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Erschienen in:

02.05.2023 | Original Communication

Muscle MRI patterns for limb girdle muscle dystrophies: systematic review

verfasst von: Issa Alawneh, Ana Stosic, Hernan Gonorazky

Erschienen in: Journal of Neurology | Ausgabe 8/2023

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Abstract

Limb girdle muscle dystrophies (LGMDs) are a group of inherited neuromuscular disorders comprising more than 20 genes. There have been increasing efforts to characterize this group with Muscle MRI. However, due to the complexity and similarities, the interpretation of the MRI patterns is usually done by experts in the field. Here, we proposed a step-by-step image interpretation of Muscle MRI in LGDM by evaluating the variability of muscle pattern involvement reported in the literature. A systematic review with an open start date to November 2022 was conducted to describe all LGMDs’ muscle MRI patterns. Eighty-eight studies were included in the final review. Data were found to describe muscle MRI patterns for 15 out of 17 LGMDs types. Although the diagnosis of LGMDs is challenging despite the advanced genetic testing and other diagnostic modalities, muscle MRI is shown to help in the diagnosis of LGMDs. To further increase the yield for muscle MRI in the neuromuscular field, larger cohorts of patients need to be conducted.

Bockhorst J, Wicklund M (2020) Limb girdle muscular dystrophies. Neurol Clin 38(3):493–504CrossRefPubMed

Van De Vlekkert J et al (2015) Combining MRI and muscle biopsy improves diagnostic accuracy in subacute-onset idiopathic inflammatory myopathy. Muscle Nerve 51(2):253–258CrossRefPubMed

Theodorou DJ, Theodorou SJ, Kakitsubata Y (2012) Skeletal muscle disease: patterns of MRI appearances. Br J Radiol 85(1020):e1298–e1308CrossRefPubMedPubMedCentral

Moher D et al (2015) Preferred reporting items for systematic review and meta-analysis protocols (PRISMA-P) 2015 statement. Syst Rev 4(1):1CrossRefPubMedPubMedCentral

Mercuri E, Talim B, Moghadaszadeh B, Petit N, Brockington M, Counsell S et al (2002) Clinical and imaging findings in six cases of congenital muscular dystrophy with rigid spine syndrome linked to chromosome 1p (RSMD1). Neuromuscul Disord 12(7–8):631–638CrossRefPubMed

Mercuri E, Bushby K, Ricci E, Birchall D, Pane M, Kinali M, Allsop J, Nigro V, Sáenz A, Nascimbeni A, Fulizio L, Angelini C, Muntoni F (2005) Muscle MRI findings in patients with limb girdle muscular dystrophy with calpain 3 deficiency (LGMD2A) and early contractures. Neuromuscul Disord 15(2):164–171. https://doi.org/10.1016/j.nmd.2004.10.008. (Epub 2004 Nov 26)CrossRefPubMed

Wang L, Zhang VW, Li S, Li H, Sun Y, Li J, Zhu Y, He R, Lin J, Zhang C (2018) The clinical spectrum and genetic variability of limb-girdle muscular dystrophy in a cohort of Chinese patients. Orphanet J Rare Dis 13(1):133. https://doi.org/10.1186/s13023-018-0859-6CrossRefPubMedPubMedCentral

Albuquerque MA, Abath Neto O, Silva FM, Zanoteli E, Reed UC (2015) Limb-girdle muscular dystrophy type 2A in Brazilian children. Arq Neuropsiquiatr 73(12):993–997. https://doi.org/10.1590/0004-282X20150168CrossRefPubMed

Stramare R, Beltrame V, Dal Borgo R, Gallimberti L, Frigo AC, Pegoraro E, Angelini C, Rubaltelli L, Feltrin GP (2010) MRI in the assessment of muscular pathology: a comparison between limb-girdle muscular dystrophies, hyaline body myopathies and myotonic dystrophies. Radiol Med 115(4):585–599. https://doi.org/10.1007/s11547-010-0531-2. (English, Italian; Epub 2010 Feb 22)CrossRefPubMed

10.

Arrigoni F, De Luca A, Velardo D, Magri F, Gandossini S, Russo A, Froeling M, Bertoldo A, Leemans A, Bresolin N, D’angelo G (2018) Multiparametric quantitative MRI assessment of thigh muscles in limb-girdle muscular dystrophy 2A and 2B. Muscle Nerve 58(4):550–558. https://doi.org/10.1002/mus.26189. (Epub 2018 Aug 22)CrossRefPubMed

11.

Oliveira Santos M, Ninitas P, Conceição I (2018) Severe limb-girdle muscular dystrophy 2A in two young siblings from Guinea-Bissau associated with a novel null homozygous mutation in CAPN3 gene. Neuromuscul Disord 28(12):1003–1005. https://doi.org/10.1016/j.nmd.2018.09.009. (Epub 2018 Oct 9)CrossRefPubMed

12.

Schutz PW, Scalco RS, Barresi R, Houlden H, Parton M, Holton JL (2017) Calpainopathy with macrophage-rich, regional inflammatory infiltrates. Neuromuscul Disord 27(8):738–741. https://doi.org/10.1016/j.nmd.2017.04.012. (Epub 2017 Apr 27)CrossRefPubMed

13.

