Post-exercise carbohydrate and energy availability induce independent effects on Skeletal muscle cell signalling and bone turnover: implications for training adaptation
Open accessAbstract
Key points: Reduced carbohydrate (CHO) availability before and after exercise may augment endurance training‐induced adaptations of human skeletal muscle, as mediated via modulation of cell signalling pathways. However, it is not known whether such responses are mediated by CHO restriction, energy restriction or a combination of both. In recovery from a twice per day training protocol where muscle glycogen concentration is maintained within 200–350 mmol kg−1 dry weight (dw), we demonstrate that acute post‐exercise CHO and energy restriction (i.e. < 24 h) does not potentiate potent cell signalling pathways that regulate hallmark adaptations associated with endurance training. In contrast, consuming CHO before, during and after an acute training session attenuated markers of bone resorption, effects that are independent of energy availability. Whilst the enhanced muscle adaptations associated with CHO restriction may be regulated by absolute muscle glycogen concentration, the acute within‐day fluctuations in CHO availability inherent to twice per day training may have chronic implications for bone turnover. We examined the effects of post‐exercise carbohydrate (CHO) and energy availability (EA) on potent skeletal muscle cell signalling pathways (regulating mitochondrial biogenesis and lipid metabolism) and indicators of bone metabolism. In a repeated measures design, nine males completed a morning (AM) and afternoon (PM) high‐intensity interval (HIT) (8 × 5 min at 85% ) running protocol (interspersed by 3.5 h) under dietary conditions of (1) high CHO availability (HCHO: CHO ∼12 g kg−1, EA∼ 60 kcal kg−1 fat free mass (FFM)), (2) reduced CHO but high fat availability (LCHF: CHO ∼3 (−1, EA∼ 60 kcal kg−1 FFM) or (3), reduced CHO and reduced energy availability (LCAL: CHO ∼3 g kg−1, EA∼ 20 kcal kg−1 FFM). Muscle glycogen was reduced to ∼200 mmol kg−1 dw in all trials immediately post PM HIT (P < 0.01) and remained lower at 17 h (171, 194 and 316 mmol kg−1 dw) post PM HIT in LCHF and LCAL (P < 0.001) compared to HCHO. Exercise induced comparable p38MAPK phosphorylation (P < 0.05) immediately post PM HIT and similar mRNA expression (all P < 0.05) of PGC‐1α, p53 and CPT1 mRNA in HCHO, LCHF and LCAL. Post‐exercise circulating βCTX was lower in HCHO (P < 0.05) compared to LCHF and LCAL whereas exercise‐induced increases in IL‐6 were larger in LCAL (P < 0.05) compared to LCHF and HCHO. In conditions where glycogen concentration is maintained within 200–350 mmol kg−1 dw, we conclude post‐exercise CHO and energy restriction (i.e. < 24 h) does not potentiate cell signalling pathways that regulate hallmark adaptations associated with endurance training. In contrast, consuming CHO before, during and after HIT running attenuates bone resorption, effects that are independent of energy availability and circulating IL‐6.
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Short-term (≤6 days) investigations in male endurance athletes have reported increases in bone resorption biomarkers with concomitant impairment in bone formation biomarkers, and increased postexercise IL-6 and hepcidin after LCA.
“These studies have reported increases in bone resorption biomarkers 52 53 with a concomitant impairment in biomarkers of bone formation, 53 as well as increased postexercise concentrations of interleukin-6 (IL-6) and hepcidin after LCA.54”
From 2023 international olympic committee's (IOC) consensus statement on relative energy deficiency in sport (REDs) (2023) · cites this paper as [52]
The Interleukin-6 (IL-6) responses section (page unavailable) reports a greater postexercise IL-6 increase in the low-carbohydrate, low-energy (LCAL) condition than in either comparison condition. The Discussion says carbohydrate availability alone did not apparently affect IL-6. Citation 54 is attached to the IL-6 and hepcidin claim, but our copy does not report hepcidin measurements or an increase in hepcidin. (LLM, conf=0.88)
Experimental — accuracy not yet measuredSix studies since 2019 have shown an energy-independent and/or magnifying impact of LCA in the accelerated development of REDs outcomes.
