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Cited by 65Bone health and osteoporosis researchLower Extremity Biomechanics and PathologiesMuscle metabolism and nutrition

Short-term carbohydrate restriction impairs bone formation at rest and during prolonged exercise to a greater degree than low energy availability

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Fensham, Nikita C., Heikura, Ida A., McKay, Alannah K.A., Tee, Nicolin, Ackerman, Kathryn E., Burke, Louise M.·2020·Journal of Bone and Mineral Research
DOI 10.1002/jbmr.4658PMC PMC9804216
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Abstract

Bone stress injuries are common in athletes, resulting in time lost from training and competition. Diets that are low in energy availability have been associated with increased circulating bone resorption and reduced bone formation markers, particularly in response to prolonged exercise. However, studies have not separated the effects of low energy availability per se from the associated reduction in carbohydrate availability. The current study aimed to compare the effects of these two restricted states directly. In a parallel group design, 28 elite racewalkers completed two 6-day phases. In the Baseline phase, all athletes adhered to a high carbohydrate/high energy availability diet (CON). During the Adaptation phase, athletes were allocated to one of three dietary groups: CON, low carbohydrate/high fat with high energy availability (LCHF), or low energy availability (LEA). At the end of each phase, a 25-km racewalk was completed, with venous blood taken fasted, pre-exercise, and 0, 1, 3 hours postexercise to measure carboxyterminal telopeptide (CTX), procollagen-1 N-terminal peptide (P1NP), and osteocalcin (carboxylated, gla-OC; undercarboxylated, glu-OC). Following Adaptation, LCHF showed decreased fasted P1NP (~26%; p < 0.0001, d = 3.6), gla-OC (~22%; p = 0.01, d = 1.8), and glu-OC (~41%; p = 0.004, d = 2.1), which were all significantly different from CON (p < 0.01), whereas LEA demonstrated significant, but smaller, reductions in fasted P1NP (~14%; p = 0.02, d = 1.7) and glu-OC (~24%; p = 0.049, d = 1.4). Both LCHF (p = 0.008, d = 1.9) and LEA (p = 0.01, d = 1.7) had significantly higher CTX pre-exercise to 3 hours post-exercise but only LCHF showed lower P1NP concentrations (p < 0.0001, d = 3.2). All markers remained unchanged from Baseline in CON. Short-term carbohydrate restriction appears to result in reduced bone formation markers at rest and during exercise with further exercise-related increases in a marker of bone resorption. Bone formation markers during exercise seem to be maintained with LEA although resorption increased. In contrast, nutritional support with adequate energy and carbohydrate appears to reduce unfavorable bone turnover responses to exercise in elite endurance athletes. © 2022 The Authors. Journal of Bone and Mineral Research published by Wiley Periodicals LLC on behalf of American Society for Bone and Mineral Research (ASBMR).

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  • Six 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 [53]

    Split into 2 atoms — 1 confirmed, 1 partially supported, 0 disputed, 0 misattributed, 0 unverifiable. Expand the claim to see per-atom verdicts.

    Experimental — accuracy not yet measured

  • Low 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 [43]

    Split into 2 atoms — 0 confirmed, 1 partially supported, 0 disputed, 0 misattributed, 1 unverifiable. Expand the claim to see per-atom verdicts.

    Experimental — accuracy not yet measured

  • Low carbohydrate availability is independently associated with poor bone outcomes, such as bone stress injuries and decreased bone mineral density, even with adequate energy availability.

    “Therefore, LCA is independently associated with poor bone outcomes (e.g., bone stress injuries, decreased bone mineral density (BMD)), even with adequate EA [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 [43]

    The Discussion (page not provided) reports that a high-energy, low-carbohydrate diet negatively affected bone-formation markers, supporting an effect of carbohydrate restriction despite adequate energy availability. But the study measured short-term bone-turnover markers, not bone stress injuries or changes in BMD; the Discussion says that translating those markers into structural bone changes or fracture risk requires further research. (LLM, conf=0.90)

    Experimental — accuracy not yet measured

  • Bone health consequences were more deleterious in the low carbohydrate, high fat group compared to the low energy availability group.

    “However, bone health consequences were more deleterious (e.g., greater decreases in bone formation markers and increases in bone resorption markers) in the LCHF group compared to the LEA group [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 [43]

    The Results (Percent change in fasting concentrations) report larger decreases in bone-formation markers in LCHF than LEA, although the between-group differences were not significant. The claim’s resorption comparison is not supported: fasting CTX increases did not differ significantly between groups, and exercise-associated CTX increased by 28.0% in LCHF versus 30.9% in LEA (Results, Exercise-associated AUC). These markers also do not establish structural bone-health consequences. (LLM, conf=0.90)

    Experimental — accuracy not yet measured

  • By maintaining naturally cycling hormones, carbohydrate helps regulate normal menstrual cycles and bone health maintenance through benefits to hormones such as estrogen, IGF-1, cortisol, and growth hormone influencing bone mineral density.

    “By maintaining these naturally cycling hormones, CHO helps regulate normal menstrual cycles and bone health maintenance through benefits to hormones (e.g., estrogen, IGF-1, cortisol, growth hormone) influencing BMD [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 [43]

    The Conclusion reports that adequate carbohydrate may help prevent an unfavorable imbalance in bone turnover markers, supporting the bone-health portion of the claim. The Methods’ blood-analysis section lists bone turnover markers, not estrogen, IGF-1, cortisol, or growth hormone; the paper does not show that carbohydrate maintains menstrual cycles through those hormones or demonstrate a change in BMD. (LLM, conf=0.88)

    Experimental — accuracy not yet measured

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Cited by

Sorted by citations

Authors
Fensham, N. C., Heikura, I. A., McKay, A. K. A., Tee, N., Ackerman, K. E., & Burke, L. M.
Affiliations
  • Australian Catholic University (AU)
  • University of Victoria (CA)
  • Boston Children's Hospital (US)
Corresponding author
Fensham, Nikita C.
ORCID
Venue
Journal of Bone and Mineral Research
Publisher
Oxford University Press (OUP)
Published
2020-12-01
Volume
37
Issue
10
Pages
1915-1925
ISSN
  • 0884-0431 (ISSN-L)
  • 1523-4681
DOI
10.1002/jbmr.4658
PMC
PMC9804216
OpenAlex
W4286742150
Cited by
65
References
5
Citations by year
2026: 18 · 2025: 12 · 2024: 17 · 2023: 14 · 2022: 3
FWCI
4.25
Type
journal article
Language
en
Open access
Licence
Locations
  • Journal of Bone and Mineral Research (publishedVersion, cc-by-nc-nd)
  • PubMed Central (publishedVersion, cc-by-nc-nd)
  • PubMed (publishedVersion)
Funders
  • Australian Catholic University
  • Wu Tsai Human Performance Alliance
Topics
  • Health Sciences › Medicine › Orthopedics and Sports Medicine › Bone health and osteoporosis research
  • Physical Sciences › Engineering › Biomedical Engineering › Lower Extremity Biomechanics and Pathologies
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Cell Biology › Muscle metabolism and nutrition
Keywords
carbohydrate restriction, low energy availability, low-carbohydrate high-fat diet, bone formation, bone resorption, bone stress injuries, osteocalcin, race walking, athletes, exercise-induced bone loss, dietary adaptation, bone formation markers, bone resorption markers, undercarboxylated osteocalcin
MeSH terms
Bone Resorption, Carbohydrates, Humans, Osteogenesis, Peptides, Procollagen, Biomarkers, Exercise, Osteocalcin, Bone Remodeling, Diet, Carbohydrate-Restricted, Athletes

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