Burke G, Hillier C, Cole J, Sampson M, Bridges L, Bushby K, Barresi R, Hammans SR (2010) Calpainopathy presenting as foot drop in a 41 year old. Neuromuscul Disord 20(6):407–410. https://doi.org/10.1016/j.nmd.2010.04.006CrossRefPubMed

14.

Dobrescu MA, Chelu G, Tache DE, Purcaru SO, Petrescu IO (2015) Differential diagnosis between duchenne muscular dystrophy and limb girdle muscular dystrophy 2a. Curr Health Sci J 41(4):385–389. https://doi.org/10.12865/CHSJ.41.04.15. (Epub 2015 Dec 22)CrossRefPubMedPubMedCentral

15.

Luo SS, Xi JY, Lu JH, Zhao CB, Zhu WH, Lin J, Wang Y, Ren HM, Yin B, Andoni UJ (2011) Clinical and pathological features in 15 Chinese patients with calpainopathy. Muscle Nerve 43(3):402–409. https://doi.org/10.1002/mus.21908. (Epub 2010 Dec 9)CrossRefPubMed

16.

Barp A, Laforet P, Bello L, Tasca G, Vissing J, Monforte M, Ricci E, Choumert A, Stojkovic T, Malfatti E, Pegoraro E, Semplicini C, Stramare R, Scheidegger O, Haberlova J, Straub V, Marini-Bettolo C, Løkken N, Diaz-Manera J, Urtizberea JA, Mercuri E, Kynčl M, Walter MC, Carlier RY (2020) European muscle MRI study in limb girdle muscular dystrophy type R1/2A (LGMDR1/LGMD2A). J Neurol 267(1):45–56. https://doi.org/10.1007/s00415-019-09539-y. (Epub 2019 Sep 25)CrossRefPubMed

17.

Degardin A, Morillon D, Lacour A, Cotten A, Vermersch P, Stojkovic T (2010) Morphologic imaging in muscular dystrophies and inflammatory myopathies. Skeletal Radiol 39(12):1219–1227. https://doi.org/10.1007/s00256-010-0930-4. (Epub 2010 May 7)CrossRefPubMed

18.

Feng X, Luo S, Li J, Yue D, Xi J, Zhu W, Gao X, Guan X, Lu J, Liang Z, Zhao C (2018) Fatty infiltration evaluation and selective pattern characterization of lower limbs in limb-girdle muscular dystrophy type 2A by muscle magnetic resonance imaging. Muscle Nerve 58(4):536–541. https://doi.org/10.1002/mus.26169. (Epub 2018 Sep 3)CrossRefPubMed

19.

Peric S, Stevanovic J, Johnson K, Kosac A, Peric M, Brankovic M, Marjanovic A, Jankovic M, Banko B, Milenkovic S, Durdic M, Bozovic I, Glumac JN, Lavrnic D, Maksimovic R, Milic-Rasic V, Rakocevic-Stojanovic V (2019) Phenotypic and genetic spectrum of patients with limb-girdle muscular dystrophy type 2A from Serbia. Acta Myol 38(3):163–171PubMedPubMedCentral

20.

Fischer D, Walter MC, Kesper K, Petersen JA, Aurino S, Nigro V, Kubisch C, Meindl T, Lochmüller H, Wilhelm K, Urbach H, Schröder R (2005) Diagnostic value of muscle MRI in differentiating LGMD2I from other LGMDs. J Neurol 252(5):538–547. https://doi.org/10.1007/s00415-005-0684-4. (Epub 2005 Feb 23)CrossRefPubMed

21.

Schlaeger S, Sollmann N, Zoffl A, Becherucci EA, Weidlich D, Kottmaier E, Riederer I, Greve T, Montagnese F, Deschauer M, Schoser B, Zimmer C, Karampinos DC, Kirschke JS, Baum T (2021) Quantitative muscle MRI in patients with neuromuscular diseases-association of muscle proton density fat fraction with semi-quantitative grading of fatty infiltration and muscle strength at the thigh region. Diagnostics (Basel) 11(6):1056. https://doi.org/10.3390/diagnostics11061056CrossRefPubMed

22.

Aivazoglou LU, Guimarães JB, Costa MAF, Aihara AY, Cardoso FN, Pinto WBVR, de Souza PVS, da Silva AMS, Zanoteli E, Oliveira ASB, Carvalho AAS, Fernandes ADRC (2022) Whole-body MRI in limb girdle muscular dystrophy type R1/2A: correlation with clinical scores. Muscle Nerve 66(4):471–478. https://doi.org/10.1002/mus.27686. (Epub 2022 Aug 10)CrossRefPubMed

23.

Kesper K, Kornblum C, Reimann J, Lutterbey G, Schröder 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. (Epub 2008 Dec 22)CrossRefPubMed

24.

Algahtani H, Shirah B, Alassiri AH, Habib BA, Almuhanna R, Ahamed MF (2018) Limb-girdle muscular dystrophy type 2B: an unusual cause of proximal muscular weakness in Saudi Arabia. J Back Musculoskelet Rehabil 31(5):999–1004. https://doi.org/10.3233/BMR-181129CrossRefPubMed

25.

