Muscle Architecture is Associated with Muscle Fat Replacement in Duchenne and Becker Muscular Dystrophies

Overview

Journal Muscle Nerve

Date 2021 Aug 12

PMID 34383334

Citations 8

Authors

Thom T J Veeger

Erik W van Zwet

Diaa Al Mohamad

Karin J Naarding

Nienke M van de Velde

Melissa T Hooijmans

Andrew G Webb

Erik H Niks

Jurriaan H De Groot

Hermien E Kan

Affiliations

Soon will be listed here.

Abstract

Introduction/aims: Duchenne and Becker muscular dystrophies (DMD and BMD, respectively) are characterized by fat replacement of different skeletal muscles in a specific temporal order. Given the structural role of dystrophin in skeletal muscle mechanics, muscle architecture could be important in the progressive pathophysiology of muscle degeneration. Therefore, the aim of this study was to assess the role of muscle architecture in the progression of fat replacement in DMD and BMD.

Methods: We assessed the association between literature-based leg muscle architectural characteristics and muscle fat fraction from 22 DMD and 24 BMD patients. Dixon-based magnetic resonance imaging estimates of fat fractions at baseline and 12 (only DMD) and 24 months were related to fiber length and physiological cross-sectional area (PCSA) using age-controlled linear mixed modeling.

Results: DMD and BMD muscles with long fibers and BMD muscles with large PCSAs were associated with increased fat fraction. The effect of fiber length was stronger in muscles with larger PCSA.

Discussion: Muscle architecture may explain the pathophysiology of muscle degeneration in dystrophinopathies, in which proximal muscles with a larger mass (fiber length × PCSA) are more susceptible, confirming the clinical observation of a temporal proximal-to-distal progression. These results give more insight into the mechanical role in the pathophysiology of muscular dystrophies. Ultimately, this new information can be used to help support the selection of current and the development of future therapies.

Citing Articles

Parameter optimization for proton density fat fraction quantification in skeletal muscle tissue at 7 T.

Tkotz K, Zeiger P, Hanspach J, Mathy C, Laun F, Uder M MAGMA. 2024; 37(6):969-981.

PMID: 39105951 PMC: 11582128. DOI: 10.1007/s10334-024-01195-2.

Development of respiratory care guidelines for Duchenne muscular dystrophy in the UK: key recommendations for clinical practice.

Childs A, Turner C, Astin R, Bianchi S, Bourke J, Cunningham V Thorax. 2023; 79(5):476-485.

PMID: 38123347 PMC: 11041593. DOI: 10.1136/thorax-2023-220811.

Cellular pathogenesis of Duchenne muscular dystrophy: progressive myofibre degeneration, chronic inflammation, reactive myofibrosis and satellite cell dysfunction.

Dowling P, Swandulla D, Ohlendieck K Eur J Transl Myol. 2023; 33(4).

PMID: 37846661 PMC: 10811648. DOI: 10.4081/ejtm.2023.11856.

The metabolomic plasma profile of patients with Duchenne muscular dystrophy: providing new evidence for its pathogenesis.

Xu H, Cai X, Xu K, Wu Q, Xu B Orphanet J Rare Dis. 2023; 18(1):273.

PMID: 37670327 PMC: 10481483. DOI: 10.1186/s13023-023-02885-1.

X-linked genes influence various complex traits in dairy cattle.

Sanchez M, Escouflaire C, Baur A, Bottin F, Hoze C, Boussaha M BMC Genomics. 2023; 24(1):338.

PMID: 37337145 PMC: 10278306. DOI: 10.1186/s12864-023-09438-7.

References

Wang X, Hernando D, Reeder S . Sensitivity of chemical shift-encoded fat quantification to calibration of fat MR spectrum. Magn Reson Med. 2015; 75(2):845-51. PMC: 4592785. DOI: 10.1002/mrm.25681. View

Burdi A, Huelke D, SNYDER R, LOWREY G . Infants and children in the adult world of automobile safety design: pediatric and anatomical considerations for design of child restraints. J Biomech. 1969; 2(3):267-80. DOI: 10.1016/0021-9290(69)90083-9. View

Pasternak C, Wong S, Elson E . Mechanical function of dystrophin in muscle cells. J Cell Biol. 1995; 128(3):355-61. PMC: 2120342. DOI: 10.1083/jcb.128.3.355. View

Claflin D, Brooks S . Direct observation of failing fibers in muscles of dystrophic mice provides mechanistic insight into muscular dystrophy. Am J Physiol Cell Physiol. 2008; 294(2):C651-8. DOI: 10.1152/ajpcell.00244.2007. View

