Abstract
Purpose
The impact of ingesting carbohydrates alone or combined with proteins to support exercise immune adaptation in endurance athletes is scarcely investigated. The present study compares the effect of ingesting a combined protein–carbohydrate supplement vs. a carbohydrate-only supplement post-workout on immune inflammation markers following a 10 week periodized endurance training program in well-trained athletes.
Methods
Twenty-five men completed the study after being randomly assigned to one of the following intervention groups: combined protein–carbohydrate (PRO-CHO n = 12, 31 ± 9 years, \(\dot{\mathrm{V}}\)O2peak 61.0 ± 5.6 ml.kg−1.min−1) or non-protein isoenergetic carbohydrate (CHO, n = 13, 33 ± 8 years, \(\dot{\mathrm{V}}\)O2peak 60.6 ± 6.9 ml.kg−1.min−1). Treatment consisted of ingesting 24 g of assigned supplement, mixed with 250 ml of orange juice, once a day for 10 weeks immediately post-workout (or before breakfast on non-training days). Measurements were conducted pre- and post-intervention on total leukocytes, leukocyte subsets (i.e., neutrophils, eosinophils, basophils, monocytes, and lymphocytes), and platelets. The inflammatory status was assessed by the neutrophil-to-lymphocyte ratio (NLR), the platelet-to-lymphocyte ratio (PLR), and the systemic-immune inflammation index (SII).
Results
Post-intervention, significant increases were observed for CHO group only for the three inflammatory markers: NLR (p = 0.050, d = 0.58), PLR (p = 0.041, d = 0.60), and SII (p = 0.004, d = 0.81) but not for PRO-CHO (p > 0.05).
Conclusion
Ingesting a post-workout protein–carbohydrate combined beverage promoted a more favourable immune status than carbohydrate-only ingestion by attenuating cellular inflammation over a 10 week training period in endurance male athletes.
Trial Registration
The study was registered in ClinicalTrials.gov with the following ID: NCT02954367. The study was registered by 3 November 2016.
Similar content being viewed by others
Data availability
Data are available upon request to the corresponding author.
References
Albers R, Antoine JM, Bourdet-Sicard R, Calder PC, Gleeson M, Lesourd B, Samartin S, Sanderson IR, Van Loo J, Vas Dias FW, Watzl B (2005) Markers to measure immunomodulation in human nutrition intervention studies. Br J Nutr 94(3):452–481. https://doi.org/10.1079/bjn20051469
Bessa AL, Oliveira VN, Agostini GG, Oliveira RJ, Oliveira AC, White GE, Wells GD, Teixeira DN, Espindola FS (2016) Exercise intensity and recovery: biomarkers of injury, inflammation, and oxidative stress. J Strength Cond Res 30(2):311–319. https://doi.org/10.1519/JSC.0b013e31828f1ee9
Bishop N (2006) Acute exercise and aquired immune function. Immune Function in Sport and Exercise Advances in Sport and Exercise Science. Churchill Livingstone Elsevier, Amsterdam Netherland, pp 91–113
Calder PC, Jackson AA (2000) Undernutrition, infection and immune function. Nutr Res Rev 13(1):3–29. https://doi.org/10.1079/095442200108728981
Campbell JP, Turner JE (2018) Debunking the myth of exercise-induced immune suppression: redefining the impact of exercise on immunological health across the lifespan. Front Immunol 9:648. https://doi.org/10.3389/fimmu.2018.00648
Chen CY, Liao YH, Chou CC, Sung YC, Tsai SC (2017) Initial systemic inflammatory state perturbs exercise training adaptations in elite Taekwondo athletes. PLoS ONE 12(4):e0176140. https://doi.org/10.1371/journal.pone.0176140
Chen YJ, Wong SH, Wong CK, Lam CW, Huang YJ, Siu PM (2008) The effect of a pre-exercise carbohydrate meal on immune responses to an endurance performance run. Br J Nutr 100(6):1260–1268. https://doi.org/10.1017/S0007114508975619
Cohen J (1988) Statistical power analysis for the behavioral sciences, 2nd edn. Lawrence Erlbaum, Mahwah, NJ
Costa RJ, Walters R, Bilzon JL, Walsh NP (2011) Effects of immediate postexercise carbohydrate ingestion with and without protein on neutrophil degranulation. Int J Sport Nutr Exerc Metab 21(3):205–213. https://doi.org/10.1123/ijsnem.21.3.205