Fanin M, Angelini C (2016) Progress and challenges in diagnosis of dysferlinopathy. Muscle Nerve 54(5):821–835. https://doi.org/10.1002/mus.25367CrossRefPubMed

26.

Paradas C, Llauger J, Diaz-Manera J, Rojas-García R, De Luna N, Iturriaga C, Márquez C, Usón M, Hankiewicz K, Gallardo E, Illa I (2010) Redefining dysferlinopathy phenotypes based on clinical findings and muscle imaging studies. Neurology 75(4):316–323. https://doi.org/10.1212/WNL.0b013e3181ea1564. (Epub 2010 Jun 23)CrossRefPubMed

27.

Park HJ, Hong JM, Suh GI, Shin HY, Kim SM, Sunwoo IN, Suh BC, Choi YC (2012) Heterogeneous characteristics of Korean patients with dysferlinopathy. J Korean Med Sci 27(4):423–429. https://doi.org/10.3346/jkms.2012.27.4.423. (Epub 2012 Mar 21)CrossRefPubMedPubMedCentral

28.

Jin S, Du J, Wang Z, Zhang W, Lv H, Meng L, Xiao J, Yuan Y (2016) Heterogeneous characteristics of MRI changes of thigh muscles in patients with dysferlinopathy. Muscle Nerve 54(6):1072–1079. https://doi.org/10.1002/mus.25207. (Epub 2016 Oct 11)CrossRefPubMed

29.

Diaz-Manera J, Fernandez-Torron R, Lauger JL, 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 COS Consortium (2018) Muscle MRI in patients with dysferlinopathy: pattern recognition and implications for clinical trials. J Neurol Neurosurg Psychiatry 89(10):1071–1081. https://doi.org/10.1136/jnnp-2017-317488CrossRefPubMed

30.

Díaz J, Woudt L, Suazo L, Garrido C, Caviedes P, Cárdenas AM, Castiglioni C, Bevilacqua JA (2016) Broadening the imaging phenotype of dysferlinopathy at different disease stages. Muscle Nerve 54(2):203–210. https://doi.org/10.1002/mus.25045. (Epub 2016 May 26)CrossRefPubMed

31.

Reyngoudt H, Smith FE, Caldas de Almeida Araújo E, Wilson I, Fernández-Torrón R, James MK, Moore UR, Díaz-Manera J, Marty B, Azzabou N, Gordish H, Rufibach L, Hodgson T, Wallace D, Ward L, Boisserie JM, Le Louër J, Hilsden H, Sutherland H, Canal A, Hogrel JY, Jacobs M, Stojkovic T, Bushby K, Mayhew A, Jain Clinical Outcome Study for Dysferlinopathy consortium, Straub V, Carlier PG, Blamire AM (2022) Three-year quantitative magnetic resonance imaging and phosphorus magnetic resonance spectroscopy study in lower limb muscle in dysferlinopathy. J Cachexia Sarcopenia Muscle 13(3):1850–1863. https://doi.org/10.1002/jcsm.12987. (Epub 2022 Apr 3)CrossRefPubMedPubMedCentral

32.

Wang DN, Wang ZQ, Chen YQ, Xu GR, Lin MT, Wang N (2018) Limb-girdle muscular dystrophy type 2I: two Chinese families and a review in Asian patients. Int J Neurosci 128(3):199–207. https://doi.org/10.1080/00207454.2017.1380640. (Epub 2017 Oct 2)CrossRefPubMed

33.

Xie Z, Xiao J, Zheng Y, Wang Z, Yuan Y (2018) Magnetic resonance imaging findings in the muscle tissue of patients with limb girdle muscular dystrophy type 2I harboring the founder mutation c.545A>G in the FKRP gene. Biomed Res Int 29(2018):3710814. https://doi.org/10.1155/2018/3710814CrossRef

34.

Bourteel H, Vermersch P, Cuisset JM, Maurage CA, Laforet P, Richard P, Stojkovic T (2009) Clinical and mutational spectrum of limb-girdle muscular dystrophy type 2I in 11 French patients. J Neurol Neurosurg Psychiatry 80(12):1405–1408. https://doi.org/10.1136/jnnp.2007.141804. (PMID: 19917824)CrossRefPubMed

35.

Revsbech KL, Rudolf K, Sheikh AM, Khawajazada T, de Stricker BJ, Dahlqvist JR, Løkken N, Witting N, Vissing J (2022) Axial muscle involvement in patients with limb girdle muscular dystrophy type R9. Muscle Nerve 65(4):405–414. https://doi.org/10.1002/mus.27491. (Epub 2022 Jan 25)CrossRefPubMed

36.

Ghaoui R, Cooper ST, Lek M, Jones K, Corbett A, Reddel SW, Needham M, Liang C, Waddell LB, Nicholson G, O’Grady G, Kaur S, Ong R, Davis M, Sue CM, Laing NG, North KN, MacArthur DG, Clarke NF (2015) Use of whole-exome sequencing for diagnosis of limb-girdle muscular dystrophy: outcomes and lessons learned. JAMA Neurol 72(12):1424–1432. https://doi.org/10.1001/jamaneurol.2015.2274CrossRefPubMed

37.

