Top

Journal of Neurology

Published in:

Open Access 01-08-2020 | Magnetic Resonance Imaging | Original Communication

Whole-body muscle MRI of patients with MATR3-associated distal myopathy reveals a distinct pattern of muscular involvement and highlights the value of whole-body examination

Authors: Alexander Mensch, Torsten Kraya, Felicitas Koester, Tobias Müller, Dietrich Stoevesandt, Stephan Zierz

Published in: Journal of Neurology | Issue 8/2020

Abstract

Objective

MATR3-associated distal myopathy is a rare distal myopathy predominantly affecting lower legs as well as wrist- and finger extensors. Whilst most distal myopathies are clinically and genetically well characterized, diagnosis often remains challenging. Pattern-based magnetic resonance imaging (MRI) approaches offer valuable additional information. However, a consistent pattern of muscular affection is missing for most distal myopathies. Thus, the aim of the present study was to establish a disease-specific pattern of muscular involvement in MATR3-associated distal myopathy using whole-body MRI.

Methods

15 patients (25–79 years of age, 7 female) with MATR3-associated distal myopathy were subjected to whole-body MRI. The grade of fatty involution for individual muscles was determined using Fischer-Grading. Results were compared to established MRI-patterns of other distal myopathies.

Results

There was a predominant affection of the distal lower extremities. Lower legs showed a severe fatty infiltration, prominently affecting gastrocnemius and soleus muscle. In thighs, a preferential involvement of semimembranous and biceps femoris muscle was observed. Severe affection of gluteus minimus muscle as well as axial musculature, mainly affecting the thoracic segments, was seen. A sufficient discrimination to other forms of distal myopathy based solely on MRI-findings of the lower extremities was not possible. However, the inclusion of additional body parts seemed to yield specificity.

Interpretation

Muscle MRI of patients with MATR3-associated distal myopathy revealed a distinct pattern of muscular involvement. The usage of whole-body muscle MRI provided valuable additional findings as compared to regular MRI of the lower extremities to improve distinction from other disease entities.

Available only for authorised users

Udd B (2014) Distal myopathies. Curr Neurol Neurosci Rep 14(3):434. https://doi.org/10.1007/s11910-013-0434-4 CrossRefPubMed

Udd B (2012) Distal myopathies–new genetic entities expand diagnostic challenge. Neuromuscul Disord 22(1):5–12. https://doi.org/10.1016/j.nmd.2011.10.003 CrossRefPubMed

Leung DG (2017) Magnetic resonance imaging patterns of muscle involvement in genetic muscle diseases: a systematic review. J Neurol 264(7):1320–1333. https://doi.org/10.1007/s00415-016-8350-6 CrossRefPubMed

Ahlberg G, Jakobsson F, Fransson A, Moritz A, Borg K, Edstrom L (1994) Distribution of muscle degeneration in Welander distal myopathy–a magnetic resonance imaging and muscle biopsy study. Neuromuscul Disord 4(1):55–62. https://doi.org/10.1016/0960-8966(94)90048-5 CrossRefPubMed

Berciano J, Gallardo E, Dominguez-Perles R, Gallardo E, Garcia A, Garcia-Barredo R, Combarros O, Infante J, Illa I (2008) Autosomal-dominant distal myopathy with a myotilin S55F mutation: sorting out the phenotype. J Neurol Neurosurg Psychiatr 79(2):205–208. https://doi.org/10.1136/jnnp.2007.125435 CrossRef

Bucelli RC, Arhzaouy K, Pestronk A, Pittman SK, Rojas L, Sue CM, Evila A, Hackman P, Udd B, Harms MB, Weihl CC (2015) SQSTM1 splice site mutation in distal myopathy with rimmed vacuoles. Neurology 85(8):665–674. https://doi.org/10.1212/WNL.0000000000001864 CrossRefPubMedPubMedCentral

