Comparison of Watermelon and Carbohydrate Beverage on Exercise-Induced Alterations in Systemic Inflammation, Immune Dysfunction, and Plasma Antioxidant Capacity

R Andrew Shanely, David C Nieman, Penelope Perkins-Veazie, Dru A Henson, Mary P Meaney, Amy M Knab, Lynn Cialdell-Kam, R Andrew Shanely, David C Nieman, Penelope Perkins-Veazie, Dru A Henson, Mary P Meaney, Amy M Knab, Lynn Cialdell-Kam

Abstract

Consuming carbohydrate- and antioxidant-rich fruits during exercise as a means of supporting and enhancing both performance and health is of interest to endurance athletes. Watermelon (WM) contains carbohydrate, lycopene, l-citrulline, and l-arginine. WM may support exercise performance, augment antioxidant capacity, and act as a countermeasure to exercise-induced inflammation and innate immune changes. Trained cyclists (n = 20, 48 ± 2 years) participated in a randomized, placebo controlled, crossover study. Subjects completed two 75 km cycling time trials after either 2 weeks ingestion of 980 mL/day WM puree or no treatment. Subjects drank either WM puree containing 0.2 gm/kg carbohydrate or a 6% carbohydrate beverage every 15 min during the time trials. Blood samples were taken pre-study and pre-, post-, 1 h post-exercise. WM ingestion versus no treatment for 2-weeks increased plasma l-citrulline and l-arginine concentrations (p < 0.0125). Exercise performance did not differ between WM puree or carbohydrate beverage trials (p > 0.05), however, the rating of perceived exertion was greater during the WM trial (p > 0.05). WM puree versus carbohydrate beverage resulted in a similar pattern of increase in blood glucose, and greater increases in post-exercise plasma antioxidant capacity, l-citrulline, l-arginine, and total nitrate (all p < 0.05), but without differences in systemic markers of inflammation or innate immune function. Daily WM puree consumption fully supported the energy demands of exercise, and increased post-exercise blood levels of WM nutritional components (l-citrulline and l-arginine), antioxidant capacity, and total nitrate, but without an influence on post-exercise inflammation and changes in innate immune function.

Keywords: ">l-arginine; ">l-citrulline; endurance exercise performance; ferric reducing ability of plasma (FRAP); oxygen radical absorbance capacity (ORAC); total nitrate.

Figures

Figure 1
Figure 1
Watermelon consumption during exercise potentiates the exercise-induced increase in plasma antioxidant capacity. (A) Plasma FRAP = ferric reducing ability of plasma (expressed as ascorbate equivalents) and (B) plasma ORAC = oxygen radical absorbance capacity (expressed as trolox equivalents) were higher in WM compared to CHO following 75 km cycling (interaction effect, p < 0.001, each); * p < 0.0125 compared to time matched CHO.
Figure 2
Figure 2
Watermelon consumption increases plasma l-citrulline (interaction effect p < 0.001), l-arginine (interaction effect p < 0.001), and total nitrate (interaction effect p = 0.004). Plasma concentrations of (A) l-citrulline; (B) arginine; and (C) total nitrate; # p < 0.0125 compared to baseline; * p < 0.0125 compared to time matched CHO.