Hu B, Xiong L, Zhou Y, Lu X, Xiong Q, Liu Q, Qi X, Ding W (2018) First familial limb-girdle muscular dystrophy 2L in China: clinical, imaging, pathological, and genetic features. Medicine (Baltimore) 97(38):e12506. https://doi.org/10.1097/MD.0000000000012506CrossRefPubMed

38.

Sarkozy A, Deschauer M, Carlier RY, Schrank B, Seeger J, Walter MC, Schoser B, Reilich P, Leturq F, Radunovic A, Behin A, Laforet P, Eymard B, Schreiber H, Hicks D, Vaidya SS, Gläser D, Carlier PG, Bushby K, Lochmüller H, Straub V (2012) Muscle MRI findings in limb girdle muscular dystrophy type 2L. Neuromuscul Disord 1(22 Suppl 2):S122–S129. https://doi.org/10.1016/j.nmd.2012.05.012CrossRef

39.

Schneider I, Stoltenburg G, Deschauer M, Winterholler M, Hanisch F (2014) Limb girdle muscular dystrophy type 2L presenting as necrotizing myopathy. Acta Myol 33(1):19–21PubMedPubMedCentral

40.

Tasca G, Evilä A, Pane M, Monforte M, Graziano A, Hackman P, Mercuri E, Udd B (2014) Isolated semitendinosus involvement in the initial stages of limb-girdle muscular dystrophy 2L. Neuromuscul Disord 24(12):1118–1119. https://doi.org/10.1016/j.nmd.2014.06.442. (Epub 2014 Jul 9)CrossRefPubMed

41.

Bohlega S, Monies DM, Abulaban AA, Murad HN, Alhindi HN, Meyer BF (2015) Clinical and genetic features of anoctaminopathy in Saudi Arabia. Neurosciences (Riyadh) 20(2):173–177. https://doi.org/10.17712/nsj.2015.2.20140547CrossRefPubMed

42.

Little AA, McKeever PE, Gruis KL (2013) Novel mutations in the Anoctamin 5 gene (ANO5) associated with limb-girdle muscular dystrophy 2L. Muscle Nerve 47(2):287–291. https://doi.org/10.1002/mus.23542. (Epub 2012 Nov 21)CrossRefPubMed

43.

Witting N, Duno M, Petri H, Krag T, Bundgaard H, Kober L, Vissing J (2013) Anoctamin 5 muscular dystrophy in Denmark: prevalence, genotypes, phenotypes, cardiac findings, and muscle protein expression. J Neurol 260(8):2084–2093. https://doi.org/10.1007/s00415-013-6934-y. (Epub 2013 May 14)CrossRefPubMed

44.

Khawajazada T, Kass K, Rudolf K, de Stricker BJ, Sheikh AM, Witting N, Vissing J (2021) Muscle involvement assessed by quantitative magnetic resonance imaging in patients with anoctamin 5 deficiency. Eur J Neurol 28(9):3121–3132. https://doi.org/10.1111/ene.14979. (Epub 2021 Jul 11)CrossRefPubMed

45.

Marago I, Roberts M, Roncaroli F, DuPlessis D, Sewry C, Nagaraju S, Limbada F, Marini-Bettolo C, Hudson J, Banerjee S, Newton L, Bukhari M, Chinoy H, Lilleker JB (2022) Limb girdle muscular dystrophy R12 (LGMD 2L, anoctaminopathy) mimicking idiopathic inflammatory myopathy: key points to prevent misdiagnosis. Rheumatology (Oxford) 61(4):1645–1650. https://doi.org/10.1093/rheumatology/keab553. (PMID: 34264321)CrossRefPubMed

46.

De Wel B, Huysmans L, Peeters R, Goosens V, Ghysels S, Byloos K, Putzeys G, D’Hondt A, De Bleecker JL, Dupont P, Maes F, Claeys KG (2022) Prospective natural history study in 24 adult patients with LGMDR12 Over 2 years of follow-up: quantitative MRI and clinical outcome measures. Neurology 99(6):e638–e649. https://doi.org/10.1212/WNL.0000000000200708. (Epub 2022 May 16)CrossRefPubMed

47.

Tasca G, Monforte M, Díaz-Manera J, Brisca G, Semplicini C, D’Amico A, Fattori F, Pichiecchio A, Berardinelli A, Maggi L, Maccagnano E, Løkken N, Marini-Bettolo C, Munell F, Sanchez A, Alshaikh N, Voermans NC, Dastgir J, Vlodavets D, Haberlová J, Magnano G, Walter MC, Quijano-Roy S, Carlier RY, van Engelen BGM, Vissing J, Straub V, Bönnemann CG, Mercuri E, Muntoni F, Pegoraro E, Bertini E, Udd B, Ricci E, Bruno C (2018) MRI in sarcoglycanopathies: a large international cohort study. J Neurol Neurosurg Psychiatry 89(1):72–77. https://doi.org/10.1136/jnnp-2017-316736. (Epub 2017 Sep 9)CrossRefPubMed

48.

