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Atrophy of Calf Muscles by Unloading Results in an Increase of Tissue Sodium Concentration and Fat Fraction Decrease: a 23Na MRI Physiology Study

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Atrophy of Calf Muscles by Unloading Results in an Increase of Tissue Sodium Concentration and Fat Fraction Decrease: a 23Na MRI Physiology Study Atrophy of calf muscles by unloading results in an increase of tissue sodium concentration and fat fraction decrease: a 23Na MRI physiology study D. A. Gerlach, K. Schopen, P. Linz, B. Johannes, J. Titze, J. Zange & J. Rittweger European Journal of Applied Physiology ISSN 1439-6319 Eur J Appl Physiol DOI 10.1007/s00421-017-3647-4 1 23 Your article is protected by copyright and all rights are held exclusively by Springer- Verlag Berlin Heidelberg. This e-offprint is for personal use only and shall not be self- archived in electronic repositories. If you wish to self-archive your article, please use the accepted manuscript version for posting on your own website. You may further deposit the accepted manuscript version in any repository, provided it is only made publicly available 12 months after official publication or later and provided acknowledgement is given to the original source of publication and a link is inserted to the published article on Springer's website. The link must be accompanied by the following text: "The final publication is available at link.springer.com”. 1 23 Author's personal copy Eur J Appl Physiol DOI 10.1007/s00421-017-3647-4 ORIGINAL ARTICLE Atrophy of calf muscles by unloading results in an increase of tissue sodium concentration and fat fraction decrease: a 23Na MRI physiology study D. A. Gerlach1 · K. Schopen1,2 · P. Linz3,4 · B. Johannes1 · J. Titze4,5 · J. Zange1 · J. Rittweger1,6 Received: 3 March 2017 / Accepted: 17 May 2017 © Springer-Verlag Berlin Heidelberg 2017 Abstract scanner. For quantifcation, a sodium reference phantom Purpose 23Na MRI demonstrated increased tissue sodium was used with 10, 20, 30, and 40 mmol/L NaCl solution. concentrations in a number of pathologies. Acute atrophy Result Tissue sodium concentration (TSC) increased as an results in muscle fbre volume shrinking that may result in effect of unloading in the orthosis leg. Relative increases a relative increase of extracellular volume and might affect were 17.4 16.8% (P 0.005) in gastrocnemius media- ± = sodium concentration. Thus, we hypothesized that local lis muscle, 11.1 12.5 (P 0.037) in gastrocnemius lat- ± = unloading of the calf muscles would lead to a decrease in eralis muscle, 16.2 4.7% (P < 0.001) in soleus muscle, ± muscle volume and an increase in muscle tissue sodium 10.0 10.5% (P 0.009) in the ventral muscle group, ± = concentration. and 10.7 10.0% (P 0.003) in the central muscle group, ± = Method One lower leg of 12 healthy male subjects was respectively. TSC in the control leg did not signifcantly submitted to a 60 day long period of unloading using the change. In the orthosis leg, muscle volume decreased Hephaistos orthosis, while the other leg served as control. as follows: medial gastrocnemius muscle: 5.4 8.3% − ± 23Na MRI and 2D PD-weighted Dixon turbo spin echo (P 0.043) and soleus muscle: 7.8 15.0% (P 0.043). = − ± = were obtained from the control and orthosis leg using a 3T Conclusion Unloading atrophy is associated with an increase in muscle sodium concentration. 23Na MRI is capable of detecting these rather small changes. Communicated by Guido Ferretti. Keywords Sodium · MRI · 23Na MRI · Tissue sodium concentration (TSC) · Quantifcation · Muscle unloading * D. A. Gerlach [email protected] Abbreviations 1 Division of Space Physiology, Institute of Aerospace FoV Field of view (FoV) Medicine, German Aerospace Center (DLR), Cologne, LME Linear mixed effects Germany PD Proton density 2 Department of Molecular and Cellular Sport Medicine, ROI Regions of interest German Sport University Cologne, Cologne, Germany SNR Signal-to-noise ratio 3 Department of Radiology, University Hospital Erlangen, TSC Tissue sodium concentration Erlangen, Germany TSE Turbo spin echo 4 Interdisciplinary Center for Clinical Research, TA Acquisition time Nikolaus‑Fiebiger‑Center for Molecular Medicine, Friedrich- Alexander-University Erlangen-Nürnberg, Erlangen, TE Echo time Germany TR Repetition time 5 Division of Clinical Pharmacology, Vanderbilt University T2 Transversal relaxation time Medical Center, Nashville, TN, USA 6 Department of Paediatrics and Adolescent Medicine, University of Cologne, Cologne, Germany 1 3 Author's personal copy Eur J Appl Physiol Introduction Boer 2011). Thus, muscle atrophy is defned here as muscle volume loss and function loss. Since muscle fbres contain The physiological interest in the independency of water only little intracellular sodium, fbre shrinkage is expected and sodium balance (Drummer et al. 2000) and in the to result in an increased relative portion of the extracellular non-osmotical storage of sodium in skin and muscle tis- Na rich compartment and, thus, in an increase in the appar- sue (Titze et al. 2003) is currently