Angelini C, Fanin M, Pegoraro E, Freda M, Cadaldini M, Martinello F . Clinical-molecular correlation in 104 mild X-linked muscular dystrophy patients: characterization of sub-clinical phenotypes. Neuromuscul Disord. 1994; 4(4):349-58. DOI: 10.1016/0960-8966(94)90071-x. View

Tasca G, Iannaccone E, Monforte M, Masciullo M, Bianco F, Laschena F . Muscle MRI in Becker muscular dystrophy. Neuromuscul Disord. 2012; 22 Suppl 2:S100-6. DOI: 10.1016/j.nmd.2012.05.015. View

Statland J, Tawil R . Facioscapulohumeral muscular dystrophy. Neurol Clin. 2014; 32(3):721-8, ix. PMC: 4239655. DOI: 10.1016/j.ncl.2014.04.003. View

Arora H, Willcocks R, Lott D, Harrington A, Senesac C, Zilke K . Longitudinal timed function tests in Duchenne muscular dystrophy: ImagingDMD cohort natural history. Muscle Nerve. 2018; 58(5):631-638. PMC: 6660165. DOI: 10.1002/mus.26161. View

Ponrartana S, Ramos-Platt L, Wren T, Hu H, Perkins T, Chia J . Effectiveness of diffusion tensor imaging in assessing disease severity in Duchenne muscular dystrophy: preliminary study. Pediatr Radiol. 2014; 45(4):582-9. DOI: 10.1007/s00247-014-3187-6. View

10.

Hollingsworth K, Higgins D, Mccallum M, Ward L, Coombs A, Straub V . Investigating the quantitative fidelity of prospectively undersampled chemical shift imaging in muscular dystrophy with compressed sensing and parallel imaging reconstruction. Magn Reson Med. 2013; 72(6):1610-9. DOI: 10.1002/mrm.25072. View

11.

Cros D, Harnden P, Pellissier J, Serratrice G . Muscle hypertrophy in Duchenne muscular dystrophy. A pathological and morphometric study. J Neurol. 1989; 236(1):43-7. DOI: 10.1007/BF00314217. View

12.

Lokken N, Hedermann G, Thomsen C, Vissing J . Contractile properties are disrupted in Becker muscular dystrophy, but not in limb girdle type 2I. Ann Neurol. 2016; 80(3):466-71. DOI: 10.1002/ana.24743. View

13.

Murphy R, Beardsley A . Mechanical properties of the cat soleus muscle in situ. Am J Physiol. 1974; 227(5):1008-13. DOI: 10.1152/ajplegacy.1974.227.5.1008. View

14.

Hu X, Blemker S . Musculoskeletal simulation can help explain selective muscle degeneration in Duchenne muscular dystrophy. Muscle Nerve. 2015; 52(2):174-82. DOI: 10.1002/mus.24607. View

15.

Willis T, Hollingsworth K, Coombs A, Sveen M, Andersen S, Stojkovic T . Quantitative muscle MRI as an assessment tool for monitoring disease progression in LGMD2I: a multicentre longitudinal study. PLoS One. 2013; 8(8):e70993. PMC: 3743890. DOI: 10.1371/journal.pone.0070993. View

16.

Veeger T, van Zwet E, Al Mohamad D, Naarding K, van de Velde N, Hooijmans M . Muscle architecture is associated with muscle fat replacement in Duchenne and Becker muscular dystrophies. Muscle Nerve. 2021; 64(5):576-584. PMC: 9290788. DOI: 10.1002/mus.27399. View

17.

Emery A . Muscular dystrophy into the new millennium. Neuromuscul Disord. 2002; 12(4):343-9. DOI: 10.1016/s0960-8966(01)00303-0. View

18.

Naarding K, Reyngoudt H, van Zwet E, Hooijmans M, Tian C, Rybalsky I . MRI vastus lateralis fat fraction predicts loss of ambulation in Duchenne muscular dystrophy. Neurology. 2020; 94(13):e1386-e1394. PMC: 7274919. DOI: 10.1212/WNL.0000000000008939. View

19.

Raz Y, van den Akker E, Roest T, Riaz M, van de Rest O, Suchiman H . A data-driven methodology reveals novel myofiber clusters in older human muscles. FASEB J. 2020; 34(4):5525-5537. DOI: 10.1096/fj.201902350R. View

20.

Mankodi A, Bishop C, Auh S, Newbould R, Fischbeck K, Janiczek R . Quantifying disease activity in fatty-infiltrated skeletal muscle by IDEAL-CPMG in Duchenne muscular dystrophy. Neuromuscul Disord. 2016; 26(10):650-658. PMC: 5062949. DOI: 10.1016/j.nmd.2016.07.013. View