An update on diagnosis and therapy of metabolic myopathies. Expert Rev Neurother. 2018;18:933–943.
  • Rubegni A, Malandrini A, Dosi C, et al. Next-generation sequencing approach to hyperCKemia: a 2-year cohort study. Neurology Gene. 2019;5:1–12.
  • Lollert A, Stihl C, Hötker AM, et al. Quantification of intramuscular fat in patients with late-onset Pompe disease by conventional magnetic resonance imaging for the long-term follow-up of enzyme replacement therapy. PLoS One. 2018;13:1–15.
  • Godfrey R, Quinlivan R. Skeletal muscle disorders of glycogenolysis and glycolysis. Nat Rev Neurol. 2016;12:393–402.
  • Tang H, Feuchtbaum L, Sciortino S, et al. The first year experience of newborn screening for pompe disease in California. Int J Neonatal Screen. 2020;6:9.
  • Angelini C, Semplicini C. Metabolic myopathies: the challenge of new treatments. Curr Opin Pharmacol. 2010;10:338–345.
  • van der Ploeg AT, Kruijshaar ME, Toscano A, et al. European consensus for starting and stopping enzyme replacement therapy in adult patients with Pompe disease: a 10-year experience. Eur J Neurol. 2017;24:768–e31.
  • Angelini C, Semplicini C, Ravaglia S, et al. Observational clinical study in juvenile-adult glycogenosis type 2 patients undergoing enzyme replacement therapy for up to 4 years. J Neurol. 2012;259:952–958.
  • Angelini C, Semplicini C, Ravaglia S, et al. New motor outcome function measures in evaluation of Late-Onset Pompe disease before and after enzyme replacement therapy. Muscle Nerve. 2012;45:831–834.
  • Nascimbeni AC, Fanin M, Tasca E, et al. Molecular pathology and enzyme processing in various phenotypes of acid maltase deficiency. Neurology. 2008;70:617–626.
  • Bergsma AJ, In ’T Groen SLM, van den Dorpel JJA, et al. A genetic modifier of symptom onset in Pompe disease. EBioMedicine. 2019;43:553–561.
  • Nascimbeni AC, Fanin M, Masiero E, et al. The role of autophagy in the pathogenesis of glycogen storage disease type II (GSDII). Cell Death Diff. 2012;19:1698–1708.
  • Nascimbeni AC, Fanin M, Tasca E, et al. Impaired autophagy affects acid α-glucosidase processing and enzyme replacement therapy efficacy in late-onset glycogen storage disease type II. Neuropathol Appl Neurobiol. 2015;41:672–675.
  • Cenacchi G, Papa V, Pegoraro V, et al. Review: danon disease: review of natural history and recent advances. Neuropathol Appl Neurobiol. 2020;46:303–322.
  • Milan G, Romanello V, Pescatore F, et al. Regulation of autophagy and the ubiquitin-proteasome system by the FoxO transcriptional network during muscle atrophy. Nat Commun. 2015;6:1–14.
  • Medina DL, Di Paola S, Peluso I, et al. Lysosomal calcium signalling regulates autophagy through calcineurin and TFEB. Nat Cell Biol. 2015;17:288–299.
  • Nascimbeni AC, Fanin M, Angelini C, et al. Autophagy dysregulation in Danon disease. Cell Death Disease. 2017;8:e2565.
  • Toscano A, Rodolico C, Musumeci O. Multisystem late onset Pompe disease (LOPD): an update on clinical aspects. Ann Translat Med. 2019;7:284.
  • Korlimarla A, Lim J-A, Kishnani PS, et al. An emerging phenotype of central nervous system involvement in Pompe disease: from bench to bedside and beyond. Ann Translat Med. 2019;7:289.
  • Haller RG, Wyrick P, Taivassalo T, et al. Aerobic conditioning: an effective therapy in McArdle’s disease. Ann Neurol. 2006;59:922–928.