References

    1. Levine S.A., Gordon B., Derick C.L. Some changes in the chemical constituents of the blood following a marathon race: With special reference to the development of hypoglycemia. J. Am. Med. Assoc. 1924;82:1778–1779. doi: 10.1001/jama.1924.02650480034015.
    1. Gordon B., Kohn L.A., Levine S.A., Matton M., Scriver W.M., Whiting W.B. Sugar content of the blood in runners following a marathon race: With especial reference to the prevention of hypoglycemia: Further observations. J. Am. Med. Assoc. 1925;85:508–509. doi: 10.1001/jama.1925.02670070028009.
    1. Coyle E.F., Hagberg J.M., Hurley B.F., Martin W.H., Ehsani A.A., Holloszy J.O. Carbohydrate feeding during prolonged strenuous exercise can delay fatigue. J. Appl. Physiol. 1983;55:230–235.
    1. Carter J., Jeukendrup A.E., Mundel T., Jones D.A. Carbohydrate supplementation improves moderate and high-intensity exercise in the heat. Pflug. Arch. 2003;446:211–219. doi: 10.1007/s00424-003-1020-4.
    1. De Sousa M.V., Madsen K., Fukui R., Santos A., da Silva M.E. Carbohydrate supplementation delays DNA damage in elite runners during intensive microcycle training. Eur. J. Appl. Physiol. 2012;112:493–500. doi: 10.1007/s00421-011-2000-6.
    1. Scharhag J., Meyer T., Auracher M., Gabriel H.H., Kindermann W. Effects of graded carbohydrate supplementation on the immune response in cycling. Med. Sci. Sports Exerc. 2006;38:286–292. doi: 10.1249/01.mss.0000191437.69493.d4.
    1. Jentjens R.L., Moseley L., Waring R.H., Harding L.K., Jeukendrup A.E. Oxidation of combined ingestion of glucose and fructose during exercise. J. Appl. Physiol. 2004;96:1277–1284. doi: 10.1152/japplphysiol.00974.2003.
    1. Shi X., Summers R.W., Schedl H.P., Flanagan S.W., Chang R., Gisolfi C.V. Effects of carbohydrate type and concentration and solution osmolality on water absorption. Med. Sci. Sports Exerc. 1995;27:1607–1615. doi: 10.1249/00005768-199512000-00005.
    1. O’Brien W.J., Stannard S.R., Clarke J.A., Rowlands D.S. Fructose-maltodextrin ratio governs exogenous and other cho oxidation and performance. Med. Sci. Sports Exerc. 2013;45:1814–1824. doi: 10.1249/MSS.0b013e31828e12d4.
    1. Too B.W., Cicai S., Hockett K.R., Applegate E., Davis B.A., Casazza G.A. Natural versus commercial carbohydrate supplementation and endurance running performance. J. Int. Soc. Sports Nutr. 2012;9:27–35. doi: 10.1186/1550-2783-9-27.
    1. Murdoch S.D., Bazzarre T.L., Snider I.P., Goldfarb A.H. Differences in the effects of carbohydrate food form on endurance performance to exhaustion. Int. J. Sport Nutr. 1993;3:41–54. doi: 10.1123/ijsn.3.1.41.
    1. Nieman D.C., Gillitt N.D., Henson D.A., Sha W., Shanely R.A., Knab A.M., Cialdella-Kam L., Jin F. Bananas as an energy source during exercise: A metabolomics approach. PLoS ONE. 2012;7:518. doi: 10.1371/journal.pone.0037479.
    1. Nieman D.C., Gillitt N.D., Sha W., Meaney M.P., John C., Pappan K.L., Kinchen J.M. Metabolomics-based analysis of banana and pear ingestion on exercise performance and recovery. J. Proteome Res. 2015;14:5367–5377. doi: 10.1021/acs.jproteome.5b00909.
    1. U.S. Department of Agriculture USDA National Nutrient Database for Standard Reference, Release 27. [(accessed on 10 July 2014)]; Available online: .
    1. Rimando A.M., Perkins-Veazie P.M. Determination of citrulline in watermelon rind. J. Chromatogr. A. 2005;1078:196–200. doi: 10.1016/j.chroma.2005.05.009.
    1. Ghavipour M., Saedisomeolia A., Djalali M., Sotoudeh G., Eshraghyan M.R., Moghadam A.M., Wood L.G. Tomato juice consumption reduces systemic inflammation in overweight and obese females. Br. J. Nutr. 2013;109:2031–2035. doi: 10.1017/S0007114512004278.
    1. Gann P.H., Ma J., Giovannucci E., Willett W., Sacks F.M., Hennekens C.H., Stampfer M.J. Lower prostate cancer risk in men with elevated plasma lycopene levels: Results of a prospective analysis. Cancer Res. 1999;59:1225–1230.
    1. Stahl W., Sies H. Antioxidant activity of carotenoids. Mol. Aspects Med. 2003;24:345–351. doi: 10.1016/S0098-2997(03)00030-X.
    1. Moran N.E., Cichon M.J., Riedl K.M., Grainger E.M., Schwartz S.J., Novotny J.A., Erdman J.W., Jr., Clinton S.K. Compartmental and noncompartmental modeling of (1)(3)c-lycopene absorption, isomerization, and distribution kinetics in healthy adults. Am. J. Clin. Nutr. 2015;102:1436–1449. doi: 10.3945/ajcn.114.103143.
