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Pilot study on facioscapulohumeral muscular dystrophy patients with dynamic phase contrast imaging of electrically stimulated quadriceps muscles
Xeni Deligianni1,2, Francesco Santini1,2, Giorgio Tasca3, Mauro Monforte3, Francesca Solazzo4, Raimondo Vitale5, Paolo Felisaz6, Giancarlo Germani4, Niels Bergsland4, Enzo Ricci3, and Anna Pichiecchio4

1Department of Radiology/Division of Radiological Physics, University Hospital Basel, Basel, Switzerland, 2Department of Biomedical Engineering, University of Basel, Basel, Switzerland, 3Unità Operativa Complessa di Neurologia, Dipartimento di Scienze dell’Invecchiamento, Neurologiche, Ortopediche e della Testa-Collo, Fondazione Policlinico Universitario A. Gemelli IRCCS, Rome, Italy, 4Neuroradiology Department, IRCCS Mondino Foundation, Pavia, Italy, 5University of Pavia, Pavia, Switzerland, 6Radiology Department, Desio Hospital ASST, Monza, Italy

Synopsis

Facioscapulohumeral muscular dystrophy is characterized by a peculiar non-linear muscle-by-muscle involvement and is very hard to predict. The purpose of this study was to use dynamic phase contrast MR imaging of electrically stimulated quadriceps muscle to characterize the elastic potential of the muscle in FSHD patients and contribute to the understanding of this challenging disease. Velocity, strain, and strain rate were analyzed and compared to the results of physical examination.

Purpose

Facioscapulohumeral muscular dystrophy (FSHD) is characterized by a peculiar non-linear muscle-by-muscle involvement, and there is evidence that changes in T2-STIR images precede irreversible fat infiltration1-4. Even though quantitative MRI is already used for FSHD follow-up, progression of the disease is very hard to predict. The purpose of this study was to use dynamic phase contrast MR imaging of electrically stimulated quadriceps muscle5 to characterize the elastic potential of the muscle in FSHD patients and contribute to the understanding of this challenging disease.

Methods

18 patients (13 male/5 female) suffering from FSHD were scanned on a clinical 3T MRI. The protocol included dynamic MRI5 of the quadriceps on both legs. Clinical Severity Scores (CSS)4 and dynamometry measurements (force peak measured in kilos) were acquired, as well as 6-minutes walking test (6MWT).

For the MRI acquisition, a commercial electrical muscle stimulation (EMS) device was synchronized with a three-directional high-temporal-resolution cine phase contrast (PC) velocity encoding acquisition at 3T5. The stimulator electrodes were placed prior to the scan by identifying the motor point, and the current was set to a sufficient level to evoke muscle twitching without knee extension. Occasionally, this level was reduced at the moment of the MR acquisition because of increased patient discomfort. During periodic contraction of the quadriceps muscle group, a parasagittal slice was acquired with voxels of 2.3x2.3x5 mm3 and a temporal resolution of 42 ms. The velocity encoding had a VENC of 25 cm/s (TR/TE=10.6/7.21 ms, bandwidth/ pixel = 400 Hz/Px, flip angle=10°, FOV=225x300 mm2, 1 k-space line per segment, acquisition time 5 min) and 94 temporal phases were acquired. Each contraction cycle lasted 5 s (1 s ramp-up, 1 s contraction, 1 s ramp-down, 2 s relaxation). Strain rate and strain vectors (over the whole vastus lateralis and vastus intermedius) were extracted from the velocity fields5,6 and normalized by the value of stimulation current for comparison. Texture analysis (gray level co-occurrence matrices (i.e., contrast properties)) was performed on the strain and strain rate maps. Finally, the rate of decay of the strain after removal of the stimulus was estimated from the time curves by fitting of a sigmoid curve.

Pearson’s correlation coefficients were calculated between the MR quantities and the clinical indices (dynamometry and 6MWT).

Results

Both dynamometry variables and 6MWT were acquired for 10 patients (3 extra only had dynamometry). Dynamic MR data were successfully acquired in all cases.

Our data did not show significant correlation of the CSS classification with the quantitative indices of the dynamic acquisitions. However, the patients with lower CSS scores (i.e. less affected by the disease) generally exhibited a larger activated area (Figure 1a). From the analysis of 2D velocities, instead of two distinctive peaks around the moment of the beginning of the stimulation and the moment of release, some intermediate activation was also occasionally present or even a 3rd distinctive peak (Figure 1b). Occasionally though for higher CSS, there was absence of distinctive peaks.

