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In vivo 31P NMR spectroscopy assessment of skeletal muscle bioenergetics after spinal cord contusion in rats

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Abstract

Purpose

Muscle paralysis after spinal cord injury leads to muscle atrophy, enhanced muscle fatigue, and increased energy demands for functional activities. Phosphorus magnetic resonance spectroscopy (31P-MRS) offers a unique non-invasive alternative of measuring energy metabolism in skeletal muscle and is especially suitable for longitudinal investigations. We determined the impact of spinal cord contusion on in vivo muscle bioenergetics of the rat hind limb muscle using 31P-MRS.

Methods

A moderate spinal cord contusion injury (cSCI) was induced at the T8–T10 thoracic spinal segments. 31P-MRS measurements were performed weekly in the rat hind limb muscles for 3 weeks. Spectra were acquired in a Bruker 11 T/470 MHz spectrometer using a 31P surface coil. The sciatic nerve was electrically stimulated by subcutaneous needle electrodes. Spectra were acquired at rest (5 min), during stimulation (6 min), and recovery (20 min). Phosphocreatine (PCr) depletion rates and the pseudo first-order rate constant for PCr recovery (k PCr) were determined. The maximal rate of PCr resynthesis, the in vivo maximum oxidative capacity (V max) and oxidative adenosine triphosphate (ATP) synthesis rate (Q max) were subsequently calculated.

Results

One week after cSCI, there was a decline in the resting total creatine of the paralyzed muscle. There was a significant reduction (~24 %) in k PCr measures of the paralyzed muscle, maximum in vivo mitochondrial capacity (V max) and the maximum oxidative ATP synthesis rate (Q max) at 1 week post-cSCI. During exercise, the PCr depletion rates in the paralyzed muscle one week after injury were rapid and to a greater extent than in a healthy muscle.

Conclusions

Using in vivo MRS assessments, we reveal an acute oxidative metabolic defect in the paralyzed hind limb muscle. These altered muscle bioenergetics might contribute to the host of motor dysfunctions seen after cSCI.

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Abbreviations

31P-MRS:

31 Phosphorus magnetic resonance spectroscopy

SCI:

Spinal cord injury

[ATP]:

Absolute concentration of biochemically determined free cytosolic adenosine triphosphate

[Pi]:

Absolute concentration of inorganic phosphate

[PCr]:

Absolute concentration of phosphocreatine

[ADP]:

Absolute concentration of free cytosolic adenosine diphosphate

[ADP] [Pi]/[ATP]:

Phosphorylation ratio

V dep :

PCr depletion rate at onset of exercise

k PCr :

Rate constant of PCr recovery

V max :

Mitochondrial oxidative capacity based on recovery rate constant

Q max :

Maximum oxidative ATP synthesis rates based on k PCr and [ADP], independent of pH

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Acknowledgments

This work was supported by the National Institutes of Health grant P01 HD059751-01A1 to K.V and the National High Magnetic Field Laboratory.

Conflict of interest

The authors declare that they have no conflict of interest.

Ethical standards

The authors declare that all experimental procedures were performed in accordance with and comply by the US Government Principle for the Utilization and Care of Vertebrate Animals by approval of the Institutional Animal Care & Use Committee at the University of Florida.

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Authors and Affiliations

  1. Department of Integrative Biology and Physiology, University of California in Los Angeles, 621 Charles E Young Dr, Los Angeles, CA, 90048, USA

    Prithvi K. Shah

  2. Department of Physical Therapy, University of Florida, Gainesville, FL, USA

    Fan Ye, Min Liu, Glenn Walter & Krista Vandenborne

  3. Rehabilitation Institute of Chicago, Chicago, IL, USA

    Arun Jayaraman

  4. Department of Physiology and Functional Genomics, University of Florida, Gainesville, FL, USA

    Celine Baligand & Glenn Walter

Authors
  1. Prithvi K. Shah
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  2. Fan Ye
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Correspondence to Prithvi K. Shah.

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Communicated by Dick F. Stegeman.

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Shah, P.K., Ye, F., Liu, M. et al. In vivo 31P NMR spectroscopy assessment of skeletal muscle bioenergetics after spinal cord contusion in rats. Eur J Appl Physiol 114, 847–858 (2014). https://doi.org/10.1007/s00421-013-2810-9

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  • DOI: https://doi.org/10.1007/s00421-013-2810-9

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