  • Vasiljevski ER, Summers MA, Little DG, et al. Lipid storage myopathies: current treatments and future directions. Progress Lipid Res. 2018;72:1–17.
  • Angelini C. Molecular update and therapeutic trials in muscle disorders of glycogen and lipid metabolism. Paediatria Croatica. 2003;47:61–67.
  • Dimauro S, Dimauro PMM. Muscle carnitine palmityltransferase deficiency and myoglobinuria. Science. 1973;182:929–931.
  • Engel AG, Angelini C. Carnitine deficiency of human skeletal muscle with associated lipid storage myopathy: a new syndrome. Science. 1973;179:899–902.
  • Chapoy PR, Angelini C, Brown WJ, et al. Systemic carnitine deficiency — a treatable inherited lipid-storage disease presenting as Reye’s syndrome. N Engl J Med. 1980;303:1389–1394.
  • Tang NLS, Ganapathy V, Wu X, et al. Mutations of OCTN2, an organic cation/carnitine transporter, lead to deficient cellular carnitine uptake in primary carnitine deficiency. Hum Mol Genet. 1999;8:655–660.
  • Schulze A, Lindner M, Kohlmüller D, et al. Expanded newborn screening for inborn errors of metabolism by electrospray ionization-tandem mass spectrometry: results, outcome, and implications. Pediatrics. 2003;111:1399–1406.
  • Gempel K, Topaloglu H, Talim B, et al. The myopathic form of coenzyme Q10 deficiency is caused by mutations in the electron-transferring-flavoprotein dehydrogenase (ETFDH) gene. Brain. 2007;130:2037–2044.
  • Pennisi E, Garibaldi M, Antonini G. Lipid Myopathies. J Clin Med. 2018;7:472.
  • Dorfman ML, Hershko C, Eisenberg S, et al. Ichthyosiform dermatosis with systemic lipidosis. Arch Dermatol. 1974;110:261–266.
  • Chanarin I, Patel A, Slavin G, et al. Neutral-lipid storage disease: a new disorder of lipid metabolism. Br Med J. 1975;1:553–555.
  • Angelini C, Philippart M, Borrone C, et al. Multisystem triglyceride storage disorder with impaired long-chain fatty acid oxidation. Ann Neurol. 1980;7:5–10.
  • Tavian D, Colombo R. Improved cytochemical method for detecting Jordans’ bodies in neutral lipid storage diseases. J Clin Pathol. 2007;60:956–958.
  • Missaglia S, Coleman R, Mordente A, et al. Neutral lipid storage diseases as cellular model to study lipid droplet function. Cells. 2019;8:187.
  • Durdu M, Missaglia S, Moro L, et al. Clinical and genetic characterization of a Chanarin Dorfman Syndrome patient born to diseased parents. BMC Med Gene. 2018;19:88.
  • Redaelli C, Coleman RA, Moro L, et al. Clinical and genetic characterization of chanarin-dorfman syndrome patients: first report of large deletions in the ABHD5 gene. Orphanet J Rare Diseases. 2010;5:33.
  • Gupta N, Gothwal S, Satpathy AK, et al. Chanarin Dorfman syndrome: a case report with novel nonsense mutation. Gene. 2016;575:359–362.
  • Goetzman ES. Advances in the understanding and treatment of mitochondrial fatty acid oxidation disorders. Current Genetic Medicine Reports. 2017;5:132–142.
  • Madsen KL, Preisler N, Orngreen MC, et al. Patients with medium-chain acyl-coenzyme a dehydrogenase deficiency have impaired oxidation of fat during exercise but no effect of L-Carnitine supplementation. J Clin Endocrinol Metabol. 2013;98:1667–1675.
  • Ørngreen MC, Vissing J, Laforét P. No effect of bezafibrate in patients with CPTII and VLCAD deficiencies. J Inherit Metabol Disease. 2015;38:373–374.