In the strain maps (Figure 2), at the point of highest strain, maximum “activation” was either along the muscle length or localized and in many cases the two legs exhibited very different patterns. Similar effects were seen on the strain rate maps (see Figure 3). While the first strain rate peak map (see Figure 3) provided similar information as the maximum strain, the second peak (at the time point of muscle released from the contraction) yielded different localized information.

Regarding the physical examination, weak correlations of strain and strain rate values with 6MWT (see Figure 4) were found, while correlations were stronger between the 6MWT results and the contrast indices. Finally, the decay rates correlated with the dynamometry with r = 0.61 (Figure 5).

Discussion

The purpose of this study was to investigate the feasibility of using dynamic phase contrast MRI to study electrically stimulated muscle response in FSHD patients. The results so far have shown that even though the results concur with the 6MWT and dynamometry, they do not always agree with the CSS evaluation. In some cases with equal CSS scores, the activation areas were very different and in addition for a patient with CSS=4.5 the activation area and strain magnitude were much higher than expected, an observation that requires further investigation.

Conclusion

MRI of EMS-controlled involuntary muscle contraction in FSHD patients yields strain and strain rate values that agree with some of the physical examination results, but not always with the clinical evaluation. Further investigation will show whether this dynamic evaluation of the muscle deformation can predict the disease evolution before other MRI acquisitions.

Acknowledgements

This work was supported by the Swiss National Science Foundation (grant Nr. 172876) and by the Italian Ministry of Health (RC 2018-2020).

References

  1. Padberg GW, van Engelen BG, Facioscapulohumeral muscular dystrophy. Curr Opin Neurol 2009; 22: 539–542.
  2. Tasca G, Pescatori M, Monforte M, Mirabella M, Iannaccone E, Frusciante R, et al., Different Molecular Signatures in Magnetic Resonance Imaging-Staged Facioscapulohumeral Muscular Dystrophy Muscles. PLoS ONE 2012; 7(6): e38779.
  3. Tasca G., Monforte M., Ottaviani P., Pelliccioni M., Frusciante M., Laschena F., Ricci E., Magnetic resonance imaging in a large cohort of facioscapulohumeral muscular dystrophy patients: Pattern refinement and implications for clinical trials, Ann Neurol 2016;79:854–864.
  4. Ricci E, Galluzzi G, Deidda G, et al. Progress in the molecular diagnosis of facioscapulohumeral muscular dystrophy and correlation between the number of KpnI repeats at the 4q35 locus and clinical phenotype. Ann Neurol 1999;45:751–757.
  5. Deligianni X., Pansini M., Garcia M., Hirschmann A., Schmidt‐Trucksäss A., Bieri O., Santini F., Synchronous MRI of muscle motion induced by electrical stimulation, Magn Reson Med 2017; 77(2):664-672 .
  6. Sinha U., Malis V., Csapo R., Moghadasi A., Kinugasa R., and Sinha S. Age-Related Differences in Strain Rate Tensor of the Medial Gastrocnemius Muscle During Passive Plantarflexion and Active Isometric Contraction Using Velocity Encoded MR Imaging: Potential Index of Lateral Force Transmission, Magn Reson Med 2015; 73:1852–1863.

Figures

Figure 1.a. An example of velocity maps from six exemplary patients with different CSS classifications. The frame showing the beginning of contraction is shown here. The color-coded vectors show the direction of motion. CSS range: 1=No awareness of symptoms-5wheelchair bound, b. Respective 2D velocity curves.

Figure 2. Strain maps of both left and right leg for six exemplary patients for the time frame with maximum strain magnitude.

Figure 3. Strain rate maps of both left and right leg for six exemplary patients. Both peaks of strain rate are presented here (i.e., at the moment of the beginning of the contraction and at the moment of muscle release).

Figure 4. Maximum strain and magnitude of first and second strain rate in 10 patients where 6MWT could be assessed: (up) original strain/ strain values versus 6MWT results, (down) contrast of strain and strain rate values versus 6MWT results. Correlation (r) values are given for every parameter comparison.

Figure 5. Negative rate of strain time curves versus dynamometry results in 13 patients (r = 0.61458).

Proc. Intl. Soc. Mag. Reson. Med. 27 (2019)
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