sharply increasing. ent 23Na concentration in MRI muscle scans. However, As a consequence, 23Na MRI has recently also become a such changes in Na concentration in response to atrophy prominent topic in MRI methodology and pathophysiol- have not yet been assessed. ogy as well. Some groups have focused on method devel- We have recently developed an exoskeleton that effec- opment and feasibility studies and discussed their poten- tively unloads the mobilizing muscle group, the plantar tial for diagnostics (Lu et al. 2010; Nagel et al. 2009). fexor triceps surae muscles, as a model of localized mus- Clinically relevant topics have been addressed, such as cle immobilization model (Weber et al. 2013). At the same hypertension (Kopp et al. 2012, 2013), kidney failure time, this orthotic device leaves gait almost unaffected. (Dahlmann et al. 2015), cancer diagnostics (Ouwerkerk Now, we have used this model in the NutriHEP study (clin- et al. 2003), muscle diseases (Constantinides et al. 2000; ical trials number NCT02698878) to test the effectiveness Nagel et al. 2011; Weber et al. 2012), cartilage degenera- of a countermeasure intervention against muscle atrophy tion (Borthakur et al. 2000, 2006), spinal disc morphol- and insulin resistance (Zange et al. 2017). Here, we report ogy (Ooms et al. 2008), and multiple sclerosis (Inglese on the 23Na MRI data from this study. et al. 2010; Maarouf et al. 2014; Paling et al. 2013). We hypothesized an increase in sodium tissue concen- Sodium has a nuclear spin of 3/2 which leads to a quad- tration in the calf muscles due to unloading. This hypoth- rupolar moment when interacting with electric gradient esized effect should be explicable by shrinkage of muscle felds. Such a coupling causes one central transition and fbres. Accordingly, the secondary hypothesis was that the two satellite transitions in ordered environments, such as total 23Na content within the muscle would be unaffected human tissue. 60% of the NMR signal corresponds to the by the atrophy. Moreover, the water and fat composition two satellite transitions and 40% of the signal originates in the muscle was hypothesized to change towards higher from the central transition. Depending on the 23Na ion water content in the immobilized leg. binding, the transversal relaxation time (T2) can result in As a tertiary aim, we were interested in how atrophy two components. Within the tissue, the two satellite transi- induced by the Hephaistos orthosis would affect the fat/ tions result in a fast T2 decay, whereas the central transi- water constitution of skeletal muscle. This is because lack tion exhibits a slow T2 decay (Bansal et al. 2000; Ra et al. of physical activity and old age has been associated with in 1986). The fact that 60% of the signal is fast decaying intramuscular fat accumulation as assessed by radiological in human tissue makes 23Na MRI challenging. Fast echo techniques (Goodpaster et al. 2000). Contrary to the idea of time and sophisticated acquisition methods are required, increases fat content as a sign of muscle disuse, however, and achieving suffcient signal to noise is time consum- we had observed increases in muscular X-ray absorption ing. That is why 23Na MRI is still under development and in response to bed rest (Rittweger et al. 2013). As X-ray mostly used in pre-clinical studies. The methodological based approaches are not specifc for the assessment of developments have recently been reviewed (Konstandin lipid content, other factors such as enrichment of intramus- and Nagel 2014; Madelin and Regatte 2013). cular blood content could explain that observation. Thus, to A few studies have already applied 23Na MRI in skel- further clarify whether there are changes in intramuscular etal muscle. For example, it has been shown that the tissue lipid content as a result of immobilization, we also strived sodium concentration (TSC: defned as tissue 23Na content to assess muscular fat content in the present study. per volume) increased by 34% 7% during one leg toe lift ± exercise (3–4 min) (Bansal et al. 2000) or hoped on one leg till fatigue 8–13% (2 0.6 min) (Chang et al. 2010) Materials and methods ± compared to baseline. Furthermore, muscle disorders such as Duchenne’s dystrophy or channelopathies are associated Subjects with increased TSC (Nagel et al. 2011; Weber et al. 2012). Muscle wasting, at old age also called sarcopenia Fourteen healthy male subjects were recruited for this (Roubenoff 2000), is a physiological consequence of study. All of these subjects completed the interventional immobilization and unloading (Rittweger et al. 2005) and protocol, but two of them failed to attend one or more space fight (LeBlanc et al. 2000). MRI examinations and are, therefore, not included in the At least in young people, the disuse-related muscle atro- present analysis. The remaining 12 subjects had a mean phy is caused by shrinkage of muscle fbres (Narici and de age of 27.3 3.9 years and a mean body mass index of ± 1 3 Author's personal copy Eur J Appl Physiol 23.0 1.54 kg/m2 participated in the study.
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