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MRI assessment of the thigh musculature in dermatomyositis and healthy subjects using diffusion tensor imaging, intravoxel incoherent motion and dynamic DTI

  • Musculoskeletal
  • Published:
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A Correction to this article was published on 09 July 2018

This article has been updated

Abstract

Introduction

Dermatomyositis (DM) is an idiopathic inflammatory myopathy involving severe debilitation in need of diagnostics. We evaluated the proximal lower extremity musculature with diffusion tensor imaging (DTI), intravoxel incoherent motion (IVIM) and dynamic DTI in DM patients and controls and compared with standard clinical workup. 

Methods

In this IRB-approved, HIPAA-compliant study with written informed consent, anatomical, Dixon fat/water and diffusion imaging were collected in bilateral thigh MRI of 22 controls and 27 DM patients in a 3T scanner. Compartments were scored on T1/T2 scales. Single voxel dynamic DTI metrics in quadriceps before and after 3-min leg exercise were measured. Spearman rank correlation and mixed model analysis of variance/covariance (ANOVA/ANCOVA) were used to correlate with T1 and T2 scores and to compare patients with controls.

Results

DM patients showed significantly lower pseudo-diffusion and volume in quadriceps than controls. All subjects showed significant correlation between T1 score and signal-weighted fat fraction; tissue diffusion and pseudo-diffusion varied significantly with T1 and T2 score in patients. Radial and mean diffusion exercise response in patients was significantly higher than controls.

Conclusion

Static and dynamic diffusion imaging metrics show correlation with conventional imaging scores, reveal spatial heterogeneity, and provide means to differentiate dermatomyositis patients from controls.

Key Points

• Diffusion imaging shows regional differences between thigh muscles of dermatomyositis patients and controls.

• Signal-weighted fat fraction and diffusion metrics correlate with T1/T2 scores of disease severity.

• Dermatomyositis patients show significantly higher radial diffusion exercise response than controls.

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Change history

  • 09 July 2018

    The original version of this article, published on 04 June 2018, unfortunately contained a mistake.

Abbreviations

AD:

Adductor magnus

ANCOVA:

Analysis of covariance

ANOVA:

Analysis of variance

BF:

Biceps femoris

CK:

Creatine kinase

DM:

Dermatomyositis

DTI:

Diffusion tensor imaging

DWI:

Diffusion-weighted imaging

ECG:

Electrocardiogram

FA:

Fractional anisotropy

GRE:

Gradient echo

IVIM:

Intravoxel incoherent motion

MD:

Mean diffusivity

MMT:

Manual muscle test

PC:

Phase contrast

RF:

Rectus femoris

ROI:

Region of interest

SM:

Semimembranosus

SPAIR:

Spectral adiabatic inversion recovery

ST:

Semitendinosus

SV-MEDITATE:

Single voxel multiple echo diffusion tensor acquisition technique

SWFF:

Signal-weighted fat fraction

TSE:

Turbo spin echo

VI:

Vastus intermedius

VL:

Vastus lateralis

VM:

Vastus medialis

References

  1. Basser PJ (1995) Inferring microstructural features and the physiological state of tissues from diffusion-weighted images. NMR Biomed 8:333–344

    Article  CAS  Google Scholar 

  2. Galban CJ, Maderwald S, Uffmann K, de Greiff A, Ladd ME (2004) Diffusive sensitivity to muscle architecture: a magnetic resonance diffusion tensor imaging study of the human calf. Eur J Appl Physiol 93:253–262

    Article  Google Scholar 

  3. Li K, Dortch RD, Welch EB et al (2014) Multi-parametric MRI characterization of healthy human thigh muscles at 3.0 T - relaxation, magnetization transfer, fat/water, and diffusion tensor imaging. NMR Biomed 27:1070–1084

    Article  Google Scholar 

  4. Sinha S, Sinha U, Edgerton VR (2006) In vivo diffusion tensor imaging of the human calf muscle. J Magn Reson Imaging 24:182–190