Cruzat VF, Krause M (2014) Newsholme P (2014) Amino acid supplementation and impact on immune function in the context of exercise. J Int Soc Sports Nutr 11(1):61. https://doi.org/10.1186/s12970-014-0061-8
Esteve-Lanao J, Foster C, Seiler S, Lucia A (2007) Impact of training intensity distribution on performance in endurance athletes. J Strength Cond Res 21(3):943–949. https://doi.org/10.1519/R-19725.1
Esteve-Lanao J, Moreno-Perez D, Cardona CA, Larumbe-Zabala E, Munoz I, Selles S, Cejuela R (2017) Is marathon training harder than the ironman training? ECO-Method Comp Front Physiol 8:298. https://doi.org/10.3389/fphys.2017.00298
Fest J, Ruiter R, Ikram MA, Voortman T, van Eijck CHJ, Stricker BH (2018) Reference values for white blood-cell-based inflammatory markers in the rotterdam study: a population-based prospective cohort study. Sci Rep 8(1):10566. https://doi.org/10.1038/s41598-018-28646-w
Gleeson M (2002) Biochemical and immunological markers of over-training. J Sports Sci Med 1(2):31–41
Gleeson M (2007) Immune function in sport and exercise. J Appl Physiol 103(2):693–699. https://doi.org/10.1152/japplphysiol.00008.2007
Gunzer W, Konrad M, Pail E (2012) Exercise-induced immunodepression in endurance athletes and nutritional intervention with carbohydrate, protein and fat-what is possible, what is not? Nutrients 4(9):1187–1212. https://doi.org/10.3390/nu4091187
Henson DA, Nieman DC, Blodgett AD, Butterworth DE, Utter A, Davis JM, Sonnenfeld G, Morton DS, Fagoaga OR, Nehlsen-Cannarella SL (1999) Influence of exercise mode and carbohydrate on the immune response to prolonged exercise. Int J Sport Nutr 9(2):213–228. https://doi.org/10.1123/ijsn.9.2.213
Jeukendrup A, Gleeson M (2010) Sport nutrition: an introduction to energy production and performance, 2nd edn. Human Kinetics. Champaign, IL, USA
Kato H, Suzuki K, Bannai M, Moore DR (2016) Protein requirements are elevated in endurance athletes after exercise as determined by the indicator amino acid oxidation method. PLoS ONE 11(6):e0157406. https://doi.org/10.1371/journal.pone.0157406
Li P, Yin YL, Li D, Kim SW, Wu G (2007) Amino acids and immune function. Br J Nutr 98(2):237–252. https://doi.org/10.1017/S000711450769936X
Maggini S, Pierre A, Calder PC (2018) Immune function and micronutrient requirements change over the life course. Nutrients 10(10):1531. https://doi.org/10.3390/nu10101531
Makras P, Koukoulis GN, Bourikas G, Papatheodorou G, Bedevis K, Menounos P, Pappas D, Kartalis G (2005) Effect of 4 weeks of basic military training on peripheral blood leucocytes and urinary excretion of catecholamines and cortisol. J Sports Sci 23(8):825–834. https://doi.org/10.1080/02640410400021815
Matsuo K, Kubota M, Sasaki H, Toyooka J, Nagatomi R (2009) The association of the blood lymphocytes to neutrophils ratio with overtraining in endurance athletes. New Studies Athletics 24:23–29
Mojtahedi MC, Thorpe MP, Karampinos DC, Johnson CL, Layman DK, Georgiadis JG, Evans EM (2011) The effects of a higher protein intake during energy restriction on changes in body composition and physical function in older women. J Gerontol A Biol Sci Med Sci 66(11):1218–1225. https://doi.org/10.1093/gerona/glr120
Moreno-Perez D, Marin PJ, Lopez-Samanes A, Cejuela R, Esteve-Lanao J (2020) Muscle activation in middle-distance athletes with compression stockings. Sensors 20(5):1268. https://doi.org/10.3390/s20051268
Mori H, Nishijo K, Kawamura H, Abo T (2002) Unique immunomodulation by electro-acupuncture in humans possibly via stimulation of the autonomic nervous system. Neurosci Lett 320(1–2):21–24. https://doi.org/10.1016/s0304-3940(02)00012-5
Naclerio F, Larumbe-Zabala E, Ashrafi N, Seijo M, Nielsen B, Allgrove J, Earnest CP (2017) Effects of protein–carbohydrate supplementation on immunity and resistance training outcomes: a double-blind, randomized, controlled clinical trial. Eur J Appl Physiol 117(2):267–277. https://doi.org/10.1007/s00421-016-3520-x
Naclerio F, Larumbe-Zabala E, Seijo M, Ashrafi N, Nielsen BV, Earnest CP (2019) Effects of protein versus carbohydrate supplementation on markers of immune response in master triathletes: a randomized controlled trial. J Am Coll Nutr 38(5):395–404. https://doi.org/10.1080/07315724.2018.1528906