    1. Tsitsimpikou C., Kioukia-Fougia N., Tsarouhas K., Stamatopoulos P., Rentoukas E., Koudounakos A., Papalexis P., Liesivuori J., Jamurtas A. Administration of tomato juice ameliorates lactate dehydrogenase and creatinine kinase responses to anaerobic training. Food Chem. Toxicol. 2013;61:9–13. doi: 10.1016/j.fct.2012.12.023.
    1. Harms-Ringdahl M., Jenssen D., Haghdoost S. Tomato juice intake suppressed serum concentration of 8-oxodg after extensive physical activity. Nutr. J. 2012;11:29. doi: 10.1186/1475-2891-11-29.
    1. Wu G., Morris S.M., Jr. Arginine metabolism: Nitric oxide and beyond. Biochem. J. 1998;336:1–17. doi: 10.1042/bj3360001.
    1. Sureda A., Cordova A., Ferrer M.D., Tauler P., Perez G., Tur J.A., Pons A. Effects of l-citrulline oral supplementation on polymorphonuclear neutrophils oxidative burst and nitric oxide production after exercise. Free Radic. Res. 2009;43:828–835. doi: 10.1080/10715760903071664.
    1. Bradley S.J., Kingwell B.A., McConell G.K. Nitric oxide synthase inhibition reduces leg glucose uptake but not blood flow during dynamic exercise in humans. Diabetes. 1999;48:1815–1821. doi: 10.2337/diabetes.48.9.1815.
    1. Mandel H., Levy N., Izkovitch S., Korman S.H. Elevated plasma citrulline and arginine due to consumption of citrullus vulgaris (watermelon) J. Inherit. Metab. Dis. 2005;28:467–472. doi: 10.1007/s10545-005-0467-1.
    1. Collins J.K., Wu G., Perkins-Veazie P., Spears K., Claypool P.L., Baker R.A., Clevidence B.A. Watermelon consumption increases plasma arginine concentrations in adults. Nutrition. 2007;23:261–266. doi: 10.1016/j.nut.2007.01.005.
    1. Root M.M., McGinn M.C., Nieman D.C., Henson D.A., Heinz S.A., Shanely R.A., Knab A.M., Jin F. Combined fruit and vegetable intake is correlated with improved inflammatory and oxidant status from a cross-sectional study in a community setting. Nutrients. 2012;4:29–41. doi: 10.3390/nu4010029.
    1. Akashi K., Miyake C., Yokota A. Citrulline, a novel compatible solute in drought-tolerant wild watermelon leaves, is an efficient hydroxyl radical scavenger. FEBS Lett. 2001;508:438–442. doi: 10.1016/S0014-5793(01)03123-4.
    1. Müller L., Fröhlich K., Böhm V. Comparative antioxidant activities of carotenoids measured by ferric reducing antioxidant power (FRAP), abts bleaching assay (αTEAC), DPPH assay and peroxyl radical scavenging assay. Food Chem. 2011;129:139–148. doi: 10.1016/j.foodchem.2011.04.045.
    1. Benzie I.F., Strain J.J. The ferric reducing ability of plasma (FRAP) as a measure of “antioxidant power”: The frap assay. Anal. Biochem. 1996;239:70–76. doi: 10.1006/abio.1996.0292.
    1. Edwards A.J., Vinyard B.T., Wiley E.R., Brown E.D., Collins J.K., Perkins-Veazie P., Baker R.A., Clevidence B.A. Consumption of watermelon juice increases plasma concentrations of lycopene and beta-carotene in humans. J. Nutr. 2003;133:1043–1050.
    1. Tarazona-Diaz M.P., Alacid F., Carrasco M., Martinez I., Aguayo E. Watermelon juice: Potential functional drink for sore muscle relief in athletes. J. Agric. Food Chem. 2013;61:7522–7528. doi: 10.1021/jf400964r.
    1. Cutrufello P.T., Gadomski S.J., Zavorsky G.S. The effect of l-citrulline and watermelon juice supplementation on anaerobic and aerobic exercise performance. J. Sports Sci. 2015;33:1459–1466. doi: 10.1080/02640414.2014.990495.
    1. U.S. Department of Agriculture USDA National Nutrient Database for Standard Reference, Release 27. [(accessed on 17 July 2015)];2015 Available online: .
    1. Dill D.B., Costill D.L. Calculation of percentage changes in volumes of blood, plasma, and red cells in dehydration. J. Appl. Physiol. 1974;37:247–248.
    1. Knab A.M., Nieman D.C., Gillitt N.D., Shanely R.A., Cialdella-Kam L., Henson D., Sha W., Meaney M.P. Effects of a freeze-dried juice blend powder on exercise-induced inflammation, oxidative stress, and immune function in cyclists. Appl. Physiol. Nutr. Metab. 2014;39:381–385. doi: 10.1139/apnm-2013-0338.
    1. Meaney M.P., Nieman D.C., Henson D.A., Jiang Q., Wang F.Z. Measuring granulocyte and monocyte phagocytosis and oxidative burst activity in human blood. J. Vis. Exp. 2016 in press.
    1. Shanely R.A., Knab A.M., Nieman D.C., Jin F., McAnulty S.R., Landram M.J. Quercetin supplementation does not alter antioxidant status in humans. Free Radic. Res. 2010;44:224–231. doi: 10.3109/10715760903407293.