    Article  Google Scholar 

  5. Zaraiskaya T, Kumbhare D, Noseworthy MD (2006) Diffusion tensor imaging in evaluation of human skeletal muscle injury. J Magn Reson Imaging 24:402–408

    Article  Google Scholar 

  6. Qi J, Olsen NJ, Price RR, Winston JA, Park JH (2008) Diffusion-weighted imaging of inflammatory myopathies: polymyositis and dermatomyositis. J Magn Reson Imaging 27:212–217

    Article  Google Scholar 

  7. Karampinos DC, King KF, Sutton BP, Georgiadis JG (2010) Intravoxel partially coherent motion technique: characterization of the anisotropy of skeletal muscle microvasculature. J Magn Reson Imaging 31:942–953

    Article  Google Scholar 

  8. Morvan D (1995) In vivo measurement of diffusion and pseudo-diffusion in skeletal muscle at rest and after exercise. Magn Reson Imaging 13:193–199

    Article  CAS  Google Scholar 

  9. Zhou H, Novotny JE (2007) Cine phase contrast MRI to measure continuum Lagrangian finite strain fields in contracting skeletal muscle. J Magn Reson Imaging 25:175–184

    Article  Google Scholar 

  10. Litwiller DV, Amrami KK, Dahm DL et al (2007) Chronic exertional compartment syndrome of the lower extremities: improved screening using a novel dual birdcage coil and in-scanner exercise protocol. Skeletal Radiol 36:1067–1075

    Article  Google Scholar 

  11. Bendahan D, Giannesini B, Cozzone PJ (2004) Functional investigations of exercising muscle: a noninvasive magnetic resonance spectroscopy-magnetic resonance imaging approach. Cell Mol Life Sci 61:1001–1015

    Article  CAS  Google Scholar 

  12. Andreisek G, White LM, Sussman MS et al (2009) T2*-Weighted and Arterial Spin Labeling MRI of Calf Muscles in Healthy Volunteers and Patients With Chronic Exertional Compartment Syndrome: Preliminary Experience. AJR Am J Roentgenol 193:W327–W333

    Article  Google Scholar 

  13. Ababneh ZQ, Ababneh R, Maier SE et al (2008) On the correlation between T(2) and tissue diffusion coefficients in exercised muscle: quantitative measurements at 3T within the tibialis anterior. MAGMA 21:273–278

    Article  CAS  Google Scholar 

  14. Morvan D, Leroy-Willig A, Malgouyres A, Cuenod CA, Jehenson P, Syrota A (1993) Simultaneous temperature and regional blood volume measurements in human muscle using an MRI fast diffusion technique. Magn Reson Med 29:371–377

    Article  CAS  Google Scholar 

  15. Filli L, Boss A, Wurnig MC, Kenkel D, Andreisek G, Guggenberger R (2015) Dynamic intravoxel incoherent motion imaging of skeletal muscle at rest and after exercise. NMR Biomed 28:240–246

    Article  Google Scholar 

  16. Tomasova Studynkova J, Charvat F, Jarosova K, Vencovsky J (2007) The role of MRI in the assessment of polymyositis and dermatomyositis. Rheumatology (Oxford) 46:1174–1179

    Article  CAS  Google Scholar 

  17. 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 87:20140261

    Article  CAS  Google Scholar 

  18. Rockel C, Akbari A, Kumbhare DA, Noseworthy MD (2017) Dynamic DTI (dDTI) shows differing temporal activation patterns in post-exercise skeletal muscles. MAGMA 30:127–138

    Article  Google Scholar 

  19. Mammen AL (2010) Dermatomyositis and polymyositis: Clinical presentation, autoantibodies, and pathogenesis. Ann N Y Acad Sci 1184:134–153

    Article  CAS  Google Scholar 

  20. Arnson Y, Dovrish Z, Hadari R, Amital H (2007) Amyopathic dermatomyositis--an uncommon presentation of dermatomyositis. Isr Med Assoc J 9:492–493

