Effect of 4-Week Ingestion of Tomato-Based Carotenoids on Exercise-Induced Inflammation, Muscle Damage, and Oxidative Stress in Endurance Runners

in International Journal of Sport Nutrition and Exercise Metabolism
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This double-blind, randomized, placebo-controlled crossover trial determined if ingestion of a supplement containing a tomato complex with lycopene, phytoene, and phytofluene (T-LPP) and other compounds for 4 weeks would attenuate inflammation, muscle damage, and oxidative stress postexercise and during recovery from a 2-hr running bout that included 30 min of −10% downhill running. Study participants ingested the T-LPP supplement or placebo with the evening meal for 4 weeks prior to running 2 hr at high intensity. Blood samples and delayed onset muscle soreness ratings were taken pre- and post-4-week supplementation, and immediately following the 2-hr run, and then 1-hr, 24-hr, and 48-hr postrun. After a 2-week washout period, participants crossed over to the opposite treatment and repeated all procedures. Plasma lycopene, phytoene, and phytofluene increased significantly in T-LPP compared with placebo (p < .001 for each). Significant time effects were shown for serum creatine kinase, delayed onset muscle soreness, C-reactive protein, myoglobin, 9- and 13-hydroxyoctadecadienoic acids, ferric reducing ability of plasma, and six plasma cytokines (p < .001 for each). The pattern of increase for serum myoglobin differed between T-LPP and placebo (interaction effect, p = .016, with lower levels in T-LPP), but not for creatine kinase, delayed onset muscle soreness, C-reactive protein, the six cytokines, 9- and 13-hydroxyoctadecadienoic acids, and ferric reducing ability of plasma. No significant time or interaction effects were measured for plasma-oxidized low-density lipoprotein or serum 8-hydroxy-2′-deoxyguanosine. In summary, supplementation with T-LPP over a 4-week period increased plasma carotenoid levels 73% and attenuated postexercise increases in the muscle damage biomarker myoglobin, but not inflammation and oxidative stress.

Nieman, C.L. Capps, C.R. Capps, Shue, and McBride are with the Human Performance Lab, North Carolina Research Campus, Appalachian State University, Kannapolis, NC.

Address author correspondence to David C. Nieman at niemandc@appstate.edu.
  • Agarwal, S., & Rao, A.V. (1998). Tomato lycopene and low density lipoprotein oxidation: A human dietary intervention study. Lipids, 33, 981–984. PubMed doi:10.1007/s11745-998-0295-6

    • Crossref
    • Search Google Scholar
    • Export Citation
  • Benzie, I.F., & Strain, J.J. (1996). The ferric reducing ability of plasma (FRAP) as a measure of ‘antioxidant power’: The FRAP assay. Analytical Biochemistry, 239, 70–76. PubMed doi:10.1006/abio.1996.0292

    • Crossref
    • Search Google Scholar
    • Export Citation
  • Brancaccio, P., Lippi, G., & Maffulli, N. (2010). Biochemical markers of muscular damage. Clinical Chemistry and Laboratory Medicine, 48, 757–767. PubMed doi:10.1515/CCLM.2010.179

    • Crossref
    • Search Google Scholar
    • Export Citation
  • Burton-Freeman, B., & Sesso, H.D. (2014). Whole food versus supplement: Comparing the clinical evidence of tomato intake and lycopene supplementation on cardiovascular risk factors. Advances in Nutrition, 5, 457–485. PubMed doi:10.3945/an.114.005231

    • Crossref
    • Search Google Scholar
    • Export Citation
  • Chen, J., Song, Y., & Zhang, L. (2013). Effect of lycopene supplementation on oxidative stress: An exploratory systematic review and meta-analysis of randomized controlled trials. Journal of Medicinal Food, 16, 361–374. PubMed doi:10.1089/jmf.2012.2682

    • Crossref
    • Search Google Scholar
    • Export Citation
  • Deplanque, X., Muscente-Paque, D., & Chappuis, E. (2016). Proprietary tomato extract improves metabolic response to high-fat meal in healthy normal weight subjects. Food & Nutrition Research, 60, 32537. PubMed doi:10.3402/fnr.v60.32537

