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Cited by 159Bone health and osteoporosis researchMuscle metabolism and nutritionBone Metabolism and Diseases

Effects of reduced energy availability on bone metabolism in women and men

Open access
Papageorgiou, Maria, Elliott-Sale, Kirsty J., Parsons, Alan, Tang, Johnathan C.Y., Greeves, Julie P., Fraser, William D., Sale, Craig·2017·Bone
DOI 10.1016/j.bone.2017.08.019
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Abstract

Background The short-term effects of low energy availability (EA) on bone metabolism in physically active women and men are currently unknown. Purpose We evaluated the effects of low EA on bone turnover markers (BTMs) in a cohort of women and a cohort of men, and compared effects between sexes. Methods These studies were performed using a randomised, counterbalanced, crossover design. Eleven eumenorrheic women and eleven men completed two 5-day protocols of controlled (CON; 45kcal·kgLBM-1·d-1) and restricted (RES; 15kcal·kgLBM-1·d-1) EAs. Participants ran daily on a treadmill at 70% of their peak aerobic capacity (VO 2 peak) resulting in an exercise energy expenditure of 15kcal·kgLBM-1·d-1 and consumed diets providing 60 and 30kcal·kgLBM-1·d-1. Blood was analysed for BTMs [β-carboxyl-terminal cross-linked telopeptide of type I collagen (β-CTX) and amino-terminal propeptide of type 1 procollagen (P1NP)], markers of calcium metabolism [parathyroid hormone (PTH), albumin-adjusted calcium (ACa), magnesium (Mg) and phosphate (PO 4)] and regulatory hormones [sclerostin, insulin-like growth factor 1 (IGF-1), triiodothyronine (T 3), insulin, leptin, glucagon-like-peptide-2 (GLP-2)]. Results In women, β-CTX AUC was significantly higher (P=0.03) and P1NP AUC was significantly lower (P=0.01) in RES compared to CON. In men, neither β-CTX (P=0.46) nor P1NP (P=0.12) AUCs were significantly different between CON and RES. There were no significant differences between sexes for any BTM AUCs (all P values>0.05). Insulin and leptin AUCs were significantly lower following RES in women only (for both P=0.01). There were no differences in any AUCs of regulatory hormones or markers of calcium metabolism between men and women following RES (all P values>0.05). Conclusions When comparing within groups, five days of low EA (15kcal·kgLBM-1·d-1) decreased bone formation and increased bone resorption in women, but not in men, and no sex specific differences were detected.

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  • Most LEA intervention studies are accompanied by a substantial reduction (25%-60%) in carbohydrate ingestion, resulting in concurrent LCA.

    “Most LEA intervention studies are also accompanied by a substantial reduction (25%-60%, depending on magnitude of LEA) in carbohydrate (CHO) ingestion, resulting in concurrent LCA.”

    From 2023 international olympic committee's (IOC) consensus statement on relative energy deficiency in sport (REDs) (2023) · cites this paper as [47]

    The Experimental Diets section says this study halved dietary energy intake while maintaining participants’ habitual dietary composition, which supports a substantial reduction in carbohydrate intake in this intervention. The paper does not establish that most LEA intervention studies reduce carbohydrate intake by 25%–60%, or explicitly characterize the resulting intake as concurrent low carbohydrate availability. (LLM, conf=0.84)

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  • Current findings show a strong correlation between the Female Athlete Triad and negative bone health outcomes, such as increased bone stress injuries and decreased bone mineral density.

    “current findings show a strong correlation between Triad and negative bone health outcomes, such as increased bone stress injuries and decreased BMD [6,7,9,11,14,15,16,17,18].”

    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 [16]

    The Introduction links the Female Athlete Triad with impaired bone health and identifies energy-deficiency factors as risks for low BMD and stress-fracture injury. It does not characterize the correlation as strong; the paper also studies bone metabolism rather than measuring BMD or injury incidence directly. (LLM, conf=0.84)

    Experimental — accuracy not yet measured

  • Most intervention studies assessing low energy availability in athletes are also accompanied by a considerable reduction in carbohydrate intake, approximately 25-60% depending on the magnitude of low energy availability.

