Effects of post exercise protein supplementation on markers of bone turnover in adolescent swimmers

Alexandros Theocharidis, Brandon J McKinlay, Dimitris Vlachopoulos, Andrea R Josse, Bareket Falk, Panagiota Klentrou, Alexandros Theocharidis, Brandon J McKinlay, Dimitris Vlachopoulos, Andrea R Josse, Bareket Falk, Panagiota Klentrou

Abstract

Background: This study examined the effects of whey protein supplementation, compared with an isocaloric carbohydrate beverage and water, consumed immediately following an intense swimming trial on bone turnover in adolescent swimmers.

Methods: Fifty-eight (31 female, 27 male) swimmers (14.1 ± 0.4 years) were stratified into three groups matched for age, sex and body mass. The protein and carbohydrate groups consumed two isocaloric post-exercise beverages each containing 0.3 g.kg- 1 of whey protein (with ~ 6 mg of calcium) or maltodextrin while the control group consumed water. Participants provided a morning, fasted, resting blood sample, then performed an intense swimming trial consisting of a maximal 200 m swim followed by a high intensity interval swimming protocol (5x100m, 5x50m and 5x25m; 1:1 work-to-rest ratio). Following swimming, they consumed their first respective post-exercise beverage, and 2 h later, they performed a second maximal swim immediately followed by the second beverage. Approximately 3 h after the second beverage, two post-consumption blood samples were collected at 8 h and 24 h from baseline. Procollagen type 1 intact N-terminal propeptide (PINP) and carboxy-terminal collagen crosslinks (CTXI) were measured in serum. The multiples of medians of PINP and CTXI were also used to calculate bone turnover rate and balance.

Results: No significant changes were observed in PINP. CTXI increased (+ 11%) at 8 h in all groups, but then significantly decreased (- 22%) at 24 h in the protein group only. The protein group also had a significantly higher calculated rate of bone turnover at 8 h and 24 h compared to baseline, which was not observed in the other groups.

Conclusions: These results shed light on the potential importance of protein consumed shortly after intense swimming in promoting positive bone turnover responses up to 24 h following exercise in adolescent athletes.

Clinical trial registration: ClinicalTrials.gov PRS; NCT04114045. Registered 1 October 2019 - Retrospectively registered.

Keywords: Bone turnover; CTXI; High intensity swimming; PINP.

Conflict of interest statement

The authors declare that they have no competing interests.

Figures

Fig. 1
Fig. 1
Study design
Fig. 2
Fig. 2
Relative changes in serum concentrations (mean ± SEM) of carboxy-terminal collagen crosslinks (CTXI) following the two post-exercise supplement beverages (i.e., 8 h and 24 h from baseline) in adolescent female and male swimmers, where baseline values are taken as 100%. There was a significant main effect for time (F = 11.48, p = 0.001, ηp2 = 0.18) and a significant time-by-group interaction (F = 4.88, p = 0.001, ηp2 = 0.16), reflecting a significant decrease (*p = 0.04) from 8 h to 24 h in the protein group only
Fig. 3
Fig. 3
Relative serum concentrations (mean ± SEM) of procollagen type 1 intact N-terminal propeptide (PINP) following the two post-exercise supplement beverages (i.e., 8 h and 24 h from baseline) in adolescent female and male swimmers, where baseline values are taken as 100%. No significant main effects were observed for time, group or sex, and no significant interactions