Cirak S, von Deimling F, Sachdev S, Errington WJ, Herrmann R, Bonnemann C, Brockmann K, Hinderlich S, Lindner TH, Steinbrecher A, Hoffmann K, Prive GG, Hannink M, Nurnberg P, Voit T (2010) Kelch-like homologue 9 mutation is associated with an early onset autosomal dominant distal myopathy. Brain 133(Pt 7):2123–2135. https://doi.org/10.1093/brain/awq108 CrossRefPubMedPubMedCentral

Diaz-Manera J, Fernandez-Torron R, LLauger J, James MK, Mayhew A, Smith FE, Moore UR, Blamire AM, Carlier PG, Rufibach L, Mittal P, Eagle M, Jacobs M, Hodgson T, Wallace D, Ward L, Smith M, Stramare R, Rampado A, Sato N, Tamaru T, Harwick B, Rico Gala S, Turk S, Coppenrath EM, Foster G, Bendahan D, Le Fur Y, Fricke ST, Otero H, Foster SL, Peduto A, Sawyer AM, Hilsden H, Lochmuller H, Grieben U, Spuler S, Tesi Rocha C, Day JW, Jones KJ, Bharucha-Goebel DX, Salort-Campana E, Harms M, Pestronk A, Krause S, Schreiber-Katz O, Walter MC, Paradas C, Hogrel JY, Stojkovic T, Takeda S, Mori-Yoshimura M, Bravver E, Sparks S, Bello L, Semplicini C, Pegoraro E, Mendell JR, Bushby K, Straub V, Jain COSC (2018) Muscle MRI in patients with dysferlinopathy: pattern recognition and implications for clinical trials. J Neurol Neurosurg Psychiatr 89(10):1071–1081. https://doi.org/10.1136/jnnp-2017-317488 CrossRef

Evila A, Palmio J, Vihola A, Savarese M, Tasca G, Penttila S, Lehtinen S, Jonson PH, De Bleecker J, Rainer P, Auer-Grumbach M, Pouget J, Salort-Campana E, Vilchez JJ, Muelas N, Olive M, Hackman P, Udd B (2017) Targeted next-generation sequencing reveals novel TTN mutations causing recessive distal titinopathy. Mol Neurobiol 54(9):7212–7223. https://doi.org/10.1007/s12035-016-0242-3 CrossRefPubMed

10.

Fischer D, Kley RA, Strach K, Meyer C, Sommer T, Eger K, Rolfs A, Meyer W, Pou A, Pradas J, Heyer CM, Grossmann A, Huebner A, Kress W, Reimann J, Schroder R, Eymard B, Fardeau M, Udd B, Goldfarb L, Vorgerd M, Olive M (2008) Distinct muscle imaging patterns in myofibrillar myopathies. Neurology 71(10):758–765. https://doi.org/10.1212/01.wnl.0000324927.28817.9b CrossRefPubMedPubMedCentral

11.

Kesper K, Kornblum C, Reimann J, Lutterbey G, Schroder R, Wattjes MP (2009) Pattern of skeletal muscle involvement in primary dysferlinopathies: a whole-body 3.0-T magnetic resonance imaging study. Acta Neurol Scand 120(2):111–118. https://doi.org/10.1111/j.1600-0404.2008.01129.x CrossRefPubMed

12.

Lee Y, Jonson PH, Sarparanta J, Palmio J, Sarkar M, Vihola A, Evila A, Suominen T, Penttila S, Savarese M, Johari M, Minot MC, Hilton-Jones D, Maddison P, Chinnery P, Reimann J, Kornblum C, Kraya T, Zierz S, Sue C, Goebel H, Azfer A, Ralston SH, Hackman P, Bucelli RC, Taylor JP, Weihl CC, Udd B (2018) TIA1 variant drives myodegeneration in multisystem proteinopathy with SQSTM1 mutations. J Clin Invest 128(3):1164–1177. https://doi.org/10.1172/JCI97103 CrossRefPubMedPubMedCentral

13.

Mahjneh I, Bashir R, Kiuru-Enari S, Linssen W, Lamminen A, Visser M (2012) Selective pattern of muscle involvement seen in distal muscular dystrophy associated with anoctamin 5 mutations: a follow-up muscle MRI study. Neuromuscul Disord 22(2):S130–136. https://doi.org/10.1016/j.nmd.2012.02.007 CrossRefPubMed

14.