    • Crossref
    • Search Google Scholar
    • Export Citation
  • Devaraj, S., Mathur, S., Basu, A., Aung, H.H., Vasu, V.T., Meyers, S., & Jialal, I. (2008). A dose-response study on the effects of purified lycopene supplementation on biomarkers of oxidative stress. Journal of the American College of Nutrition, 27, 267–273. PubMed doi:10.1080/07315724.2008.10719699

    • Crossref
    • Search Google Scholar
    • Export Citation
  • Eliassen, A.H., Liao, X., Rosner, B., Tamimi, R.M., Tworoger, S.S., & Hankinson, S.E. (2015). Plasma carotenoids and risk of breast cancer over 20 y of follow-up. American Journal of Clinical Nutrition, 101, 1197–1205. PubMed doi:10.3945/ajcn.114.105080

    • Crossref
    • Search Google Scholar
    • Export Citation
  • Gann, P.H., Ma, J., Giovannucci, E., Willett, W., Sacks, F.M., Hennekens, C.H., & Stampfer, M.J. (1999). Lower prostate cancer risk in men with elevated plasma lycopene levels: Results of a prospective analysis. Cancer Research, 59, 1225–1230. PubMed

    • Search Google Scholar
    • Export Citation
  • Ghavipour, M., Saedisomeolia, A., Djalali, M., Sotoudeh, G., Eshraghyan, M.R., Moghadam, A.M., & Wood, L.G. (2013). Tomato juice consumption reduces systemic inflammation in overweight and obese females. British Journal of Nutrition, 109, 2031–2035. PubMed doi:10.1017/S0007114512004278

    • Crossref
    • Search Google Scholar
    • Export Citation
  • Harms-Ringdahl, M., Jenssen, D., & Haghdoost, S. (2012). Tomato juice intake suppressed serum concentration of 8-oxodG after extensive physical activity. Nutrition Journal, 11, 29. PubMed doi:10.1186/1475-2891-11-29

    • Crossref
    • Search Google Scholar
    • Export Citation
  • Hininger, I.A., Meyer-Wenger, A., Moser, U., Wright, A., Southon, S., Thurnham, D., . . . Roussel, A.M. (2001). No significant effects of lutein, lycopene or beta-carotene supplementation on biological markers of oxidative stress and LDL oxidizability in healthy adult subjects. Journal of the American College of Nutrition, 20, 232–238. PubMed doi:10.1080/07315724.2001.10719037

    • Crossref
    • Search Google Scholar
    • Export Citation
  • Jacob, K., Periago, M.J., Böhm, V., & Berruezo, G.R. (2008). Influence of lycopene and vitamin C from tomato juice on biomarkers of oxidative stress and inflammation. British Journal of Nutrition, 99, 137–146. PubMed doi:10.1017/S0007114507791894

    • Crossref
    • Search Google Scholar
    • Export Citation
  • Liu, C.C., Huang, C.C., Lin, W.T., Hsieh, C.C., Huang, S.Y., Lin, S.J., & Yang, S.C. (2005). Lycopene supplementation attenuated xanthine oxidase and myeloperoxidase activities in skeletal muscle tissues of rats after exhaustive exercise. British Journal of Nutrition, 94, 595–601. PubMed doi:10.1079/BJN20051541

    • Crossref
    • Search Google Scholar
    • Export Citation
  • Meléndez-Martínez, A.J., Mapelli-Brahm, P., Benítez-González, A., & Stinco, C.M. (2015). A comprehensive review on the colorless carotenoids phytoene and phytofluene. Archives of Biochemistry and Biophysics, 572, 188–200. doi:10.1016/j.abb.2015.01.003

    • Crossref
    • Search Google Scholar
    • Export Citation
  • Moran, N.E., Cichon, M.J., Riedl, K.M., Grainger, E.M., Schwartz, S.J., Novotny, J.A., . . . Clinton, S.K. (2015). Compartmental and noncompartmental modeling of 13C-lycopene absorption, isomerization, and distribution kinetics in healthy adults. American Journal of Clinical Nutrition, 102, 1436–1449. PubMed doi:10.3945/ajcn.114.103143

    • Crossref
    • Search Google Scholar
    • Export Citation
  • Moran, N.E., Novotny, J.A., Cichon, M.J., Riedl, K.M., Rogers, R.B., Grainger, E.M., . . . Clinton, S.K. (2016). Absorption and distribution kinetics of the 13C-labeled tomato carotenoid phytoene in healthy adults. Journal of Nutrition, 146, 368–376. PubMed doi:10.3945/jn.115.220525