References

    1. Rauch F, Bailey DA, Baxter-Jones A, Mirwald R, Faulkner R. The “muscle-bone unit” during the pubertal growth spurt. Bone. 2004;34(5):771–775. doi: 10.1016/j.bone.2004.01.022.
    1. Meyer F, O’Connor H, Shirreffs SM. International Association of Athletics Federations. Nutrition for the young athlete. J Sports Sci. 2007;25(Suppl 1):S73–S82. doi: 10.1080/02640410701607338.
    1. Canada H. Dietary Reference Intakes Tables. AEM. 2005 [Cited 30 Dec 2019]. Available from: .
    1. Ilich JZ, Kerstetter JE. Nutrition in bone health revisited: a story beyond calcium. J Am Coll Nutr. 2000;19(6):715–737. doi: 10.1080/07315724.2000.10718070.
    1. Bonjour J-P, Ammann P, Chevalley T, Rizzoli R. Protein intake and bone growth. Can J Appl Physiol. 2001;26(S1):S153–S166. doi: 10.1139/h2001-050.
    1. Pellet PL. Protein requirements in humans. Am J Clin Nutr. 1990;51(5):723–737. doi: 10.1093/ajcn/51.5.723.
    1. Volterman KA, Atkinson SA. Protein needs of physically active children. Pediatr Exerc Sci. 2016;28(2):187–193. doi: 10.1123/pes.2015-0257.
    1. ADA, DC & ACSM Position of dietitians of Canada, the American dietetic association, and the American College of Sports Medicine: nutrition and athletic performance. Can J Diet Pract Res. 2000;61(4):176–192.
    1. Phillips SM, Van Loon LJC. Dietary protein for athletes: from requirements to optimum adaptation. J Sports Sci. 2011;29(Suppl 1):S29–S38. doi: 10.1080/02640414.2011.619204.
    1. Gomez-Bruton A, Montero-Marín J, González-Agüero A, García-Campayo J, Moreno LA, Casajús JA, et al. The effect of swimming during childhood and adolescence on bone mineral density: a systematic review and meta-analysis. Sports Med. 2016;46(3):365–379. doi: 10.1007/s40279-015-0427-3.
    1. Kouvelioti R, Kurgan N, Falk B, Ward WE, Josse AR, Klentrou P. Response of Sclerostin and bone turnover markers to high intensity interval exercise in young women: does impact matter? Biomed Res Int. 2018;2018:1–8. doi: 10.1155/2018/4864952.
    1. Kouvelioti R, LeBlanc P, Falk B, Ward WE, Josse AR, Klentrou P. Effects of high-intensity interval running versus cycling on Sclerostin, and markers of bone turnover and oxidative stress in young men. Calcif Tissue Int. 2019;104(6):582–590. doi: 10.1007/s00223-019-00524-1.
    1. Hoffman JR, Falvo MJ. Protein - which is best? J Sports Sci Med. 2004;3(3):118–130.
    1. Hoffman JR, Ratamess NA, Kang J, Falvo MJ, Faigenbaum AD. Effects of protein supplementation on muscular performance and resting hormonal changes in college football players. J Sports Sci Med. 2007;6(1):85–92.
    1. Schoenfeld BJ, Aragon A, Wilborn C, Urbina SL, Hayward SE, Krieger J. Pre- versus post-exercise protein intake has similar effects on muscular adaptations. Peer J. 2017;5:1. doi: 10.17159/1727-3781/2002/v5i1a2875.
    1. Townsend R, Elliott-Sale KJ, Currell K, Tang J, Fraser WD, Sale C. The effect of Postexercise carbohydrate and protein ingestion on bone metabolism. Med Sci Sports Exerc. 2017;49(6):1209–1218. doi: 10.1249/MSS.0000000000001211.
    1. Sale C, Varley I, Jones TW, James RM, Tang JCY, Fraser WD, et al. Effect of carbohydrate feeding on the bone metabolic response to running. J Appl Physiol. 2015;119(7):824–830. doi: 10.1152/japplphysiol.00241.2015.
    1. Szulc P, Naylor K, Hoyle NR, Eastell R, Leary ET. National Bone Health Alliance Bone Turnover Marker Project. Use of CTX-I and PINP as bone turnover markers: National Bone Health Alliance recommendations to standardize sample handling and patient preparation to reduce pre-analytical variability. Osteoporos Int. 2017;28(9):2541–2556. doi: 10.1007/s00198-017-4082-4.
    1. Candow DG, Chilibeck PD, Facci M, Abeysekara S, Zello GA. Protein supplementation before and after resistance training in older men. Eur J Appl Physiol. 2006;97(5):548–556. doi: 10.1007/s00421-006-0223-8.
    1. Moore DR, Volterman KA, Obeid J, Offord EA, Timmons BW. Postexercise protein ingestion increases whole body net protein balance in healthy children. J Appl Physiol. 2014;117(12):1493–1501. doi: 10.1152/japplphysiol.00224.2014.
    1. Argopur Davisco Business Unit. BiPro Protein Powder [Internet]. BiPro USA. [Cited 17 Oct 2018]. Available from: .
    1. Mirwald RL, Baxter-Jones ADG, Bailey DA, Beunen GP. An assessment of maturity from anthropometric measurements. Med Sci Sports Exerc. 2002;34(4):689–694.
    1. Subar AF, Thompson FE, Kipnis V, Midthune D, Hurwitz P, McNutt S, et al. Comparative validation of the block, Willett, and National Cancer Institute food frequency questionnaires the eating at America’s table study. Am J Epidemiol. 2001;154(12):1089–1099. doi: 10.1093/aje/154.12.1089.
    1. Dekker J, Nelson K, Kurgan N, Falk B, Josse A, Klentrou P. Wnt signaling-related Osteokines and transforming growth factors before and after a single bout of plyometric exercise in child and adolescent females. Pediatr Exerc Sci. 2017;29(4):504–512. doi: 10.1123/pes.2017-0042.