Mahjneh I, Lamminen AE, Udd B, Paetau AE, Hackman P, Korhola OA, Somer HV (2004) Muscle magnetic resonance imaging shows distinct diagnostic patterns in Welander and tibial muscular dystrophy. Acta Neurol Scand 110(2):87–93. https://doi.org/10.1111/j.1600-0404.2004.00283.x CrossRefPubMed

15.

McNeill A, Birchall D, Straub V, Goldfarb L, Reilich P, Walter MC, Schramm N, Lochmuller H, Chinnery PF (2009) Lower limb radiology of distal myopathy due to the S60F myotilin mutation. Eur Neurol 62(3):161–166. https://doi.org/10.1159/000227266 CrossRefPubMedPubMedCentral

16.

Niu Z, Pontifex CS, Berini S, Hamilton LE, Naddaf E, Wieben E, Aleff RA, Martens K, Gruber A, Engel AG, Pfeffer G, Milone M (2018) Myopathy with SQSTM1 and TIA1 variants: clinical and pathological features. Front Neurol 9:147. https://doi.org/10.3389/fneur.2018.00147 CrossRefPubMedPubMedCentral

17.

Ohlsson M, Hedberg C, Bradvik B, Lindberg C, Tajsharghi H, Danielsson O, Melberg A, Udd B, Martinsson T, Oldfors A (2012) Hereditary myopathy with early respiratory failure associated with a mutation in A-band titin. Brain 135(Pt 6):1682–1694. https://doi.org/10.1093/brain/aws103 CrossRefPubMed

18.

Olive M, Odgerel Z, Martinez A, Poza JJ, Bragado FG, Zabalza RJ, Jerico I, Gonzalez-Mera L, Shatunov A, Lee HS, Armstrong J, Maravi E, Arroyo MR, Pascual-Calvet J, Navarro C, Paradas C, Huerta M, Marquez F, Rivas EG, Pou A, Ferrer I, Goldfarb LG (2011) Clinical and myopathological evaluation of early- and late-onset subtypes of myofibrillar myopathy. Neuromuscul Disord 21(8):533–542. https://doi.org/10.1016/j.nmd.2011.05.002 CrossRefPubMedPubMedCentral

19.

Palmio J, Evila A, Chapon F, Tasca G, Xiang F, Bradvik B, Eymard B, Echaniz-Laguna A, Laporte J, Karppa M, Mahjneh I, Quinlivan R, Laforet P, Damian M, Berardo A, Taratuto AL, Bueri JA, Tommiska J, Raivio T, Tuerk M, Golitz P, Chevessier F, Sewry C, Norwood F, Hedberg C, Schroder R, Edstrom L, Oldfors A, Hackman P, Udd B (2014) Hereditary myopathy with early respiratory failure: occurrence in various populations. J Neurol Neurosurg Psychiatr 85(3):345–353. https://doi.org/10.1136/jnnp-2013-304965 CrossRef

20.

Palmio J, Leonard-Louis S, Sacconi S, Savarese M, Penttila S, Semmler AL, Kress W, Mozaffar T, Lai T, Stojkovic T, Berardo A, Reisin R, Attarian S, Urtizberea A, Cobo AM, Maggi L, Kurbatov S, Nikitin S, Milisenda JC, Fatehi F, Raimondi M, Silveira F, Hackman P, Claeys KG, Udd B (2019) Expanding the importance of HMERF titinopathy: new mutations and clinical aspects. J Neurol 266(3):680–690. https://doi.org/10.1007/s00415-019-09187-2 CrossRefPubMedPubMedCentral

21.

