Symmorphosis and skeletal muscle : in vivo and in vitro measures reveal differing constraints in the exercise‐trained and untrained human

Abstract

Key pointsr The concept of symmorphosis predicts that the capacity of each step of the oxygen cascade is attuned to the task demanded of it during aerobic exercise at maximal rates of oxygen consumption (V O 2 max ) such that no single process is limiting or in excess atV O 2 max .r The present study challenges the applicability of this concept to humans by revealing clear, albeit very different, limitations and excesses in oxygen supply and consumption among untrained and endurance-trained humans.r Among untrained individuals,V O 2 max is limited by the capacity of the mitochondria to consume oxygen, despite an excess of oxygen supply, whereas, among trained individuals,V O 2 max is limited by the supply of oxygen to the mitochondria, despite an excess of mitochondrial respiratory capacity. AbstractThe concept of symmorphosis postulates a matching of structural capacity to functional demand within a defined physiological system, regardless of endurance exercise training status. Whether this concept applies to oxygen (O 2 ) supply and demand during maximal skeletal muscle O 2 consumption (V O 2 max ) in humans is unclear. Therefore, in vitro skeletal muscle mitochondrialV O 2 max ( MitoVO 2 max , mitochondrial respiration of fibres biopsied from vastus lateralis) was compared with in vivo skeletal muscleV O 2 max during single leg knee extensor exercise ( KEVO 2 max , direct Fick by femoral arterial and venous blood samples and Doppler ultrasound blood flow measurements) and whole-bodyV O 2 max during cycling ( BodyVO 2 max , indirect calorimetry) in 10 endurance exercise-trained and 10 untrained young males. In untrained subjects, during KE exercise, maximal O 2 supply ( KEQ O 2max ) exceeded (462 ± 37 ml kg −1 min −1 , P < 0.05) and KEVO 2 max matched (340 ± 22 ml kg −1 min −1 , P > 0.05) MitoVO 2 max (364 ± 16 ml kg −1 min −1 ). Conversely, in trained subjects, both KEQ O 2max (557 ± 35 ml kg −1 min −1 ) and KEVO 2 max (458 ± 24 ml kg −1 min −1 ) fell far short of MitoVO 2 max (743 ± 35 ml kg −1 min −1 , P < 0.05). Although MitoVO 2 max was related to KEVO 2 max (r = 0.69, P < 0.05) and BodyVO 2 max (r = 0.91, P < 0.05) in untrained subjects, these variables were entirely unrelated in trained subjects. Therefore, in untrained subjects,V O 2 max is limited by mitochondrial O 2 demand, with evidence of adequate O 2 supply, whereas, in trained subjects, an exercise training-induced mitochondrial reserve results in skeletal muscleV untrained and trained humans and challenge the concept of symmorphosis as it applies to O 2 supply and demand in humans. Abbreviations BIOPS, biopsy preservation fluid; Body, whole-body; KE, knee extensor; Mito, mitochondrial;Q O 2max , maximum specific oxygen uptake rate;V O2max , maximal oxygen uptake; WR max , maximum work rate.

Reply to Gifford et al.: Symmorphosis in chronic heart failure patients?

“…The observed dysmorphosis in trained subjects by Gifford et al (2) was not confirmed in our larger sample containing a wider range of V O 2 max (5). We did not intend to suggest that Gifford et al (2) based their results, challenging symmorphosis, on only four subjects.…”

“…We did not intend to suggest that Gifford et al (2) based their results, challenging symmorphosis, on only four subjects. In our view, six of the trained subjects fitted the (extrapolated) relationship between V O 2 max and mitochondrial capacity of the untrained subjects rather well (cf.…”

Determinants of the diminished exercise capacity in patients with chronic obstructive pulmonary disease: looking beyond the lungs

“…Estimation of peak quadriceps muscle O 2 utilization (Gifford et al . ), from in vitro mitochondrial respiration data, in patients with COPD is markedly greater (>0.40 l min −1 ) than the in the current patients with COPD (Gifford et al . , ).…”

GreaterV̇O2peakis correlated with greater skeletal muscle deoxygenation amplitude and hemoglobin concentration within individual muscles during ramp-incremental cycle exercise

“…Participants were grouped into those with low aerobic capacity (LO: n = 8, ≤45 mL kg −1 min −1 ), mid‐range (MID, n = 9, 46–55 mL kg −1 min −1 ) and those with high aerobic capacity (HI, n = 7, ≥56 mL kg −1 min −1 ) using similar reference ranges as in a previous study (Gifford et al. ). Analysis of deoxy‐ and total[Hb+Mb] was performed after correction for ATT to a thickness of 0 mm using linear regression of the relationship between total[Hb+Mb] and ATT at rest (Bowen et al.…”

“…; Gifford et al. ) and therefore the muscle deoxygenation/fractional O 2 extraction will reach a greater peak in fitter individuals (Ferreira et al. ; Gifford et al.…”