    PubMed  Google Scholar 

  21. Sato S, Kuwana M (2010) Clinically amyopathic dermatomyositis. Curr Opin Rheumatol 22:639–643

    Article  Google Scholar 

  22. Ghazi E, Sontheimer RD, Werth VP (2013) The importance of including amyopathic dermatomyositis in the idiopathic inflammatory myositis spectrum. Clin Exp Rheumatol 31:128–134

    PubMed  Google Scholar 

  23. Schnabel A, Reuter M, Biederer J, Richter C, Gross WL (2003) Interstitial lung disease in polymyositis and dermatomyositis: clinical course and response to treatment. Semin Arthritis Rheum 32:273–284

    Article  Google Scholar 

  24. Lam WW, Chan H, Chan YL, Fung JW, So NM, Metreweli C (1999) MR imaging in amyopathic dermatomyositis. Acta Radiol 40:69–72

    Article  CAS  Google Scholar 

  25. Barsotti S, Zampa V, Talarico R et al (2016) Thigh magnetic resonance imaging for the evaluation of disease activity in patients with idiopathic inflammatory myopathies followed in a single center. Muscle Nerve 54:666–672

    Article  CAS  Google Scholar 

  26. Ran J, Liu Y, Sun D et al (2016) The diagnostic value of biexponential apparent diffusion coefficients in myopathy. J Neurol 263:1296–1302

    Article  CAS  Google Scholar 

  27. Baete SH, Cho G, Sigmund EE (2013) Multiple-echo diffusion tensor acquisition technique (MEDITATE) on a 3T clinical scanner. NMR Biomed 26:1471–1483

    Article  Google Scholar 

  28. Baete SH, Cho GY, Sigmund EE (2015) Dynamic diffusion-tensor measurements in muscle tissue using the single-line multiple-echo diffusion-tensor acquisition technique at 3T. NMR Biomed 28:667–678

    Article  Google Scholar 

  29. Burakiewicz J, Hooijmans MT, Webb AG, Verschuuren J, Niks EH, Kan HE (2018) Improved olefinic fat suppression in skeletal muscle DTI using a magnitude-based dixon method. Magn Reson Med 79:152–159

    Article  CAS  Google Scholar 

  30. Varnier GC, Rosina S, Ferrari C et al (2017) Development and testing of a hybrid measure of muscle strength in juvenile dermatomyositis for use in routine care. Arthritis Care Res. https://doi.org/10.1002/acr.23491

    Article  Google Scholar 

  31. Poulsen KB, Alexanderson H, Dalgård C, Jacobsen S, Weile L, Diederichsen LP (2017) Quality of life correlates with muscle strength in patients with dermato- or polymyositis. Clin Rheumatol 36:2289–2295

    Article  Google Scholar 

  32. Rider LG, Koziol D, Giannini EH et al (2010) Validation of manual muscle testing and a subset of eight muscles for adult and juvenile idiopathic inflammatory myopathies. Arthritis Care Res 62:465–472

    Article  Google Scholar 

  33. Kim HK, Laor T, Horn PS, Racadio JM, Wong B, Dardzinski BJ (2010) T2 mapping in Duchenne muscular dystrophy: distribution of disease activity and correlation with clinical assessments. Radiology 255:899–908

    Article  Google Scholar 

  34. Mercuri E, Pichiecchio A, Allsop J, Messina S, Pane M, Muntoni F (2007) Muscle MRI in inherited neuromuscular disorders: past, present, and future. J Magn Reson Imaging 25:433–440

    Article  Google Scholar 

  35. Carlo B, Roberta P, Stramere R, Marina F, Corrado A (2006) Limb-girdle Muscular Dystrophies Type 2A and 2B: Clinical and Radiological Aspects. Basic Appl Myology 16:17–25