Lodi R, Muntoni F, Taylor J, Kumar S, Sewry CA, Blamire A, Styles P, Taylor DJ (1997) Correlative MR imaging and 31P-MR spectroscopy study in sarcoglycan deficient limb girdle muscular dystrophy. Neuromuscul Disord 7(8):505–511. https://doi.org/10.1016/s0960-8966(97)00108-9CrossRefPubMed

49.

Gonzalez-Quereda L, Gallardo E, Töpf A, Alonso-Jimenez A, Straub V, Rodriguez MJ, Lleixa C, Illa I, Gallano P, Diaz-Manera J (2018) A new mutation of the SCGA gene is the cause of a late onset mild phenotype limb girdle muscular dystrophy type 2D with axial involvement. Neuromuscul Disord 28(8):633–638. https://doi.org/10.1016/j.nmd.2018.06.002. (Epub 2018 Jul 13)CrossRefPubMed

50.

Chamova T, Bichev S, Todorov T, Gospodinova M, Taneva A, Kastreva K, Zlatareva D, Krupev M, Hadjiivanov R, Guergueltcheva V, Grozdanova L, Tzoneva D, Huebner A, V der Hagen M, Schoser B, Lochmüller H, Todorova A, Tournev I (2018) Limb girdle muscular dystrophy 2G in a religious minority of Bulgarian Muslims homozygous for the c.75G>A, p.Trp25X mutation. Neuromuscul Disord 28(8):625–632. https://doi.org/10.1016/j.nmd.2018.05.005. (Epub 2018 May 17)CrossRefPubMed

51.

Brusa R, Magri F, Papadimitriou D, Govoni A, Del Bo R, Ciscato P, Savarese M, Cinnante C, Walter MC, Abicht A, Bulst S, Corti S, Moggio M, Bresolin N, Nigro V, Comi GP (2018) A new case of limb girdle muscular dystrophy 2G in a Greek patient, founder effect and review of the literature. Neuromuscul Disord 28(6):532–537. https://doi.org/10.1016/j.nmd.2018.04.006. (Epub 2018 Apr 13)CrossRefPubMed

52.

Francis A, Sunitha B, Vinodh K, Polavarapu K, Katkam SK, Modi S, Bharath MM, Gayathri N, Nalini A, Thangaraj K (2014) Novel TCAP mutation c.32C>A causing limb girdle muscular dystrophy 2G. PLoS ONE 9(7):e102763. https://doi.org/10.1371/journal.pone.0102763CrossRefPubMedPubMedCentral

53.

Ikenberg E, Karin I, Ertl-Wagner B, Abicht A, Bulst S, Krause S, Schoser B, Reilich P, Walter MC (2017) Rare diagnosis of telethoninopathy (LGMD2G) in a Turkish patient. Neuromuscul Disord 27(9):856–860. https://doi.org/10.1016/j.nmd.2017.05.017. (Epub 2017 Jun 1. Erratum in: Neuromuscul Disord. 2017 Dec;27(12 ):e1)CrossRefPubMed

54.

Negrão L, Matos A, Geraldo A, Rebelo O (2010) Limb-girdle muscular dystrophy in a Portuguese patient caused by a mutation in the telethonin gene. Acta Myol 29(1):21–24PubMedPubMedCentral

55.

Chen H, Xu G, Lin F, Jin M, Cai N, Qiu L, Ye Z, Wang L, Lin M, Wang N (2020) Clinical and genetic characterization of limb girdle muscular dystrophy R7 telethonin-related patients from three unrelated Chinese families. Neuromuscul Disord 30(2):137–143. https://doi.org/10.1016/j.nmd.2019.12.004. (Epub 2019 Dec 17)CrossRefPubMed

56.

Van den Bergh PYK, Sznajer Y, Van Parys V, van Tol W, Wevers RA, Lefeber DJ, Xu L, Lek M, MacArthur DG, Johnson K, Phillips L, Töpf A, Straub V (2017) A homozygous DPM3 mutation in a patient with alpha-dystroglycan-related limb girdle muscular dystrophy. Neuromuscul Disord 27(11):1043–1046. https://doi.org/10.1016/j.nmd.2017.07.006. (Epub 2017 Jul 17. Erratum in: Neuromuscul Disord. 2017 Dec 12)CrossRefPubMed

57.

Hafner P, Bonati U, Fischmann A, Schneider J, Frank S, Morris-Rosendahl DJ, Dumea A, Heinimann K, Fischer D (2014) Skeletal muscle MRI of the lower limbs in congenital muscular dystrophy patients with novel POMT1 and POMT2 mutations. Neuromuscul Disord 24(4):321–324. https://doi.org/10.1016/j.nmd.2014.01.009. (Epub 2014 Jan 28)CrossRefPubMed

58.

Ganassi M, Zammit PS (2022) Involvement of muscle satellite cell dysfunction in neuromuscular disorders: expanding the portfolio of satellite cell-opathies. Eur J Transl Myol 32(1):10064. https://doi.org/10.4081/ejtm.2022.10064CrossRefPubMedPubMedCentral

59.

