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A conceptual framework: the early and late phases of skeletal muscle dysfunction in the acute respiratory distress syndrome

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Abstract

Patients with acute respiratory distress syndrome (ARDS) often develop severe diaphragmatic and limb skeletal muscle dysfunction. Impaired muscle function in ARDS is associated with increased mortality, increased duration of mechanical ventilation, and functional disability in survivors. In this review, we propose that muscle dysfunction in ARDS can be categorized into an early and a late phase. These early and late phases are based on the timing in relationship to lung injury and the underlying mechanisms. The early phase occurs temporally with the onset of lung injury, is driven by inflammation and disuse, and is marked predominantly by muscle atrophy from increased protein degradation. The ubiquitin-proteasome, autophagy, and calpain-caspase pathways have all been implicated in early-phase muscle dysfunction. Late-phase muscle weakness persists in many patients despite resolution of lung injury and cessation of ongoing acute inflammation-driven muscle atrophy. The clinical characteristics and mechanisms underlying late-phase muscle dysfunction do not involve the massive protein degradation and atrophy of the early phase and may reflect a failure of the musculoskeletal system to regain homeostatic balance. Owing to these underlying mechanistic differences, therapeutic interventions for treating muscle dysfunction in ARDS may differ during the early and late phases. Here, we review clinical and translational investigations of muscle dysfunction in ARDS, placing them in the conceptual framework of the early and late phases. We hypothesize that this conceptual model will aid in the design of future mechanistic and clinical investigations of the skeletal muscle system in ARDS and other critical illnesses.

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Abbreviations

AKT:

Protein kinase B

ARDS:

Acute respiratory distress syndrome

FoxO:

Forkhead box o

GLUT4:

Glucose transporter-4

ICUAW:

Intensive care unit-acquired weakness

IGF-1:

Insulin like growth factor 1

IL:

Interleukin

MMT:

Manual muscle testing

MuRF1:

Muscle ring finger 1

MyHC:

Myosin heavy chain

NF-κB:

Nuclear factor kappa light chain enhancer of activated B cells

NMB:

Neuromuscular blockade

NMES:

Neuromuscular electrical stimulation

NMJ:

Neuromuscular junction

PN:

Parenteral nutrition

UPS:

Ubiquitin-proteasome system

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Acknowledgments

DCF would like to thank his mentors, Michael T Crow and Landon S King, without whom none of this work would be possible. The authors thank Karen Klein for editorial assistance and Nick Weir at Creative Communications for the illustrations. This work was supported by institutional funds from the Wake Forest School of Medicine, the Department of Medicine (DCF), the Claude D. Pepper Older Americans Independence Center (grant P30-AG21332), the Parker B. Francis Foundation (DCF), the American Thoracic Society Foundation (DCF), the National Institutes of Health (grant 1R01NR011186-01 to PEM), and the Department of the Army (ERMS #12340010 to PEM).

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Authors and Affiliations

  1. Section on Pulmonary, Critical Care, Allergy and Immunologic Diseases, Wake Forest School of Medicine, Medical Center Boulevard, Winston-Salem, NC, 27157, USA

    D. Clark Files, Michael A. Sanchez & Peter E. Morris

  2. Critical Illness Injury and Recovery Research Center Chadwick Miller MD Department of Emergency Medicine, Wake Forest School of Medicine, Medical Center Boulevard, Winston-Salem, NC, 27157, USA

    D. Clark Files & Peter E. Morris

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  1. D. Clark Files
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  2. Michael A. Sanchez
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  3. Peter E. Morris
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Correspondence to D. Clark Files.

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The authors declare that they have no competing interests.

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Files, D.C., Sanchez, M.A. & Morris, P.E. A conceptual framework: the early and late phases of skeletal muscle dysfunction in the acute respiratory distress syndrome. Crit Care 19, 266 (2015). https://doi.org/10.1186/s13054-015-0979-5

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