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

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

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.

Figures

Fig. 1
Fig. 1
The early and late phases of muscle wasting in acute respiratory distress syndrome. The early phase of muscle wasting begins with the onset of lung injury and is caused by lung and systemic inflammation and to a lesser degree disuse, both leading to muscle atrophy. The late phase of muscle wasting begins as lung function recovers and acute systemic inflammation resolves. Disuse continues in many patients during the late phase. Muscle function deteriorates in the early phase, and dysfunction persists in many patients during the late phase, which may last for years despite resolution of lung injury and cessation of ongoing muscle atrophy. Factors mediating recovery trajectories in the late phase are poorly understood
Fig. 2
Fig. 2
Mediators of acute respiratory distress syndrome (ARDS)-induced muscle dysfunction. Skeletal muscle atrophy is the most universal feature of the early phase, which is driven fundamentally by inflammation and disuse. Other factors such as neuropathic injury and medications can exacerbate atrophy (blue arrow) and independently cause muscle dysfunction. Therefore, inhibiting muscle protein degradation is the most promising potential early-phase therapy. The late phase is marked by cessation of inflammation-induced muscle proteolysis and therefore potential treatments at this time point will differ. Mediators of the late phase may involve persistence of some early-phase injuries or a failure to regain muscle homeostasis following the early phase. Late-phase dysfunction may be compounded by underlying pre-ARDS neuromuscular defects. NMJ, neuromuscular junction; SR Ca+, sarcoplasmic reticulum calcium; UPS, ubiquitin-proteasome system

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