Haberlova J, Mitrović Z, Zarković K, Lovrić D, Barić V, Berlengi L, Bilić K, Fumić K, Kranz K, Huebner A, von der Hagen M, Barresi R, Bushby K, Straub V, Barić I, Lochmüller H (2014) Psycho-organic symptoms as early manifestation of adult onset POMT1-related limb girdle muscular dystrophy. Neuromuscul Disord 24(11):990–992. https://doi.org/10.1016/j.nmd.2014.06.440. (Epub 2014 Jul 3)CrossRefPubMed

60.

Harris E, Töpf A, Vihola A, Evilä A, Barresi R, Hudson J, Hackman P, Herron B, MacArthur D, Lochmüller H, Bushby K, Udd B, Straub V (2017) A “second truncation” in TTN causes early onset recessive muscular dystrophy. Neuromuscul Disord 27(11):1009–1017. https://doi.org/10.1016/j.nmd.2017.06.013. (Epub 2017 Jun 22)CrossRefPubMed

61.

Dabby R, Sadeh M, Hilton-Jones D, Plotz P, Hackman P, Vihola A, Udd B, Leshinsky-Silver E (2015) Adult onset limb-girdle muscular dystrophy—a recessive titinopathy masquerading as myositis. J Neurol Sci 351(1–2):120–123. https://doi.org/10.1016/j.jns.2015.03.001. (Epub 2015 Mar 6)CrossRefPubMed

62.

Udd B, Vihola A, Sarparanta J, Richard I, Hackman P (2005) Titinopathies and extension of the M-line mutation phenotype beyond distal myopathy and LGMD2J. Neurology 64(4):636–642. https://doi.org/10.1212/01.WNL.0000151853.50144.82CrossRefPubMed

63.

Neri M, Selvatici R, Scotton C, Trabanelli C, Armaroli A, De Grandis D, Levy N, Gualandi F, Ferlini A (2013) A patient with limb girdle muscular dystrophy carries a TRIM32 deletion, detected by a novel CGH array, in compound heterozygosis with a nonsense mutation. Neuromuscul Disord 23(6):478–482. https://doi.org/10.1016/j.nmd.2013.02.003. (Epub 2013 Mar 28)CrossRefPubMed

64.

Johnson K, De Ridder W, Töpf A, Bertoli M, Phillips L, De Jonghe P, Baets J, Deconinck T, Rakocevic Stojanovic V, Perić S, Durmus H, Jamal-Omidi S, Nafissi S, Mongini T, Łusakowska A, Busby M, Miller J, Norwood F, Hudson J, Barresi R, Lek M, MacArthur DG, Straub V (2019) Extending the clinical and mutational spectrum of TRIM32-related myopathies in a non-Hutterite population. J Neurol Neurosurg Psychiatry 90(4):490–493. https://doi.org/10.1136/jnnp-2018-318288. (Epub 2018 Jun 19)CrossRefPubMed

65.

Panicucci C, Traverso M, Baratto S, Romeo C, Iacomino M, Gemelli C, Tagliafico A, Broda P, Zara F, Bruno C, Minetti C, Fiorillo C (2019) Novel TRIM32 mutation in sarcotubular myopathy. Acta Myol 38(1):8–12PubMedPubMedCentral

66.

Tian WT, Zhou HY, Zhan FX, Zhu ZY, Yang J, Chen SD, Luan XH, Cao L (2019) Lysosomal degradation of GMPPB is associated with limb-girdle muscular dystrophy type 2T. Ann Clin Transl Neurol 6(6):1062–1071. https://doi.org/10.1002/acn3.787CrossRefPubMedPubMedCentral

67.

Astrea G, Romano A, Angelini C, Antozzi CG, Barresi R, Battini R, Battisti C, Bertini E, Bruno C, Cassandrini D, Fanin M, Fattori F, Fiorillo C, Guerrini R, Maggi L, Mercuri E, Morani F, Mora M, Moro F, Pezzini I, Picillo E, Pinelli M, Politano L, Rubegni A, Sanseverino W, Savarese M, Striano P, Torella A, Trevisan CP, Trovato R, Zaraieva I, Muntoni F, Nigro V, D’Amico A, Santorelli FM, Italian CMD Network (2018) Broad phenotypic spectrum and genotype-phenotype correlations in GMPPB-related dystroglycanopathies: an Italian cross-sectional study. Orphanet J Rare Dis 13(1):170. https://doi.org/10.1186/s13023-018-0863-xCrossRefPubMedPubMedCentral

68.

Oestergaard ST, Stojkovic T, Dahlqvist JR, Bouchet-Seraphin C, Nectoux J, Leturcq F, Cossée M, Solé G, Thomsen C, Krag TO, Vissing J (2016) Muscle involvement in limb-girdle muscular dystrophy with GMPPB deficiency (LGMD2T). Neurol Genet 2(6):e112. https://doi.org/10.1212/NXG.0000000000000112CrossRefPubMedPubMedCentral

69.

