CoChat
Sign Up
Cited by 46Muscle metabolism and nutritionBone health and osteoporosis researchExercise and Physiological Responses

The effect of postexercise carbohydrate and protein ingestion on bone metabolism

Open access
TOWNSEND, REBECCA, ELLIOTT-SALE, KIRSTY J., CURRELL, KEVIN, TANG, JONATHAN, FRASER, WILLIAM D., SALE, CRAIG·2017·Medicine & Science in Sports & Exercise
DOI 10.1249/mss.0000000000001211
Open this paper in CoChat — free accountOpen PDF

Abstract

PURPOSE: This study aimed to investigate the effect of feeding carbohydrate and protein (CHO + PRO), immediately or 2 h after an exhaustive run, on the bone turnover response in endurance runners. METHODS: Ten men (age = 28 ± 5 yr, height = 1.74 ± 0.05 m, body mass [BM] = 69.7 ± 6.3 kg) performed treadmill running at 75% V˙O2max, until exhaustion, on three occasions. Blood was collected before and immediately, 1, 2, 3, 4, and 24 h postexercise, for measurement of β-CTX, P1NP, parathyroid hormone, PO4, ACa, and Ca. This was a randomized, counterbalanced, placebo-controlled, and single-blinded crossover study. The three trials were (i) placebo (PLA), where the PLA solution was ingested immediately and 2 h postexercise; (ii) immediate feeding (IF), where CHO + PRO (1.5 g·kg BM dextrose and 0.5 g·kg BM whey) was ingested immediately postexercise and PLA 2 h postexercise; and (iii) delayed feeding (DF), where PLA was ingested immediately postexercise and CHO + PRO solution 2 h postexercise. Data were analyzed using repeated-measures ANOVA and Tukey's HSD post hoc test. RESULTS: At 1 and 2 h postexercise, β-CTX concentrations were lower in the IF trial compared with the DF and PLA trials (P ≤ 0.001). At 3 h postexercise, β-CTX concentrations were higher in the PLA trial compared with the IF (P ≤ 0.001) and DF trials (P = 0.026). At 4 h postexercise, β-CTX concentrations were lower in the DF trial compared with the IF (P = 0.003) and PLA trials (P ≤ 0.001). At 4 h postexercise, P1NP was higher in the IF trial compared with the DF (P = 0.026) and PLA trials (P = 0.001). At 3 h postexercise, parathyroid hormone was higher in the IF trial compared with the DF trial (P ≤ 0.001). CONCLUSIONS: After exhaustive running, immediate ingestion of CHO + PRO may be beneficial, as it decreases bone resorption marker concentrations and increases bone formation marker concentrations, creating a more positive bone turnover balance.

The claims and statistics of this paper haven’t been checked yet.

Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.

A few free checks a day · papers already verified open instantly · results are public

Integrity signals

Registry

Crossref · 10.1249/mss.0000000000001211

Cites

4 of 4 references verified0 citation errors · 0 not checkable

Statistics

Claims the paper makes

The claims and statistics of this paper haven’t been checked yet.

Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.

A few free checks a day · papers already verified open instantly · results are public

Claims other papers make about this one

Each is checked against this paper’s own text: does it say what the citing paper says it does?

  • Post-exercise carbohydrate with protein is protective for bone health as it decreases bone resorption markers and increases bone formation markers, creating a positive bone turnover balance.

    “the effects of post-exercise CHO (with protein) are protective for bone health as it decreases bone resorption markers and increases bone formation markers, which creates a positive bone turnover balance [39].”

    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 [39]

    The Discussion reports that CHO+PRO immediately after intense exercise reduced bone-resorption markers and increased bone-formation markers during short-term recovery. It does not establish a positive bone-turnover balance or a protective effect on bone health; the Discussion says the effects did not persist to the following morning and cautions that suppressing resorption may not always be desirable. Page numbers were not available in our copy. (LLM, conf=0.88)

    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 [39]

    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

Self-check

Percentages, sums and reported differences re-computed from the paper’s own numbers.

The self-check needs the paper’s full text.