    Google Scholar 

  36. 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

    Article  Google Scholar 

  37. Steidle G, Schick F (2015) Addressing spontaneous signal voids in repetitive single-shot DWI of musculature: spatial and temporal patterns in the calves of healthy volunteers and consideration of unintended muscle activities as underlying mechanism. NMR Biomed 28:801–810

    Article  Google Scholar 

  38. Yao L, Sinha U (2000) Imaging the microcirculatory proton fraction of muscle with diffusion-weighted echo-planar imaging. Acad Radiol 7:27–32

    Article  CAS  Google Scholar 

  39. Guiu B, Petit JM, Capitan V et al (2012) Intravoxel incoherent motion diffusion-weighted imaging in nonalcoholic fatty liver disease: a 3.0-T MR study. Radiology 265:96–103

    Article  Google Scholar 

  40. Cho GY, Moy L, Zhang JL et al (2015) Comparison of fitting methods and b-value sampling strategies for intravoxel incoherent motion in breast cancer. Magn Reson Med 74:1077–1085

    Article  Google Scholar 

  41. Hooijmans MT, Damon BM, Froeling M et al (2015) Evaluation of skeletal muscle DTI in patients with duchenne muscular dystrophy. NMR Biomed 28:1589–1597

    Article  CAS  Google Scholar 

  42. Hernando D, Karampinos DC, King KF et al (2011) Removal of olefinic fat chemical shift artifact in diffusion MRI. Magn Reson Med 65:692–701

    Article  CAS  Google Scholar 

  43. Hsu EW, Mori S (1995) Analytical expressions for the NMR apparent diffusion coefficients in an anisotropic system and a simplified method for determining fiber orientation. Magn Reson Med 34:194–200

    Article  CAS  Google Scholar 

  44. Karampinos DC, King KF, Sutton BP, Georgiadis JG (2009) Myofiber ellipticity as an explanation for transverse asymmetry of skeletal muscle diffusion MRI in vivo signal. Ann Biomed Eng 37:2532–2546

    Article  Google Scholar 

  45. Galban CJ, Maderwald S, Uffmann K, Ladd ME (2005) A diffusion tensor imaging analysis of gender differences in water diffusivity within human skeletal muscle. NMR Biomed 18:489–498

    Article  Google Scholar 

  46. Damon BM (2008) Effects of image noise in muscle diffusion tensor (DT)-MRI assessed using numerical simulations. Magn Reson Med 60:934–944

    Article  Google Scholar 

  47. Yoon MA, Hong SJ, Ku MC, Kang CH, Ahn KS, Kim BH (2017) Multiparametric MR imaging of age-related changes in healthy thigh muscles. Radiology. https://doi.org/10.1148/radiol.2017171316:171316

  48. Froeling M, Oudeman J, Strijkers GJ et al (2015) Muscle changes detected with diffusion-tensor imaging after long-distance running. Radiology 274:548–562

    Article  Google Scholar 

  49. Scheel M, von Roth P, Winkler T et al (2013) Fiber type characterization in skeletal muscle by diffusion tensor imaging. NMR Biomed 26:1220–1224

    Article  Google Scholar 

  50. Nguyen A, Ledoux JB, Omoumi P, Becce F, Forget J, Federau C (2017) Selective microvascular muscle perfusion imaging in the shoulder with intravoxel incoherent motion (IVIM). Magn Reson Imaging 35:91–97

    Article  Google Scholar 

  51. Filli L, Wurnig MC, Luechinger R, Eberhardt C, Guggenberger R, Boss A (2015) Whole-body intravoxel incoherent motion imaging. Eur Radiol 25:2049–2058

    Article  Google Scholar 

  52. Sasaki M, Sumi M, Van Cauteren M, Obara M, Nakamura T (2013) Intravoxel incoherent motion imaging of masticatory muscles: pilot study for the assessment of perfusion and diffusion during clenching. AJR Am J Roentgenol 201:1101–1107