Servián-Morilla E, Takeuchi H, Lee TV, Clarimon J, Mavillard F, Area-Gómez E, Rivas E, Nieto-González JL, Rivero MC, Cabrera-Serrano M, Gómez-Sánchez L, Martínez-López JA, Estrada B, Márquez C, Morgado Y, Suárez-Calvet X, Pita G, Bigot A, Gallardo E, Fernández-Chacón R, Hirano M, Haltiwanger RS, Jafar-Nejad H, Paradas C (2016) A POGLUT1 mutation causes a muscular dystrophy with reduced Notch signaling and satellite cell loss. EMBO Mol Med 8(11):1289–1309. https://doi.org/10.15252/emmm.201505815CrossRefPubMedPubMedCentral

70.

Servián-Morilla E, Cabrera-Serrano M, Johnson K, Pandey A, Ito A, Rivas E, Chamova T, Muelas N, Mongini T, Nafissi S, Claeys KG, Grewal RP, Takeuchi M, Hao H, Bönnemann C, Lopes Abath Neto O, Medne L, Brandsema J, Töpf A, Taneva A, Vilchez JJ, Tournev I, Haltiwanger RS, Takeuchi H, Jafar-Nejad H, Straub V, Paradas C (2020) POGLUT1 biallelic mutations cause myopathy with reduced satellite cells, α-dystroglycan hypoglycosylation and a distinctive radiological pattern. Acta Neuropathol 139(3):565–582. https://doi.org/10.1007/s00401-019-02117-6. (Epub 2020 Jan 3)CrossRefPubMedPubMedCentral

71.

Bohlega SA, Alfawaz S, Abou-Al-Shaar H, Al-Hindi HN, Murad HN, Bohlega MS, Meyer BF, Monies D (2018) LGMD1D myopathy with cytoplasmic and nuclear inclusions in a Saudi family due to DNAJB6 mutation. Acta Myol 37(3):221–226PubMedPubMedCentral

72.

Jonson PH, Palmio J, Johari M, Penttilä S, Evilä A, Nelson I, Bonne G, Wiart N, Meyer V, Boland A, Deleuze JF, Masson C, Stojkovic T, Chapon F, Romero NB, Solé G, Ferrer X, Ferreiro A, Hackman P, Richard I, Udd B (2018) Novel mutations in DNAJB6 cause LGMD1D and distal myopathy in French families. Eur J Neurol 25(5):790–794. https://doi.org/10.1111/ene.13598. (Epub 2018 Mar 30)CrossRefPubMed

73.

Zima J, Eaton A, Pál E, Till Á, Ito YA, Warman-Chardon J, Hartley T, Cagnone G, Melegh BI, Care4Rare Canada, Boycott KM, Melegh B, Hadzsiev K (2020) Intrafamilial variability of limb-girdle muscular dystrophy, LGMD1D type. Eur J Med Genet 63(2):103655. https://doi.org/10.1016/j.ejmg.2019.04.012. (Epub 2019 Apr 27)CrossRefPubMed

74.

Nam TS, Li W, Heo SH, Lee KH, Cho A, Shin JH, Kim YO, Chae JH, Kim DS, Kim MK, Choi SY (2015) A novel mutation in DNAJB6, p.(Phe91Leu), in childhood-onset LGMD1D with a severe phenotype. Neuromuscul Disord 25(11):843–851. https://doi.org/10.1016/j.nmd.2015.08.002. (Epub 2015 Aug 11)CrossRefPubMed

75.

Sato T, Hayashi YK, Oya Y, Kondo T, Sugie K, Kaneda D, Houzen H, Yabe I, Sasaki H, Noguchi S, Nonaka I, Osawa M, Nishino I (2013) DNAJB6 myopathy in an Asian cohort and cytoplasmic/nuclear inclusions. Neuromuscul Disord 23(3):269–276. https://doi.org/10.1016/j.nmd.2012.12.010. (Epub 2013 Feb 6)CrossRefPubMed

76.

Palmio J, Jonson PH, Evilä A, Auranen M, Straub V, Bushby K, Sarkozy A, Kiuru-Enari S, Sandell S, Pihko H, Hackman P, Udd B (2015) Novel mutations in DNAJB6 gene cause a very severe early-onset limb-girdle muscular dystrophy 1D disease. Neuromuscul Disord 25(11):835–842. https://doi.org/10.1016/j.nmd.2015.07.014. (Epub 2015 Jul 27)CrossRefPubMed

77.

Hackman P, Sandell S, Sarparanta J, Luque H, Huovinen S, Palmio J, Paetau A, Kalimo H, Mahjneh I, Udd B (2011) Four new Finnish families with LGMD1D; refinement of the clinical phenotype and the linked 7q36 locus. Neuromuscul Disord 21(5):338–344. https://doi.org/10.1016/j.nmd.2011.02.008. (Epub 2011 Mar 3)CrossRefPubMed

78.

Gibertini S, Ruggieri A, Saredi S, Salerno F, Blasevich F, Napoli L, Moggio M, Nigro V, Morandi L, Maggi L, Mora M (2018) Long term follow-up and further molecular and histopathological studies in the LGMD1F sporadic TNPO3-mutated patient. Acta Neuropathol Commun 6(1):141. https://doi.org/10.1186/s40478-018-0648-4CrossRefPubMedPubMedCentral

79.