Park HJ, Hong YB, Choi YC, Lee J, Kim EJ, Lee JS, Mo WM, Ki SM, Kim HI, Kim HJ, Hyun YS, Hong HD, Nam K, Jung SC, Kim SB, Kim SH, Kim DH, Oh KW, Kim SH, Yoo JH, Lee JE, Chung KW, Choi BO (2016) ADSSL1 mutation relevant to autosomal recessive adolescent onset distal myopathy. Ann Neurol 79(2):231–243. https://doi.org/10.1002/ana.24550 CrossRefPubMed

22.

Park HJ, Shin HY, Kim S, Kim SH, Lee Y, Lee JH, Hong JM, Kim SM, Park KD, Choi BO, Lee JH, Choi YC (2017) Distal myopathy with ADSSL1 mutations in Korean patients. Neuromuscul Disord 27(5):465–472. https://doi.org/10.1016/j.nmd.2017.02.004 CrossRefPubMed

23.

Peric S, Glumac JN, Topf A, Savic-Pavicevic D, Phillips L, Johnson K, Cassop-Thompson M, Xu L, Bertoli M, Lek M, MacArthur D, Brkusanin M, Milenkovic S, Rasic VM, Banko B, Maksimovic R, Lochmuller H, Stojanovic VR, Straub V (2017) A novel recessive TTN founder variant is a common cause of distal myopathy in the Serbian population. Eur J Hum Genet 25(5):572–581. https://doi.org/10.1038/ejhg.2017.16 CrossRefPubMedPubMedCentral

24.

Pfeffer G, Elliott HR, Griffin H, Barresi R, Miller J, Marsh J, Evila A, Vihola A, Hackman P, Straub V, Dick DJ, Horvath R, Santibanez-Koref M, Udd B, Chinnery PF (2012) Titin mutation segregates with hereditary myopathy with early respiratory failure. Brain 135(Pt 6):1695–1713. https://doi.org/10.1093/brain/aws102 CrossRefPubMedPubMedCentral

25.

Schramm N, Born C, Weckbach S, Reilich P, Walter MC, Reiser MF (2008) Involvement patterns in myotilinopathy and desminopathy detected by a novel neuromuscular whole-body MRI protocol. Eur Radiol 18(12):2922–2936. https://doi.org/10.1007/s00330-008-1071-1 CrossRefPubMed

26.

Tasca G, Ricci E, Monforte M, Laschena F, Ottaviani P, Rodolico C, Barca E, Silvestri G, Iannaccone E, Mirabella M, Broccolini A (2012) Muscle imaging findings in GNE myopathy. J Neurol 259(7):1358–1365. https://doi.org/10.1007/s00415-011-6357-6 CrossRefPubMed

27.

Ten Dam L, van der Kooi AJ, Rovekamp F, Linssen WH, de Visser M (2014) Comparing clinical data and muscle imaging of DYSF and ANO5 related muscular dystrophies. Neuromuscul Disord 24(12):1097–1102. https://doi.org/10.1016/j.nmd.2014.07.004 CrossRefPubMed

28.

Bugiardini E, Morrow JM, Shah S, Wood CL, Lynch DS, Pitmann AM, Reilly MM, Houlden H, Matthews E, Parton M, Hanna MG, Straub V, Yousry TA (2018) The diagnostic value of MRI pattern recognition in distal myopathies. Front Neurol 9:456. https://doi.org/10.3389/fneur.2018.00456 CrossRefPubMedPubMedCentral

29.

Muller TJ, Kraya T, Stoltenburg-Didinger G, Hanisch F, Kornhuber M, Stoevesandt D, Senderek J, Weis J, Baum P, Deschauer M, Zierz S (2014) Phenotype of matrin-3-related distal myopathy in 16 German patients. Ann Neurol 76(5):669–680. https://doi.org/10.1002/ana.24255 CrossRefPubMed

30.

Kraya T, Schmidt B, Muller T, Hanisch F (2015) Impairment of respiratory function in late-onset distal myopathy due to MATR3 mutation. Muscle Nerve 51(6):916–918. https://doi.org/10.1002/mus.24603 CrossRefPubMed

31.

Barp A, Malfatti E, Metay C, Jobic V, Carlier RY, Laforet P (2018) The first French case of MATR3-related distal myopathy: Clinical, radiological and histopathological characterization. Rev Neurol (Paris). https://doi.org/10.1016/j.neurol.2017.08.004 CrossRef

32.