  • El-Gharbawy A, Vockley J. Inborn errors of metabolism with myopathy: defects of fatty acid oxidation and the carnitine shuttle system. Pediatr Clin North Am. 2018;65:317–335.
  • Magoulas PL, El-Hattab AW. Systemic primary carnitine deficiency: an overview of clinical manifestations, diagnosis, and management. Orphanet J Rare Diseases. 2012;7:68.
  • Nezu JI, Tamai I, Oku A, et al. Primary systemic carnitine deficiency is caused by mutations in a gene encoding sodium ion-dependent carnitine transporter. Nature Genet. 1999;21:91–94.
  • Tein I, De Vivo DC, Bierman F, et al. Impaired skin fibroblast carnitine uptake in primary systemic carnitine deficiency manifested by childhood carnitine-responsive cardiomyopathy. Pediat Res. 1990;28:247–255.
  • Amat C, Filippo S, Longo N. Tyrosine residues affecting sodium stimulation of carnitine transport in the OCTN2 carnitine/organic cation transporter. J Biol Chem. 2003;279:7247–7253.
  • Inano A, Sai Y, Kato Y, et al. Functional regions of organic cation/carnitine transporter OCTN2 (SLC22A5): roles in carnitine recognition. Drug Metabol Pharmacokinetics. 2004;19:180–189.
  • Filippo CA Di S, Ardon O, Longo N. Glycosylation of the OCTN2 carnitine transporter: study of natural mutations identified in patients with primary carnitine deficiency. Biochimica Et Biophysica Acta - Mol Basis Disease. 2011;1812:312–320.
  • Longo N, Frigeni M, Pasquali M. Carnitine transport and fatty acid oxidation. Biochimica Et Biophysica Acta - Mol Cell Res. 2016;1863:2422–2435.
  • Missaglia S, Tavian D, Moro L, et al. Characterization of two ETFDH mutations in a novel case of riboflavin-responsive multiple acyl-CoA dehydrogenase deficiency. Lipids Health Disease. 2018;17:254.
  • Zhang J, Frerman FE, Kim JJP. Structure of electron transfer flavoprotein-ubiquinone oxidoreductase and electron transfer to the mitochondrial ubiquinone pool. Proc Natl Acad Sci USA. 2006;103:16212–16217.
  • Watmough NJ, Frerman FE. The electron transfer flavoprotein: ubiquinone oxidoreductases. Biochimica et Biophysica Acta - Bioenergetics. 2010;1797:1910–1916.
  • J. Henriques B, K. Olsen R, Bross P, et al. Emerging roles for riboflavin in functional rescue of mitochondrial β-oxidation flavoenzymes. Curr Med Chem. 2010;17:3842–3854.
  • Olsen RKJ, Andresen BS, Christensen E, et al. Clear relationship between ETF/ETFDH genotype and phenotype in patients with multiple acyl-CoA dehydrogenation deficiency. Human Mutat. 2003;22:12–23.
  • Angle B, Burton BK. Risk of sudden death and acute life-threatening events in patients with glutaric acidemia type II. Mol Gene Metabol. 2008;93:36–39.
  • Pollard LM, Williams NR, Espinoza L, et al. Diagnosis, treatment, and long-term outcomes of late-onset (Type III) multiple Acyl-CoA dehydrogenase deficiency. J Child Neurol. 2010;25:954–960.
  • Mosegaard S, Bruun GH, Flyvbjerg KF, et al. An intronic variation in SLC52A1 causes exon skipping and transient riboflavin-responsive multiple acyl-CoA dehydrogenation deficiency. Mol Gene Metabol. 2017;122:182–188.
  • Olsen RKJ, Koňaříková E, Giancaspero TA, et al. Riboflavin-responsive and -non-responsive mutations in FAD synthase cause multiple Acyl-CoA dehydrogenase and combined respiratory-chain deficiency. Am J Hum Genet. 2016;98:1130–1145.