Peterle E, Fanin M, Semplicini C, Padilla JJ, Nigro V, Angelini C (2013) Clinical phenotype, muscle MRI and muscle pathology of LGMD1F. J Neurol 260(8):2033–2041. https://doi.org/10.1007/s00415-013-6931-1. (Epub 2013 Apr 30)CrossRefPubMed

80.

Pál E, Zima J, Hadzsiev K, Ito YA, Hartley T, Care4Rare Canada Consortium, Boycott KM, Melegh B (2019) A novel pathogenic variant in TNPO3 in a Hungarian family with limb-girdle muscular dystrophy 1F. Eur J Med Genet 62(7):103662. https://doi.org/10.1016/j.ejmg.2019.05.001. (Epub 2019 May 6)CrossRefPubMed

81.

Vihola A, Palmio J, Danielsson O, Penttilä S, Louiselle D, Pittman S, Weihl C, Udd B (2019) Novel mutation in TNPO3 causes congenital limb-girdle myopathy with slow progression. Neurol Genet 5(3):e337. https://doi.org/10.1212/NXG.0000000000000337CrossRefPubMedPubMedCentral

82.

Melià MJ, Kubota A, Ortolano S, Vílchez JJ, Gámez J, Tanji K, Bonilla E, Palenzuela L, Fernández-Cadenas I, Pristoupilová A, García-Arumí E, Andreu AL, Navarro C, Hirano M, Martí R (2013) Limb-girdle muscular dystrophy 1F is caused by a microdeletion in the transportin 3 gene. Brain 136(5):1508–1517. https://doi.org/10.1093/brain/awt074. (Epub 2013 Mar 29)CrossRefPubMedPubMedCentral

83.

Angelini C, Marozzo R, Pinzan E, Pegoraro V, Molnar MJ, Torella A, Nigro V (2019) A new family with transportinopathy: increased clinical heterogeneity. Ther Adv Neurol Disord 9(12):1756286419850433. https://doi.org/10.1177/1756286419850433CrossRef

84.

Berardo A, Lornage X, Johari M, Evangelista T, Cejas C, Barroso F, Dubrovsky A, Bui MT, Brochier G, Saccoliti M, Bohm J, Udd B, Laporte J, Romero NB, Taratuto AL (2019) HNRNPDL-related muscular dystrophy: expanding the clinical, morphological and MRI phenotypes. J Neurol 266(10):2524–2534. https://doi.org/10.1007/s00415-019-09437-3. (Epub 2019 Jul 2)CrossRefPubMed

85.

Sun Y, Chen H, Lu Y, Duo J, Lei L, OuYang Y, Hao Y, Da Y, Shen XM (2019) Limb girdle muscular dystrophy D3 HNRNPDL related in a Chinese family with distal muscle weakness caused by a mutation in the prion-like domain. J Neurol 266(2):498–506. https://doi.org/10.1007/s00415-018-9165-4. (Epub 2019 Jan 2)CrossRefPubMed

86.

Angelini CLGMD (2020) Identification, description and classification. Acta Myol 39(4):207–217. https://doi.org/10.36185/2532-1900-024CrossRefPubMedPubMedCentral

87.

Yu M, Zheng Y, Jin S, Gang Q, Wang Q, Yu P, Lv H, Zhang W, Yuan Y, Wang Z (2017) Mutational spectrum of Chinese LGMD patients by targeted next-generation sequencing. PLoS ONE 12(4):e0175343. https://doi.org/10.1371/journal.pone.0175343CrossRefPubMedPubMedCentral

88.

Grigull L, Lechner W, Petri S, Kollewe K, Dengler R, Mehmecke S, Schumacher U, Lücke T, Schneider-Gold C, Köhler C, Güttsches AK, Kortum X, Klawonn F (2016) Diagnostic support for selected neuromuscular diseases using answer-pattern recognition and data mining techniques: a proof of concept multicenter prospective trial. BMC Med Inform Decis Mak 8(16):31. https://doi.org/10.1186/s12911-016-0268-5CrossRef

89.

Lecouvet FE, Whole-Body MR (2016) Imaging: musculoskeletal applications. Radiology 279(2):345–365. https://doi.org/10.1148/radiol.2016142084CrossRefPubMed

90.

Vilanova JC, García-Figueiras R, Luna A, Baleato-González S, Tomás X, Narváez JA (2019) Update on whole-body MRI in musculoskeletal applications. Semin Musculoskelet Radiol 23(3):312–323. https://doi.org/10.1055/s-0039-1685540. (Epub 2019 Jun 4)CrossRefPubMed

91.

Khan IA, Mahabadi N, D’Abarno A, Varacallo M (2022) Anatomy, bony pelvis and lower limb, leg lateral compartment. 2022 Aug 8. In: StatPearls. Treasure Island (FL): StatPearls Publishing

Titel: Muscle MRI patterns for limb girdle muscle dystrophies: systematic review
verfasst von: Issa Alawneh
Ana Stosic
Hernan Gonorazky
Publikationsdatum: 02.05.2023
Verlag: Springer Berlin Heidelberg
Erschienen in: Journal of Neurology / Ausgabe 8/2023
Print ISSN: 0340-5354
Elektronische ISSN: 1432-1459
DOI: https://doi.org/10.1007/s00415-023-11722-1

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