Feit H, Silbergleit A, Schneider LB, Gutierrez JA, Fitoussi RP, Reyes C, Rouleau GA, Brais B, Jackson CE, Beckmann JS, Seboun E (1998) Vocal cord and pharyngeal weakness with autosomal dominant distal myopathy: clinical description and gene localization to 5q31. Am J Hum Genet 63(6):1732–1742. https://doi.org/10.1086/302166 CrossRefPubMedPubMedCentral

33.

Palmio J, Evila A, Bashir A, Norwood F, Viitaniemi K, Vihola A, Huovinen S, Straub V, Hackman P, Hirano M, Bushby K, Udd B (2016) Re-evaluation of the phenotype caused by the common MATR3 p.Ser85Cys mutation in a new family. J Neurol Neurosurg Psychiatr 87(4):448–450. https://doi.org/10.1136/jnnp-2014-309349 CrossRef

34.

Senderek J, Garvey SM, Krieger M, Guergueltcheva V, Urtizberea A, Roos A, Elbracht M, Stendel C, Tournev I, Mihailova V, Feit H, Tramonte J, Hedera P, Crooks K, Bergmann C, Rudnik-Schoneborn S, Zerres K, Lochmuller H, Seboun E, Weis J, Beckmann JS, Hauser MA, Jackson CE (2009) Autosomal-dominant distal myopathy associated with a recurrent missense mutation in the gene encoding the nuclear matrix protein, matrin 3. Am J Hum Genet 84(4):511–518. https://doi.org/10.1016/j.ajhg.2009.03.006 CrossRefPubMedPubMedCentral

35.

Yamashita S, Mori A, Nishida Y, Kurisaki R, Tawara N, Nishikami T, Misumi Y, Ueyama H, Imamura S, Higuchi Y, Hashiguchi A, Higuchi I, Morishita S, Yoshimura J, Uchino M, Takashima H, Tsuji S, Ando Y (2015) Clinicopathological features of the first Asian family having vocal cord and pharyngeal weakness with distal myopathy due to a MATR3 mutation. Neuropathol Appl Neurobiol 41(3):391–398. https://doi.org/10.1111/nan.12179 CrossRefPubMed

36.

Khaleeli AA, Edwards RH, Gohil K, McPhail G, Rennie MJ, Round J, Ross EJ (1983) Corticosteroid myopathy: a clinical and pathological study. Clin Endocrinol (Oxf) 18(2):155–166. https://doi.org/10.1111/j.1365-2265.1983.tb03198.x CrossRef

37.

May DA, Disler DG, Jones EA, Balkissoon AA, Manaster BJ (2000) Abnormal signal intensity in skeletal muscle at MR imaging: patterns, pearls, and pitfalls. Radiographics 20:S295–315. https://doi.org/10.1148/radiographics.20.suppl_1.g00oc18s295 CrossRefPubMed

38.

Burian E, Syvari J, Holzapfel C, Drabsch T, Kirschke JS, Rummeny EJ, Zimmer C, Hauner H, Karampinos DC, Baum T, Franz D (2018) Gender- and age-related changes in trunk muscle composition using chemical shift encoding-based water(-)fat MRI. Nutrients 10(12):1972. https://doi.org/10.3390/nu10121972 CrossRefPubMedCentral

39.

Yin L, Xie ZY, Xu HY, Zheng SS, Wang ZX, Xiao JX, Yuan Y (2019) T2 Mapping and fat quantification of thigh muscles in children with Duchenne muscular dystrophy. Curr Med Sci 39(1):138–145. https://doi.org/10.1007/s11596-019-2012-8 CrossRefPubMed

40.