  • Grünert SC. Clinical and genetical heterogeneity of late-onset multiple acyl-coenzyme A dehydrogenase deficiency. Orphanet J Rare Diseases. 2014;9:117.
  • Wang Z, Hong D, Zhang W, et al. Severe sensory neuropathy in patients with adult-onset multiple acyl-CoA dehydrogenase deficiency. Neuro Disord. 2016;26:170–175.
  • Angelini C, Tavian D, Missaglia S. Heterogeneous phenotypes in lipid storage myopathy due to ETFDH gene mutations. JIMD Rep. 2018;38:33–40.
  • Zhao YW, Liu XJ, Zhang W, et al. Muscle magnetic resonance imaging for the differentiation of multiple Acyl-CoA dehydrogenase deficiency and immune-mediated necrotizing myopathy. Chinese Med J. 2018;131:144–150.
  • Cornelius N, Frerman FE, Corydon TJ, et al. Molecular mechanisms of riboflavin responsiveness in patients with ETF-QO variations and multiple acyl-CoA dehydrogenation deficiency. Hum Mol Genet. 2012;21:3435–3448.
  • Er TK, Chen CC, Liu YY, et al. Computational analysis of a novel mutation in ETFDH gene highlights its long-range effects on the FAD-binding motif. BMC Struct Biol. 2011;11:43.
  • Xue Y, Zhou Y, Zhang K, et al. Compound heterozygous mutations in electron transfer flavoprotein dehydrogenase identified in a young Chinese woman with late-onset glutaric aciduria type II. Lipids Health Disease. 2017;16:185.
  • Martín MA, Rubio JC, Del Hoyo P, et al. Identification of novel mutations in Spanish patients with muscle carnitine palmitoyltransferase II deficiency. Human Mutation. 2000;15:579–580.
  • Bonnefont JP, Djouadi F, Prip-Buus C, et al. Carnitine palmitoyltransferases 1 and 2: biochemical, molecular and medical aspects. Mol Aspect Med. 2004;25:495–520.
  • Isackson PJ, Bennett MJ, Vladutiu GD. Identification of 16 new disease-causing mutations in the CPT2 gene resulting in carnitine palmitoyltransferase II deficiency. Mol Gene Metabol. 2006;89:323–331.
  • Corti S, Bordoni A, Ronchi D, et al. Clinical features and new molecular findings in Carnitine Palmitoyltransferase II (CPT II) deficiency. J Neurolog Sci. 2008;266:97–103.
  • Fanin M, Anichini A, Cassandrini D, et al. Allelic and phenotypic heterogeneity in 49 Italian patients with the muscle form of CPT-II deficiency. Clin Genet. 2012;82:232–239.
  • Lehmann D, Motlagh L, Robaa D, et al. Muscle carnitine palmitoyltransferase ii deficiency: a review of enzymatic controversy and clinical features. Int J Mol Sci. 2017;18:82.
  • Vladutiu GD, Saponara I, Conroy JM, et al. Immunoquantitation of carnitine palmitoyl transferase in skeletal muscle of 31 patients. Neuro Disord. 1992;2:249–259.
  • Angelini C, Federico A, Reichmann H, et al. Fatty acid mitochondrial disorders. In: European handbook of neurological management. 2nd ed. Wiley-Blackwell; 2010. p. 501–511.
  • Gempel K, Kiechl S, Hofmann S, et al. Screening for carnitine palmitoyltransferase II deficiency by tandem mass spectrometry. J Inherit Metabol Disease. 2002;25:17–27.
  • Rizos I. Three-year survival of patients with heart failure caused by dilated cardiomyopathy and L-carnitine administration. Am Heart J. 2000;139:S120–S123.
  • Longo N, Amat Di San Filippo C, Pasquali M. Disorders of carnitine transport and the carnitine cycle. Am J Med Genet A. 2006;142:C:77–85.