    “Most intervention studies assessing LEA in athletes are also accompanied by a considerable reduction in CHO intake (approximately 25–60% reduction in CHO, depending on the magnitude of LEA) [16,23,24,25].”

    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 [16]

    The Experimental Design and Experimental Diets sections report that this study halved dietary energy intake while maintaining each participant’s habitual dietary composition, which supports a substantial reduction in carbohydrate intake in this intervention. The paper does not establish that most low-energy-availability interventions in athletes reduce carbohydrate intake, or document the claimed 25–60% range. (LLM, conf=0.82)

    Experimental — accuracy not yet measured

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Research works printed but not linked: 3

  1. M.J. De Souza, A. Nattiv, E. Joy, M. Misra, N.I. Williams, R.J. Mallinson, J.C. Gibbs, M. Olmsted, M. Goolsby, G. Matheson, P. Expert, 2014 Female Athlete Triad Coalition Consensus Statement on Treatment and Return to Play of the Female Athlete Triad: 1st International Conference held in San Francisco, California, May 2012 and 2nd International Conference held in Indianapolis, Indiana, May 2013, Br. J. Sports Med. 48(4) (2014) 289.
  2. L. Wentz, P.Y. Liu, E. Haymes, J.Z. Ilich, Females have a greater incidence of stress fractures than males in both military and athletic populations: a systemic review, Mil Med 176(4) (2011) 420-30.
  3. J. Knapik, S.J. Montain, S. McGraw, T. Grier, M. Ely, B.H. Jones, Stress fracture risk factors in basic combat training, Int. J. Sports Med. 33(11) (2012) 940-6.

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Authors
Papageorgiou, M., Elliott-Sale, K. J., Parsons, A., Tang, J. C. Y., Greeves, J. P., Fraser, W. D., & Sale, C.
Affiliations
  • Nottingham Trent University (GB)
  • University of Derby (GB)
  • Ministry of Defence (GB)
  • University of East Anglia (GB)
Corresponding author
Sale, Craig
ORCID
Venue
Bone
Publisher
Elsevier BV
Published
2017-12
Volume
105
Pages
191-199
ISSN
  • 1873-2763 (ISSN-L)
  • 8756-3282
DOI
10.1016/j.bone.2017.08.019
OpenAlex
W2747889246
Cited by
159
References
5
Citations by year
2026: 14 · 2025: 14 · 2024: 27 · 2023: 24 · 2022: 15 · 2021: 23 · 2020: 22 · 2019: 11 · 2018: 9
FWCI
12.69
Type
journal article
Language
en
Open access
Licence
www.elsevier.com/tdm/userlicense/1.0/ (tdm)
Locations
  • Bone (publishedVersion)
  • PubMed (publishedVersion)
  • Nottingham Trent University's Institutional Repository (Nottingham Trent Repository) (acceptedVersion)
  • UEA Digital Repository (University of East Anglia) (acceptedVersion)
Funders
  • Nottingham Trent University
  • Trent University
Topics
  • Health Sciences › Medicine › Orthopedics and Sports Medicine › Bone health and osteoporosis research
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Cell Biology › Muscle metabolism and nutrition
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Bone Metabolism and Diseases
Keywords
low energy availability, bone metabolism, bone turnover markers, β-CTX, P1NP, sex differences, caloric restriction, physical activity, bone resorption, bone formation, calcium metabolism, sclerostin, insulin-like growth factor I, leptin, insulin, eumenorrheic women, men, exercise energy expenditure, hypocaloric diet, glucagon-like peptide-2
MeSH terms
Adult, Body Weight, Bone and Bones, Calcium, Diet, Energy Metabolism, Female, Hormones, Humans, Male, Biomarkers, Exercise, Bone Remodeling, Area Under Curve

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