Chardon JW, Diaz-Manera J, Tasca G, Bonnemann CG, Gomez-Andres D, Heerschap A, Mercuri E, Muntoni F, Pichiecchio A, Ricci E, Walter MC, Hanna M, Jungbluth H, Morrow JM, Fernandez-Torron R, Udd B, Vissing J, Yousry T, Quijano-Roy S, Straub V, Carlier RY, Group M-MW (2019) MYO-MRI diagnostic protocols in genetic myopathies. Neuromuscul Disord 29(11):827–841. https://doi.org/10.1016/j.nmd.2019.08.011 CrossRef

41.

Penisson-Besnier I, Dumez C, Chateau D, Dubas F, Fardeau M (1998) Autosomal dominant late adult onset distal leg myopathy. Neuromuscul Disord 8(7):459–466. https://doi.org/10.1016/s0960-8966(98)00063-7 CrossRefPubMed

42.

Penisson-Besnier I, Talvinen K, Dumez C, Vihola A, Dubas F, Fardeau M, Hackman P, Carpen O, Udd B (2006) Myotilinopathy in a family with late onset myopathy. Neuromuscul Disord 16(7):427–431. https://doi.org/10.1016/j.nmd.2006.04.009 CrossRefPubMed

43.

Selcen D, Engel AG (2004) Mutations in myotilin cause myofibrillar myopathy. Neurology 62(8):1363–1371. https://doi.org/10.1212/01.wnl.0000123576.74801.75 CrossRefPubMed

44.

Lindberg C, Borg K, Edstrom L, Hedstrom A, Oldfors A (1991) Inclusion body myositis and Welander distal myopathy: a clinical, neurophysiological and morphological comparison. J Neurol Sci 103(1):76–81. https://doi.org/10.1016/0022-510x(91)90287-h CrossRefPubMed

45.

von Tell D, Somer H, Udd B, Edstrom L, Borg K, Ahlberg G (2002) Welander distal myopathy outside the Swedish population: phenotype and genotype. Neuromuscul Disord 12(6):544–547. https://doi.org/10.1016/s0960-8966(01)00338-8 CrossRef

46.

Udd B, Partanen J, Halonen P, Falck B, Hakamies L, Heikkila H, Ingo S, Kalimo H, Kaariainen H, Laulumaa V et al (1993) Tibial muscular dystrophy. Late adult-onset distal myopathy in 66 Finnish patients. Arch Neurol 50(6):604–608. https://doi.org/10.1001/archneur.1993.00540060044015 CrossRefPubMed

Title: Whole-body muscle MRI of patients with MATR3-associated distal myopathy reveals a distinct pattern of muscular involvement and highlights the value of whole-body examination
Authors: Alexander Mensch
Torsten Kraya
Felicitas Koester
Tobias Müller
Dietrich Stoevesandt
Stephan Zierz
Publication date: 01-08-2020
Publisher: Springer Berlin Heidelberg
Keywords: Magnetic Resonance Imaging
Magnetic Resonance Imaging
Diseases of the neuromuscular synapses and muscles
Myopathy
Published in: Journal of Neurology / Issue 8/2020
Print ISSN: 0340-5354
Electronic ISSN: 1432-1459
DOI: https://doi.org/10.1007/s00415-020-09862-9

At a glance: The ONWARDS insulin icodec trials

Springer Medicine

Whole-body muscle MRI of patients with MATR3-associated distal myopathy reveals a distinct pattern of muscular involvement and highlights the value of whole-body examination

Abstract

Objective

Methods

Results

Interpretation

At a glance: The ONWARDS insulin icodec trials

Springer Medicine

Abstract

Objective

Methods

Results

Interpretation

Please log in to get access to this content

Other articles of this Issue 8/2020

Neural mechanisms underlying state mental fatigue in multiple sclerosis: a pilot study

Etiologic distribution of dizziness and vertigo in a referral-based dizziness clinic in South Korea

Light therapy for multiple sclerosis-associated fatigue: a randomized, controlled phase II trial

Longitudinal serum neurofilament light chain (sNfL) concentration relates to cognitive function in multiple sclerosis patients

Cortical myoclonus and epilepsy in a family with a new SLC20A2 mutation

Treatment expectations and patient-reported outcomes of nusinersen therapy in adult spinal muscular atrophy