    • Crossref
    • Search Google Scholar
    • Export Citation
  • Nieman, D.C., Gillitt, N.D., Sha, W., Meaney, M.P., John, C., Pappan, K.L., & Kinchen, J.M. (2015). Metabolomics-based analysis of banana and pear ingestion on exercise performance and recovery. Journal of Proteome Research, 14, 5367–5377. PubMed doi:10.1021/acs.jproteome.5b00909

    • Crossref
    • Search Google Scholar
    • Export Citation
  • Nieman, D.C., Shanely, R.A., Luo, B., Meaney, M.P., Dew, D.A., & Pappan, K.L. (2014). Metabolomics approach to assessing plasma 13- and 9-hydroxy-octadecadienoic acid and linoleic acid metabolite responses to 75-km cycling. American Journal of Physiology—Regulatory, Integrative and Comparative Physiology, 307, 68–74. PubMed doi:10.1152/ajpregu.00092.2014

    • Crossref
    • Search Google Scholar
    • Export Citation
  • Paetau, I., Khachik, F., Brown, E.D., Beecher, G.R., Kramer, T.R., Chittams, J., & Clevidence, B.A. (1998). Chronic ingestion of lycopene-rich tomato juice or lycopene supplements significantly increases plasma concentrations of lycopene and related tomato carotenoids in humans. American Journal of Clinical Nutrition, 68, 1187–1195. PubMed

    • Crossref
    • Search Google Scholar
    • Export Citation
  • Pellegrini, N., Riso, P., & Porrini, M. (2000). Tomato consumption does not affect the total antioxidant capacity of plasma. Nutrition, 16, 268–271. PubMed doi:10.1016/S0899-9007(99)00305-6

    • Crossref
    • Search Google Scholar
    • Export Citation
  • Porrini, M., & Riso, P. (2000). Lymphocyte lycopene concentration and DNA protection from oxidative damage is increased in women after a short period of tomato consumption. Journal of Nutrition, 130, 189–192. PubMed

    • Crossref
    • Search Google Scholar
    • Export Citation
  • Richelle, M., Bortlik, K., Liardet, S., Hager, C., Lambelet, P., Baur, M., . . . Offord, E.A. (2002). A food-based formulation provides lycopene with the same bioavailability to humans as that from tomato paste. Journal of Nutrition, 132, 404–408. PubMed

    • Crossref
    • Search Google Scholar
    • Export Citation
  • Riso, P., Pinder, A., Santangelo, A, & Porrini, M. (1999). Does tomato consumption effectively increase the resistance of lymphocyte DNA to oxidative damage? American Journal of Clinical Nutrition, 69, 712–718. PubMed

    • Crossref
    • Search Google Scholar
    • Export Citation
  • Samaras, A., Tsarouhas, K., Paschalidis, E., Giamouzis, G., Triposkiadis, F., Tsitsimpikou, C., . . . Kouretas, D. (2014). Effect of a special carbohydrate–protein bar and tomato juice supplementation on oxidative stress markers and vascular endothelial dynamics in ultra-marathon runners. Food and Chemical Toxicology, 69, 231–236. PubMed doi:10.1016/j.fct.2014.03.029

    • Crossref
    • Search Google Scholar
    • Export Citation
  • Sebastian, R.S., Enns, C.W., Goldman, J.D., Steinfeldt, L.C., Martin, C.L., & Moshfegh, A.J. (2016). Flavonoid values for USDA survey foods and beverages 2007–2010. Beltsville, MD. U.S. Department of Agriculture, Agricultural Research Service, Food Surveys Research Group. Retrieved from www.ars.usda.gov/nea/bhnrc/fsrg

    • Search Google Scholar
    • Export Citation
  • Shi, J., & Le Maguer, M. (2000). Lycopene in tomatoes: Chemical and physical properties affected by food processing. Critical Reviews in Biotechnology, 20, 293–334. PubMed doi:10.1080/07388550091144212

    • Crossref
    • Search Google Scholar
    • Export Citation
  • Sies, H., & Stahl, W. (1995). Vitamins E and C, beta-carotene, and other carotenoids as antioxidants. American Journal of Clinical Nutrition, 62(Suppl. 6), 1315S–1321S. PubMed