  • Agnetti A, Bitton L, Tchana B, et al. Primary carnitine deficiency dilated cardiomyopathy: 28 years follow-up. Int J Cardiol. 2013;162:e34–35.
  • Fu H, Liu X, Wang Z, et al. Significant clinical heterogeneity with similar ETFDH genotype in three Chinese patients with late-onset multiple acyl-CoA dehydrogenase deficiency. Neurol Sci. 2016;37:1099–1105.
  • Liu XY, Wang ZQ, Wang DN, et al. A historical cohort study on the efficacy of glucocorticoids and riboflavin among patients with late-onset multiple Acyl-CoA dehydrogenase deficiency. Chinese Med J. 2016;129:142–146.
  • Fan X, Xie B, Zou J, et al. Novel ETFDH mutations in four cases of riboflavin responsive multiple acyl-CoA dehydrogenase deficiency. Mol Gene Metabol Rep. 2018;16:15–19.
  • Xi J, Wen B, Lin J, et al. Clinical features and ETFDH mutation spectrum in a cohort of 90 chinese patients with late-onset multiple acyl-CoA dehydrogenase deficiency. J Inherit Metabol Disease. 2014;37:399–404.
  • Olsen RKJ, Pourfarzam M, Morris AAM, et al. Lipid-storage myopathy and respiratory insufficiency due to ETFQO mutations in a patient with late-onset multiple acyl-CoA dehydrogenation deficiency. J Inherit Metabol Disease. 2004;27:671–678.
  • Whitaker CH, Felice KJ, Silvers D, et al. Fulminant lipid storage myopathy due to multiple acyl-coenzyme a dehydrogenase deficiency. Muscle Nerve. 2015;52:289–293.
  • Laforêt P, Vianey-Saban C. Disorders of muscle lipid metabolism: diagnostic and therapeutic challenges. Neuro Disord. 2010;20:693–700.
  • Wilson JMG, Jungner G. Principles and practice of screening for disease. Boletìn de la Oficina Sanitaria Panam. 1968;65:281–393.
  • Ross LF, Clarke AJ. A historical and current review of newborn screening for neuromuscular disorders from around the world: lessons for the United States. Pediatr Neurol. 2017;77:12–22.
  • Burlina AB, Polo G, Salviati L, et al. Newborn screening for lysosomal storage disorders by tandem mass spectrometry in North East Italy. J Inherit Metabol Disease. 2018;41:209–219.
  • Pegoraro V, Missaglia S, Marozzo R, et al. MiRNAs as biomarkers of phenotype in neutral lipid storage disease with myopathy. Muscle Nerve. 2020;61:253–257.
  • Missaglia S, Pegoraro V, Marozzo R, et al. Correlation between ETFDH mutations and dysregulation of serum myomiRs in MADD patients. Eur J Trans Myol. 2020;30:20–25.
  • Savarese M, Torella A, Musumeci O, et al. Targeted gene panel screening is an effective tool to identify undiagnosed late onset Pompe disease. Neuro Disord. 2018;28:586–591.
  • Schoser B. Pompe disease: what are we missing? Ann Translat Med. 2019;7:292.
  • Ronzitti G, Collaud F, Laforet P, et al. Progress and challenges of gene therapy for Pompe disease. Ann Translat Med. 2019;7:287.
  • Corti M, Elder ME, Falk DJ, et al. B-cell depletion is protective against anti-AAV capsid immune response: a human subject case study. Mol Therap Method Clin Develop. 2014;1:14033.
  • Ricci G, Baldanzi S, Seidita F, et al. A mobile app for patients with Pompe disease and its possible clinical applications. Neuro Disord. 2018;28:471–475.
  • Ørngreen MC, Ejstrup R, Vissing J. Effect of diet on exercise tolerance in carnitine palmitoyltransferase II deficiency. Neurology. 2003;61:559–561.

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