Cites

Flagged first, then by citations

Research works printed but not linked: 35

  1. Bennell KL, Malcolm SA, Thomas SA, et al. Risk factors for stress fractures in track and field athletes. A twelve-month prospective study. Am J Sports Med. 1996; 24(6):810-8.
  2. Bjarnason N, Henriksen E, Alexandersen P, Christgau S, Henriksen D, Christiansen C. Mechanism of circadian variation in bone resorption. Bone. 2002; 30(1):307-13.
  3. Blumsohn A, Herrington K, Hannon RA, Shao P, Eyre DR, Eastell R. The effect of calcium supplementation on the circadian rhythm of bone resorption. J Clin Endocrinol Metab. 1994; 79(3):730-5.
  4. Clowes J, Hannon R, Yap T, Hoyle N, Blumsohn A, Eastell R. Effect of feeding on bone turnover markers and its impact on biological variability of measurements. Bone. 2002; 30(6):886-90.
  5. Clowes JA, Allen HC, Prentis DM, Eastell R, Blumsohn A. Octreotide abolishes the acute decrease in bone turnover in response to oral glucose. J Clin Endocrinol Metab. 2003; 88(10):4867-73.
  6. de Papp AE, Bone HG, Caulfield MP, et al. A cross-sectional study of bone turnover markers in healthy premenopausal women. Bone. 2007; 40(5):1222-30.
  7. de Sousa MV, Pereira RMR, Fukui R, Caparbo VF, da Silva MER. Carbohydrate beverages attenuate bone resorption markers in elite runners. Metab Clin Exp. 2014; 63(12):1536-41.
  8. Fredericson M, Jennings F, Beaulieu C, Matheson GO. Stress fractures in athletes. Top Magn Reson Imaging. 2006; 17(5):309-25.
  9. Frolik CA, Black EC, Cain RL, et al. Anabolic and catabolic bone effects of human parathyroid hormone (1-34) are predicted by duration of hormone exposure. Bone. 2003; 33(3):372-9.
  10. Glover S, Garnero P, Naylor K, Rogers A, Eastell R. Establishing a reference range for bone turnover markers in young, healthy women. Bone. 2008; 42(4):623-30.
  11. Glover SJ, Gall M, Schoenborn-Kellenberger O, et al. Establishing a reference interval for bone turnover markers in 637 healthy, young, premenopausal women from the United Kingdom, France, Belgium, and the United States. J Bone and Min Res. 2009; 24(3):389-97.
  12. Guillemant J, Accarie C, Peres G, Guillemant S. Acute effects of an oral calcium load on markers of bone metabolism during endurance cycling exercise in male athletes. Calcif Tissue Int. 2004; 74(5):407-14.
  13. Henriksen DB, Alexandersen P, Bjarnason NH, et al. Role of gastrointestinal hormones in postprandial reduction of bone resorption. J Bone Miner Res. 2003; 18(12):2180-9.
  14. Ihle R, Loucks AB. Dose-response relationships between energy availability and bone turnover in young exercising women. J Bone Miner Res. 2004; 19(8):1231-40.
  15. Jones AM, Doust JH. A 1% treadmill grade most accurately reflects the energetic cost of outdoor running. J Sports Sci. 1996; 14(4):321-7.
  16. Kaysen GA, Gambertoglio J, Jimenez I, Jones H, Hutchison FN. Effect of dietary protein intake on albumin homeostasis in nephrotic patients. Kidney Int. 1986; 29(2):572-7.
  17. Kerschan-Schindl K, Thalmann M, Sodeck GH, et al. A 246-km continuous running race causes significant changes in bone metabolism. Bone. 2009; 45(6):1079-83.
  18. Kirsch R, Frith L, Black E, Hoffenberg R. Regulation of albumin synthesis and catabolism by alteration of dietary protein. Nature. 1968; 217:578-9.
  19. Maimoun L, Manetta J, Couret I, et al. The intensity level of physical exercise and the bone metabolism response. Int J Sports Med. 2006; 27(02):105-11.
  20. Matheson GO, Clement DB, McKenzie DC, Taunton JE, Lloyd-Smith DR, MacIntyre JG. Stress fractures in athletes. A study of 320 cases. Am J Sports Med. 1987; 15(1):46-58.
  21. McSheehy P, Chambers T. Osteoblast-Like Cells in the Presence of Parathyroid Hormone Release Soluble Factor that Stimulates Osteoclastic Bone Resorption*. Endocrinology. 1986; 119(4):1654-9.
  22. Oosthuyse T, Badenhorst M, Avidon I. Bone resorption is suppressed immediately after the third and fourth days of multiday cycling but persistently increased following overnight recovery. Appl Physiol Nutr Metab. 2013; 39(1):64-73.
  23. Parfitt A. The coupling of bone formation to bone resorption: a critical analysis of the concept and of its relevance to the pathogenesis of osteoporosis. Metab Bone Dis Relat Res. 1982; 4(1):1-6.
  24. Ranson CA, Burnett AF, Kerslake RW. Injuries to the lower back in elite fast bowlers: acute stress changes on MRI predict stress fracture. J Bone Joint Surg Br. 2010; 92(12):1664- 8.
  25. Riggs BL, Melton L, O'fallon W. Drug therapy for vertebral fractures in osteoporosis: evidence that decreases in bone turnover and increases in bone mass both determine antifracture efficacy. Bone. 1996; 18(3):S197-201.
  26. Schaffler M, Radin E, Burr D. Long-term fatigue behavior of compact bone at low strain magnitude and rate. Bone. 1990; 11(5):321-6.
  27. Schlemmer A, Hassager C. Acute fasting diminishes the circadian rhythm of biochemical markers of bone resorption. Eur J Endocrinol. 1999; 140(4):332-7.
  28. Scott JP, Sale C, Greeves JP, Casey A, Dutton J, Fraser WD. The effect of training status on the metabolic response of bone to an acute bout of exhaustive treadmill running. The J Clin Endocrinol Metab. 2010; 95(8):3918-25.
  29. Scott JP, Sale C, Greeves JP, Casey A, Dutton J, Fraser WD. The role of exercise intensity in the bone metabolic response to an acute bout of weight-bearing exercise. J Appl Physiol. 2011; 110(2):423-32.
  30. Scott JP, Sale C, Greeves JP, Casey A, Dutton J, Fraser WD. Effect of fasting versus feeding on the bone metabolic response to running. Bone. 2012; 51(6):990-9.
  31. Thorsen K, Kristoffersson A, Hultdin J, Lorentzon R. Effects of moderate endurance exercise on calcium, parathyroid hormone, and markers of bone metabolism in young women. Calcif Tissue Int. 1997; 60(1):16-20.
  32. Tipton KD, Elliott TA, Cree MG, Wolf SE, Sanford AP, Wolfe RR. Ingestion of casein and whey proteins result in muscle anabolism after resistance exercise. Med Sci Sports Exerc. 2004; 36:2073-81.
  33. Walsh JS, Henriksen DB. Feeding and bone. Arch Biochem Biophys. 2010; 503(1):11-9.
  34. Warden SJ, Burr DB, Brukner PD. Stress fractures: pathophysiology, epidemiology, and risk factors. Current osteoporosis reports. 2006; 4(3):103-9.
  35. Zittermann A, Sabatschus O, Jantzen S, Platen P, Danz A, Stehle P. Evidence for an acute rise of intestinal calcium absorption in response to aerobic exercise. Eur J Nutr. 2002; 41(5):189-96.