    • Crossref
    • Search Google Scholar
    • Export Citation
  • Silaste, M.L., Alfthan, G., Aro, A., Kesäniemi, Y.A., & Hörkkö, S. (2007). Tomato juice decreases LDL cholesterol levels and increases LDL resistance to oxidation. British Journal of Nutrition, 98, 1251–1258.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • Smith, L.L., Brunetz, M.H., Chenier, T.C., McCammon, M.R., Houmard, J.A., Franklin, M.E., & Israel, R.G. (1993). The effects of static and ballistic stretching on delayed onset muscle soreness and creatine kinase. Research Quarterly for Exercise and Sport, 64, 103–107. doi:10.1080/02701367.1993.10608784

    • Crossref
    • Search Google Scholar
    • Export Citation
  • Story, E.N., Kopec, R.E., Schwartz, S.J., & Harris, G.K. (2010). An update on the health effects of tomato lycopene. Annual Review of Food Science and Technology, 1, 189–210. PubMed doi:10.1146/annurev.food.102308.124120

    • Crossref
    • Search Google Scholar
    • Export Citation
  • Tsitsimpikou, C., Kioukia-Fougia, N., Tsarouhas, K., Stamatopoulos, P., Rentoukas, E., Koudounakos, A., . . . Jamurtas, A. (2013). Administration of tomato juice ameliorates lactate dehydrogenase and creatinine kinase responses to anaerobic training. Food and Chemical Toxicology, 61, 9–13. PubMed doi:10.1016/j.fct.2012.12.023

    • Crossref
    • Search Google Scholar
    • Export Citation
  • Tsitsimpikou, C., Tsarouhas, K., Kioukia-Fougia, N., Skondra, C., Fragkiadaki, P., Papalexis, P., . . . Rentoukas, E. (2014). Dietary supplementation with tomato-juice in patients with metabolic syndrome: A suggestion to alleviate detrimental clinical factors. Food and Chemical Toxicology, 74, 9–13. PubMed doi:10.1016/j.fct.2014.08.014

    • Crossref
    • Search Google Scholar
    • Export Citation
  • Tyssandier, V., Feillet-Coudray, C., Caris-Veyrat, C., Guilland, J.C., Coudray, C., Bureau, S., . . . Borel, P. (2004). Effect of tomato product consumption on the plasma status of antioxidant microconstituents and on the plasma total antioxidant capacity in healthy subjects. Journal of the American College of Nutrition, 23, 148–156. PubMed doi:10.1080/07315724.2004.10719355

    • Crossref
    • Search Google Scholar
    • Export Citation
  • Upritchard, J.E., Sutherland, W.H., & Mann, J.I. (2000). Effect of supplementation with tomato juice, vitamin E, and vitamin C on LDL oxidation and products of inflammatory activity in type 2 diabetes. Diabetes Care, 23, 733–738. PubMed doi:10.2337/diacare.23.6.733

    • Crossref
    • Search Google Scholar
    • Export Citation
  • U.S. Department of Agriculture. (2016). National nutrient database for standard reference, release 28, slightly revised May, 2016. Retrieved from https://ndb.nal.usda.gov/ndb/

    • Search Google Scholar
    • Export Citation
  • U.S. Department of Agriculture, Agricultural Research Service. (2014). Nutrient intakes from food and beverages: Mean amounts consumed per individual, by gender and age, what we eat in America, NHANES 2011–2012. Retrieved from www.ars.usda.gov/nea/bhnrc/fsrg

    • Search Google Scholar
    • Export Citation
  • Wang, X.D. (2012). Lycopene metabolism and its biological significance. American Journal of Clinical Nutrition, 96, 1214S–1222S. PubMed doi:10.3945/ajcn.111.032359

    • Crossref
    • Search Google Scholar
    • Export Citation
  • Wang, Y., Cui, R., Xiao, Y., Fang, J., & Xu, Q. (2015). Effect of carotene and lycopene on the risk of prostate cancer: A systematic review and dose-response meta-analysis of observational studies. PLoS ONE, 10, e0137427. PubMed doi:10.1371/journal.pone.0137427

    • Crossref
    • Search Google Scholar
    • Export Citation
  • Young, A.J., & Lowe, G.M. (2001). Antioxidant and prooxidant properties of carotenoids. Archives of Biochemistry and Biophysics, 385, 20–27. PubMed doi:10.1006/abbi.2000.2149

    • Crossref
    • Search Google Scholar
    • Export Citation
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