    1. Wu G., Meininger C.J. Analysis of citrulline, arginine, and methylarginines using high-performance liquid chromatography. Methods Enzymol. 2008;440:177–189.
    1. Nieman D.C., Nehlsen-Cannarella S.L., Fagoaga O.R., Henson D.A., Utter A., Davis J.M., Williams F., Butterworth D.E. Influence of mode and carbohydrate on the cytokine response to heavy exertion. Med. Sci. Sports Exerc. 1998;30:671–678. doi: 10.1097/00005768-199805000-00005.
    1. Perkins-Veazie P., Collins J.K., Davis A.R., Roberts W. Carotenoid content of 50 watermelon cultivars. J. Agric. Food Chem. 2006;54:2593–2597. doi: 10.1021/jf052066p.
    1. Rodriguez N.R., Di Marco N.M., Langley S. American College of Sports Medicine position stand: Nutrition and athletic performance. Med. Sci. Sports Exerc. 2009;41:709–731.
    1. Fujisawa T., Mulligan K., Wada L., Schumacher L., Riby J., Kretchmer N. The effect of exercise on fructose absorption. Am. J. Clin. Nutr. 1993;58:75–79.
    1. Jeukendrup A.E., Jentjens R. Oxidation of carbohydrate feedings during prolonged exercise: Current thoughts, guidelines and directions for future research. Sports Med. 2000;29:407–424. doi: 10.2165/00007256-200029060-00004.
    1. Sawka M.N., Burke L.M., Eichner E.R., Maughan R.J., Montain S.J., Stachenfeld N.S. American College of Sports Medicine position stand. Exercise and fluid replacement. Med. Sci. Sports Exerc. 2007;39:377–390.
    1. Cao G., Prior R.L. Comparison of different analytical methods for assessing total antioxidant capacity of human serum. Clin. Chem. 1998;44:1309–1315.
    1. Duthie G., Robertson J., Maughan R., Morrice P. Blood antioxidant status and erythrocyte lipid peroxidation following distance running. Arch. Biochem. Biophys. 1990;282:78–83. doi: 10.1016/0003-9861(90)90089-H.
    1. Perheentupa J., Raivio K. Fructose-induced hyperuricaemia. Lancet. 1967;2:528–531. doi: 10.1016/S0140-6736(67)90494-1.
    1. McAnulty S.R., Hosick P.A., McAnulty L.S., Quindry J.C., Still L., Hudson M.B., Dibarnardi A.N., Milne G.L., Morrow J.D., Austin M.D. Effect of pharmacological lowering of plasma urate on exercise-induced oxidative stress. Appl. Physiol. Nutr. Metab. 2007;32:1148–1155. doi: 10.1139/H07-131.
    1. Quindry J.C., Kavazis A.N., Powers S.K. The Encyclopaedia of Sports Medicine. John Wiley & Sons Ltd.; Chichester, UK: 2013. Exercise-induced oxidative stress: Are supplemental antioxidants warranted? pp. 263–276.
    1. Kruger K., Pilat C., Schild M., Lindner N., Frech T., Muders K., Mooren F.C. Progenitor cell mobilization after exercise is related to systemic levels of G-CSF and muscle damage. Scand. J. Med. Sci. Sports. 2015;25:e283–e291. doi: 10.1111/sms.12320.
    1. Mooren F.C., Volker K., Klocke R., Nikol S., Waltenberger J., Kruger K. Exercise delays neutrophil apoptosis by a G-CSF-dependent mechanism. J. Appl. Physiol. 2012;113:1082–1090. doi: 10.1152/japplphysiol.00797.2012.
    1. Yamada M., Suzuki K., Kudo S., Totsuka M., Nakaji S., Sugawara K. Raised plasma G-CSF and il-6 after exercise may play a role in neutrophil mobilization into the circulation. J. Appl. Physiol. 2002;92:1789–1794. doi: 10.1152/japplphysiol.00629.2001.
    1. Moinard C., Nicolis I., Neveux N., Darquy S., Benazeth S., Cynober L. Dose-ranging effects of citrulline administration on plasma amino acids and hormonal patterns in healthy subjects: The citrudose pharmacokinetic study. Br. J. Nutr. 2008;99:855–862. doi: 10.1017/S0007114507841110.
    1. Hickner R.C., Tanner C.J., Evans C.A., Clark P.D., Haddock A., Fortune C., Geddis H., Waugh W., McCammon M. l-citrulline reduces time to exhaustion and insulin response to a graded exercise test. Med. Sci. Sports Exerc. 2006;38:660–666. doi: 10.1249/01.mss.0000210197.02576.da.
    1. Suzuki T., Morita M., Kobayashi Y., Kamimura A. Oral l-citrulline supplementation enhances cycling time trial performance in healthy trained men: Double-blind randomized placebo-controlled 2-way crossover study. J. Int. Soc. Sports Nutr. 2016;13:6. doi: 10.1186/s12970-016-0117-z.
    1. Bailey S.J., Blackwell J.R., Lord T., Vanhatalo A., Winyard P.G., Jones A.M. l-citrulline supplementation improves O2 uptake kinetics and high-intensity exercise performance in humans. J. Appl. Physiol. 2015;119:385–395. doi: 10.1152/japplphysiol.00192.2014.

Source: PubMed

3
Abonneren