Nieman DC, Pedersen BK (1999) Exercise and immune function. Rec Develop Sports Med 27(2):73–80. https://doi.org/10.2165/00007256-199927020-00001
Peake JM, Neubauer O, Walsh NP, Simpson R (2017) Recovery of the immune system after exercise. J Appl Physiol 122(5):1077–1087. https://doi.org/10.1152/japplphysiol.00622.2016
Pedersen BK, Hoffman-Goetz L (2000) Exercise and the immune system: regulation, integration, and adaptation. Physiol Rev 80(3):1055–1081. https://doi.org/10.1152/physrev.2000.80.3.1055
Pedersen BK, Rohde T, Ostrowski K (1998) Recovery of the immune system after exercise. Acta Physiol Scand 162(3):325–332. https://doi.org/10.1046/j.1365-201X.1998.0325e.x
Seiler KS, Kjerland GO (2006) Quantifying training intensity distribution in elite endurance athletes: is there evidence for an “optimal” distribution? Scand J Med Sci Sports 16(1):49–56. https://doi.org/10.1111/j.1600-0838.2004.00418.x
Skinner JS, McLellan TM (1980) The transition from aerobic to anaerobic metabolism. Res Q Exerc Sport 51(1):234–248. https://doi.org/10.1080/02701367.1980.10609285
Svendsen IS, Killer SC, Carter JM, Randell RK, Jeukendrup AE, Gleeson M (2016) Impact of intensified training and carbohydrate supplementation on immunity and markers of overreaching in highly trained cyclists. Eur J Appl Physiol 116(5):867–877. https://doi.org/10.1007/s00421-016-3340-z
Thomas DT, Erdman KA, Burke LM (2016) American college of sports medicine joint position statement nutrition and athletic performance. Med Sci Sports Exerc 48(3):543–568. https://doi.org/10.1249/MSS.0000000000000852
Valenzuela PL, Montalvo Z, Mata F, González M, Naclerio L-Z (2021) Effects of beef protein supplementation in male elite triathletes: a randomized, controlled, double-blind cross-over study. J Am Coll Nutr 40(1):53–60. https://doi.org/10.1080/07315724.2020.1727377
Vitale K, Getzin A (2019) Nutrition and supplement update for the endurance athlete: review and recommendations. Nutrients 11(6):1289. https://doi.org/10.3390/nu11061289
Walsh NP, Gleeson M, Pyne DB, Nieman DC, Dhabhar FS, Shephard RJ, Oliver SJ, Bermon S, Kajeniene A (2011) Position statement. Part two: maintaining immune health. Exerc Immunol Rev 17:64–103
Walzik D, Joisten N, Zacher J, Zimmer P (2021) Transferring clinically established immune inflammation markers into exercise physiology: focus on neutrophil-to-lymphocyte ratio, platelet-to-lymphocyte ratio and systemic immune-inflammation index. Eur J Appl Physiol 121(7):1803–1814. https://doi.org/10.1007/s00421-021-04668-7
Acknowledgements
The authors wish to thank the subjects for their invaluable contribution to the study.
Funding
Research funding Real Madrid-European University of Madrid 2016/RM05. M. L. holds a Ramón y Cajal Fellowship 2012 11910. However, these do not affect this original research content and purpose.
Author information
Authors and Affiliations
Contributions
The study was designed by FN. Data were collected by DM and ML, and data were analysed by MR, AL, ELZ, and FN. Interpretation and manuscript preparation were undertaken by FN, DM, ML, ELZ, JR, and AL. All authors approved the final version of the paper. We would like to thank the “Run Faster & Better training group” for their participation in this project.
Corresponding author
Ethics declarations
Conflict of interest
The authors declare that they have no conflicts of interest relevant to the content of this manuscript.
Additional information
Communicated by Fabio Fischetti.
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Rights and permissions
Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.
About this article
Cite this article
Moreno-Pérez, D., López-Samanes, Á., Larrosa, M. et al. Effects of protein–carbohydrate vs. carbohydrate alone supplementation on immune inflammation markers in endurance athletes: a randomized controlled trial. Eur J Appl Physiol 123, 1495–1505 (2023). https://doi.org/10.1007/s00421-023-05168-6
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00421-023-05168-6