    Article  Google Scholar 

  53. Lemke A, Laun FB, Simon D, Stieltjes B, Schad LR (2010) An in vivo verification of the intravoxel incoherent motion effect in diffusion-weighted imaging of the abdomen. Magn Reson Med 64:1580–1585

    Article  Google Scholar 

  54. Sjogaard G, Saltin B (1982) Extra- and intracellular water spaces in muscles of man at rest and with dynamic exercise. Am J Phys 243:R271–R280

    CAS  Google Scholar 

  55. Saab G, Thompson RT (1985) Marsh GD (2000) Effects of exercise on muscle transverse relaxation determined by MR imaging and in vivo relaxometry. J Appl Physiol 88:226–233

    Article  Google Scholar 

  56. Schwenzer NF, Steidle G, Martirosian P et al (2009) Diffusion tensor imaging of the human calf muscle: distinct changes in fractional anisotropy and mean diffusion due to passive muscle shortening and stretching. NMR Biomed 22:1047–1053

    PubMed  Google Scholar 

  57. Deux JF, Malzy P, Paragios N et al (2008) Assessment of calf muscle contraction by diffusion tensor imaging. Eur Radiol 18:2303–2310

    Article  CAS  Google Scholar 

  58. Partovi S, Karimi S, Jacobi B et al (2012) Clinical implications of skeletal muscle blood-oxygenation-level-dependent (BOLD) MRI. MAGMA 25:251–261

    Article  CAS  Google Scholar 

  59. Parasoglou P, Xia D, Chang G, Regatte RR (2013) Dynamic three-dimensional imaging of phosphocreatine recovery kinetics in the human lower leg muscles at 3T and 7T: a preliminary study. NMR Biomed 26:348–356

    Article  CAS  Google Scholar 

  60. Okamoto T, Kanazawa H, Hirata K, Yoshikawa J (2003) Evaluation of oxygen uptake kinetics and oxygen kinetics of peripheral skeletal muscle during recovery from exercise in patients with chronic obstructive pulmonary disease. Clin Physiol Funct Imaging 23:257–262

    Article  Google Scholar 

  61. Reeder SB, McKenzie CA, Pineda AR et al (2007) Water-fat separation with IDEAL gradient-echo imaging. J Magn Reson Imaging 25:644–652

    Article  Google Scholar 

  62. Clendenen TV, Zeleniuch-Jacquotte A, Moy L, Pike MC, Rusinek H, Kim S (2013) Comparison of 3-point Dixon imaging and fuzzy C-means clustering methods for breast density measurement. J Magn Reson Imaging 38:474–481

    Article  Google Scholar 

  63. Knoll F, Raya JG, Halloran RO et al (2015) A model-based reconstruction for undersampled radial spin-echo DTI with variational penalties on the diffusion tensor. NMR Biomed 28:353–366

    Article  Google Scholar 

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Funding

The authors state that this work has not received any funding.

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Authors

Corresponding author

Correspondence to E. E. Sigmund.

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Guarantor

The scientific guarantor of this publication is Eric E. Sigmund, PhD.

Conflict of interest

The authors of this manuscript declare no relationships with any companies whose products or services may be related to the subject matter of the article.

Statistics and biometry

One of the authors (J.S. Babb) has significant statistical expertise.

Informed consent

Written informed consent was obtained from all subjects (patients) in this study.

Ethical approval

Institutional Review Board approval was obtained.

Methodology

• prospective

• cross-sectional study

• performed at one institution

Additional information

The original version of this article was revised: The name of A.G. Franks was presented incorrectly and one of his affiliations was missing.

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Sigmund, E.E., Baete, S.H., Luo, T. et al. MRI assessment of the thigh musculature in dermatomyositis and healthy subjects using diffusion tensor imaging, intravoxel incoherent motion and dynamic DTI. Eur Radiol 28, 5304–5315 (2018). https://doi.org/10.1007/s00330-018-5458-3

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  • DOI: https://doi.org/10.1007/s00330-018-5458-3

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