Cited by

Sorted by citations

Authors
TOWNSEND, R., ELLIOTT-SALE, K. J., CURRELL, K., TANG, J., FRASER, W. D., & SALE, C.
Affiliations
  • University of East Anglia (GB)
  • Nottingham Trent University (GB)
  • Loughborough University (GB)
ORCID
Venue
Medicine & Science in Sports & Exercise
Publisher
Ovid Technologies (Wolters Kluwer Health)
Published
2017-06
Volume
49
Issue
6
Pages
1209-1218
ISSN
0195-9131 (ISSN-L)
DOI
10.1249/mss.0000000000001211
OpenAlex
W2582856226
Cited by
46
References
4
Citations by year
2026: 5 · 2025: 2 · 2024: 4 · 2023: 3 · 2022: 5 · 2021: 6 · 2020: 7 · 2019: 9 · 2018: 4 · 2017: 1
FWCI
3.07
Type
journal article
Language
en
Open access
Locations
  • Medicine & Science in Sports & Exercise (publishedVersion)
  • PubMed (publishedVersion)
  • Nottingham Trent University's Institutional Repository (Nottingham Trent Repository) (acceptedVersion)
  • UEA Digital Repository (University of East Anglia) (submittedVersion)
Topics
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Cell Biology › Muscle metabolism and nutrition
  • Health Sciences › Medicine › Orthopedics and Sports Medicine › Bone health and osteoporosis research
  • Health Sciences › Medicine › Rehabilitation › Exercise and Physiological Responses
Keywords
bone turnover, bone resorption, bone formation, bone turnover markers, β-CTX, P1NP, parathyroid hormone, exhaustive running, endurance runners, whey protein, D-glucose, calcium, phosphate, bone metabolism, exercise-induced bone loss, osteoporosis prevention
MeSH terms
Adult, Bone and Bones, Calcium, Dietary Carbohydrates, Dietary Proteins, Humans, Male, Parathyroid Hormone, Phosphates, Physical Endurance, Running, Serum Albumin, Single-Blind Method, Bone Remodeling, Cross-Over Studies, Collagen Type I

About these checks

Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.

Statistics and arithmetic are recomputed, not judged.

Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.

What counts as a claim ›How we measure confidence ›How we check this ›

Are you an author, or do you see a problem with this page? Request a review