    1. Vilela S, Severo M, Moreira T, Ramos E, Lopes C. Evaluation of a short food frequency questionnaire for dietary intake assessment among children. Eur J Clin Nutr. 2018;30:1.
    1. Strumia MM, Sample AB, Hart ED. An improved micro hematocrit method. Am J Clin Pathol. 1954;24(9):1016–1024. doi: 10.1093/ajcp/24.9.1016.
    1. Rotstein A, Falk B, Einbinder M, Zigel L. Changes in plasma volume following intense intermittent exercise in neutral and hot environmental conditions. J Sports Med Phys Fitness. 1998;38(1):24–29.
    1. Van Beaumont W. Evaluation of hemoconcentration from hematocrit measurements. J Appl Physiol. 1972;32(5):712–713. doi: 10.1152/jappl.1972.32.5.712.
    1. Vasikaran S, Cooper C, Eastell R, Griesmacher A, Morris HA, Trenti T, et al. International Osteoporosis Foundation and International Federation of Clinical Chemistry and Laboratory Medicine position on bone marker standards in osteoporosis. Clin Chem Lab Med. 2011;49(8):1271–1274. doi: 10.1515/CCLM.2011.602.
    1. Lee J, Vasikaran S. Current recommendations for laboratory testing and use of bone turnover markers in management of osteoporosis. Ann Lab Med. 2012;32(2):105–112. doi: 10.3343/alm.2012.32.2.105.
    1. Seibel MJ. Biochemical markers of bone turnover part I: biochemistry and variability. Clin Biochem Rev. 2005;26(4):97–122.
    1. Bieglmayer C, Kudlacek S. The bone marker plot: an innovative method to assess bone turnover in women. Eur J Clin Investig. 2009;39(3):230–238. doi: 10.1111/j.1365-2362.2009.02087.x.
    1. Nakatoh S. The importance of assessing the rate of bone turnover and the balance between bone formation and bone resorption during daily teriparatide administration for osteoporosis: a pilot study. J Bone Miner Metab. 2016;34(2):216–224. doi: 10.1007/s00774-015-0665-3.
    1. Shieh A, Han W, Ishii S, Greendale GA, Crandall CJ, Karlamangla AS. Quantifying the balance between Total bone formation and Total bone resorption: an index of net bone formation. J Clin Endocrinol Metab. 2016;101(7):2802–2809. doi: 10.1210/jc.2015-4262.
    1. Obermayer-Pietsch B, Schwetz V. Utility of the determination of biomarkers of bone metabolism. In: Pietschmann P, editor. Principles of Osteoimmunology: molecular mechanisms and clinical applications. Cham: Springer International Publishing; 2016. pp. 125–148.
    1. Eastell R, Robins SP, Colwell T, Assiri AMA, Riggs BL, Russell RGG. Evaluation of bone turnover in type I osteoporosis using biochemical markers specific for both bone formation and bone resorption. Osteoporos Int. 1993;3(5):255–260. doi: 10.1007/BF01623829.
    1. Rauchenzauner M, Schmid A, Heinz-Erian P, Kapelari K, Falkensammer G, Griesmacher A, et al. Sex- and age-specific reference curves for serum markers of bone turnover in healthy children from 2 months to 18 years. J Clin Endocrinol Metab. 2007;92(2):443–449. doi: 10.1210/jc.2006-1706.
    1. Field A. Discovering Statistics Using SPSS. 3rd Edition. London: Sage Publications Ltd.; 2009. p. 857.
    1. Pallant J. SPSS survival manual: a step-by-step guide to data analysis using SPSS for windows (versions 10 and 11); [applies to SPSS for windows up to version 11]. Reprinted. Buckingham: Open Univ. Press; 2003. p. 286.
    1. Guillemant J, Le HCT, Maria AH, Guillemant S. Acute effects of oral calcium load on parathyroid function and on bone resorption in young men. Am J Nephrol. 2000;20(1):48–52. doi: 10.1159/000013555.
    1. Scott JPR, 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. J Clin Endocrinol Metab. 2010;95(8):3918–3925. doi: 10.1210/jc.2009-2516.
    1. Bridge AD, Brown J, Snider H, Ward WE, Roy BD, Josse AR. Consumption of Greek yogurt during 12 weeks of high-impact loading exercise increases bone formation in young, adult males – a secondary analysis from a randomized trial. Appl Physiol Nutr Metab. 2020;45(1):91–100. doi: 10.1139/apnm-2019-0396.
    1. Jürimäe J. Interpretation and application of bone turnover markers in children and adolescents. Curr Opin Pediatr. 2010;22(4):494–500. doi: 10.1097/MOP.0b013e32833b0b9e.
    1. Bayer M. Reference values of osteocalcin and procollagen type I N-propeptide plasma levels in a healthy central European population aged 0–18 years. Osteoporos Int. 2014;25(2):729–736. doi: 10.1007/s00198-013-2485-4.
    1. Lampl M, Johnston FE, Malcolm LA. The effects of protein supplementation on the growth and skeletal maturation of new Guinean school children. Ann Hum Biol. 1978;5(3):219–227. doi: 10.1080/03014467800002841.
    1. Ballard TL, Clapper JA, Specker BL, Binkley TL, Vukovich MD. Effect of protein supplementation during a 6-mo strength and conditioning program on insulin-like growth factor I and markers of bone turnover in young adults. Am J Clin Nutr. 2005;81(6):1442–1448. doi: 10.1093/ajcn/81.6.1442.
    1. Hannan MT, Tucker KL, Dawson-Hughes B, Cupples LA, Felson DT, Kiel DP. Effect of dietary protein on bone loss in elderly men and women: the Framingham osteoporosis study. J Bone Miner Res. 2000;15(12):2504–2512. doi: 10.1359/jbmr.2000.15.12.2504.

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