“Six studies since 2019 have shown an energy-independent and/or magnifying impact of LCA in the accelerated development of REDs outcomes.[52][53][54][55][56][57]”
From 2023 international olympic committee's (IOC) consensus statement on relative energy deficiency in sport (REDs) (2023) · cites this paper as [52]
The Bone metabolism results and Discussion (page unavailable) show that low carbohydrate availability affected an acute marker of bone resorption independently of overall energy availability. The paper does not establish accelerated development of RED-S outcomes: its Discussion says the acute study could not determine whether the regimen causes longer-term changes to bone. The claim about six studies belongs to the citing paper’s collective summary, not a finding this single source must establish. (LLM, conf=0.86)
Experimental — accuracy not yet measuredLow carbohydrate availability ranges have not been established based on these criteria for carbohydrate availability, and many studies continue to report carbohydrate intake, using low carbohydrate intake to define intake below current recommendations.
“Nonetheless, LCA ranges have not been established based on these criteria for CHO availability, and many studies continue to report CHO intake, using low CHO intake to define intake below current recommendations [34,35,36,37,38,39,40,41,42,43].”
From Considerations of Low Carbohydrate Availability (LCA) to Relative Energy Deficiency in Sport (RED-S) in Female Endurance Athletes: A Narrative Review (2023) · cites this paper as [38]
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Experimental — accuracy not yet measuredIn male runners, carbohydrate consumption before, during, and after acute training sessions attenuated bone resorption markers, independent of low energy availability.
“In male runners, CHO consumption before, during, and after acute training sessions attenuated bone resorption markers, independent of LEA [38].”
From Considerations of Low Carbohydrate Availability (LCA) to Relative Energy Deficiency in Sport (RED-S) in Female Endurance Athletes: A Narrative Review (2023) · cites this paper as [38]
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- Authors
- Hammond, K. M., Sale, C., Fraser, W., Tang, J., Shepherd, S. O., Strauss, J. A., Close, G. L., Cocks, M., Louis, J., Pugh, J., Stewart, C., Sharples, A. P., & Morton, J. P.
- Affiliations
- Liverpool John Moores University (GB)
- Nottingham Trent University (GB)
- University of East Anglia (GB)
- Corresponding author
- Morton, James P.
- ORCID
- Venue
- The Journal of Physiology
- Publisher
- Wiley
- Published
- 2019-08-21
- Volume
- 597
- Issue
- 18
- Pages
- 4779-4796
- ISSN
- 0022-3751 (ISSN-L)
- 1469-7793
- OpenAlex
- W2965716253
- Cited by
- 68
- References
- 23
- Citations by year
- 2026: 7 · 2025: 7 · 2024: 10 · 2023: 9 · 2022: 7 · 2021: 13 · 2020: 14 · 2019: 1
- FWCI
- 4.63
- Type
- journal article
- Language
- en
- Open access
- bronze
- doi.org
- Locations
- The Journal of Physiology (publishedVersion)
- PubMed (publishedVersion)
- Nottingham Trent University's Institutional Repository (Nottingham Trent Repository) (acceptedVersion)
- Liverpool John Moores University (submittedVersion)
- UEA Digital Repository (University of East Anglia) (submittedVersion)
- Funders
- English Institute of Sport
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Cell Biology › Muscle metabolism and nutrition
- Health Sciences › Medicine › Orthopedics and Sports Medicine › Sports Performance and Training
- Health Sciences › Medicine › Rehabilitation › Exercise and Physiological Responses
- Keywords
- energy availability, bone turnover, bone resorption, muscle glycogen, endurance training adaptation, high-intensity interval training, low-carbohydrate diet, caloric restriction, p38 MAPK, mitochondrial biogenesis, lipid metabolism, training effects, dietary fat restriction, muscle protein synthesis, muscle protein degradation
- MeSH terms
- Adaptation, Physiological, Adult, Organelle Biogenesis, Carbohydrates, Energy Metabolism, Glycogen, Humans, Male, Physical Endurance, Signal Transduction, Exercise, Bone Remodeling, Muscle, Skeletal, p38 Mitogen-Activated Protein Kinases, Lipid Metabolism, Young Adult
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