Abstract
This randomized study measured the influence of vitamin C (N=15) compared to placebo (N=13) supplementation on oxidative and salivary immunoglobulin A (sIgA) changes in runners competing in an ultramarathon race. Seven days prior to the race, subjects ingested in randomized, double-blind fashion three 500-mg tablets of vitamin C or placebo each day. On race day, blood and saliva samples were collected 1 h pre-race, after 32 km of running, and then again immediately post-race. During the race, runners received 1 l/h carbohydrate beverages (60 g/l) with vitamin C (150 mg/l) or without in a double-blinded fashion. The runners also ingested two to three carbohydrate gel packs per hour (25 g each). Subjects in both groups ran a mean of 69 km (range 48–80 km) in 9.8 h (range 5–12 h) and maintained an intensity of approximately 75% maximal heart rate (HRmax) throughout the ultramarathon race. Plasma ascorbic acid was higher in the vitamin C compared to placebo group pre-race, and increased significantly in the vitamin C group during the race [post-race, 3.21 (0.29) and 1.28 (0.12) μg/100 μl, respectively, P<0.001]. No significant group or interaction effects were measured for lipid hydroperoxide and F2-isoprostane, but both oxidative measures rose significantly during the ultramarathon race. Saliva volume, sIgA concentration, sIgA secretion and sIgA:saliva protein ratio all decreased significantly (P<0.001) during the race, but the pattern of change in all saliva measures did not differ significantly between groups. No significant correlations were found between post-race plasma vitamin C, oxidative, and saliva measures, except for a positive correlation between post-race serum cortisol and serum vitamin C (r=0.50, P=0.006). These data indicate that vitamin C supplementation in carbohydrate-fed runners does not serve as a countermeasure to oxidative and sIgA changes during or following a competitive ultramarathon race.
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References
Anderson R, Van Wyk H (1980) The effect of ascorbate ingestion on levels of salivary IgA in adult volunteers. Am J Clin Nutr 33:6–7
Anderson R, Oosthuizen R, Maritz R, Van Rensburg AJ (1980) The effects of increasing weekly doses of ascorbate on certain cellular and humoral immune functions in normal volunteers. Am J Clin Nutr 33:71–76
Ashton T, Young IS, Peters JR, Jones E, Jackson SK, Davies B, Rowlands CC (1999) Electron spin resonance spectroscopy, exercise, and oxidative stress: an ascorbic acid intervention study. J Appl Physiol 87:2032–2036
Bradford MM (1976) A rapid and sensitive method for the quantitation of microgram quantities protein utilizing the principle of protein-dye binding. Anal Biochem 72:248–254
Campbell JD, Cole M, Bunditrutavorn B, Vella AT (1999) Ascorbic acid is a potent inhibitor of various forms of T cell apoptosis. Cell Immunol 194:1–5
Chen CY, Huang YL, Lin TH (1998) Association between oxidative stress and cytokine production in nickel-treated rats. Arch Biochem Biophys 356:127–132
Cupps TR, Fauci, AS (1982) Corticosteroid mediated immunoregulation in man. Immunol Rev 65:133–155
Dill DB, Costill DL (1974) Calculation of percentage changes in volumes of blood, plasma, and red cells in dehydration. J Appl Physiol 37:247–248
Enwonwu CO, Sawiris P, Chanaud N (1995) Effect of marginal ascorbic acid deficiency on saliva level of cortisol in the guinea pig. Arch Oral Biol 40:737–742
Franci O, Amici A, Margarit R, Merendino N, Piccolella E (1996) Influence of thermal and dietary stress on immune response of rabbits. J Anim Sci 74:1523–1529
Gleeson M (2000) Mucosal immunity and respiratory illness in elite athletes. Int J Sports Sci 21 [Suppl. 1]:S33–S43
Gleeson M, Hall ST, McDonald WA, Flanagan AJ, Clancy RL (1999a) Salivary IgA subclasses and infection risk in elite swimmers. Immunol Cell Biol 77:351–355
Gleeson M, McDonald WA, Pyne DB, Cripps AW, Francis JL, Fricker PA, Clancy RL (1999b) Salivary IgA levels and infection risk in elite swimmers. Med Sci Sports Exerc 31:67–73
Gleeson M, McDonald WA, Pyne DB, Clancy RL, Cripps AW, Francis JL, Fricker PA (2000) Immune status and respiratory illness for elite swimmers during a 12-week training cycle. Int J Sports Med 21:302–307
Grimble RF (1997) Effect of antioxidative vitamins on immune function with clinical applications. Int J Vitam Nutr Res 67:312–320
Hughes DA (1999) Effects of dietary antioxidants on the immune function of middle-aged adults. Proc Nutr Soc 58:79–84
Jacob RA, Burri BJ (1996) Oxidative damage and defense. Am J Clin Nutr 63 [Suppl.]:985S–990S
Kodama M, Kodama T, Murakami M, Kodama M (1994) Vitamin C infusion treatment enhances cortisol production of the adrenal via the pituitary ACTH route. In Vivo 8:1079–1085
Krause R, Patruta S, Daxbock F, Fladerer P, Biegelmayer C, Wenisch C (2001) Effect of vitamin C on neutrophil function after high-intensity exercise. Eur J Clin Invest 31:258–263
Krzywkowski K, Petersen EW, Ostrowski K, Link-Amster H, Boza J, Halkjaer-Kristensen J, Pedersen BK (2001) The effect of glutamine and protein supplementation on exercise-induced decreases in salivary IgA. J Appl Physiol 91:832–838
Laney PH, Levy JA, Kipp DE (1990) Plasma cortisol and adrenal ascorbic acid levels after ACTH treatment with a high intake of ascorbic acid in the guinea pig. Ann Nutr Metab 34:85–92
Levine M, Wang Y, Sebastian P, Morrow J (2001) A new recommended dietary allowance of vitamin C for healthy young women. Proc Natl Acad Sci USA 19(17):9842–9846
Mackinnon L (1996) Immunoglobulin antibody and exercise. Exerc Immunol Rev 2:1–35
Mackinnon LT, Hooper S (1994) Mucosal (secretory) immune system response to exercise of varying intensity and during overtraining. Int J Sports Med 15 [Suppl. 3]:S179–S183
Mackinnon L, Chick TW, Van As A, Toamasi TB (1987) The effect of exercise on secretory and natural immunity. Adv Exp Med Biol 216A:869–876
McDowell SL, Chaloa K, Housh TJ, Tharp GD, Johnson GO (1991) The effect of exercise intensity and duration on salivary immunoglobulin A. Eur J Appl Physiol 63:108–111
Morrow JD (2000)The isoprostanes: their quantification as an index of oxidant stress status in vivo. Dru Metab Rev 32:377–385
Müns G, Liesen H, Riedel H, Bergmann K-Ch (1989) Einfluß von langstreckenlauf auf den IgA-gehalt in nasensekret und speichel. Deutsch Z Sportmed 40:63–65
Mylonas C, Kouretas D (1999) Lipid peroxidation and tissue damage. In Vivo 13:295–309
Nehlsen-Cannarella SL, Fagoaga OR, Nieman DC, Henson DA, Butterworth DE, Bailey E, Warren BJ, Davis JM (1997) Carbohydrate and the cytokine response to 2.5 hours of running. J Appl Physiol 82:1662–1667
Nehlsen-Cannarella SL, Nieman DC, Fagoaga OR, Kelln WJ, Henson DA, Shannon M, Davis JM (2000) Saliva immunoglobulins in elite women rowers. Eur J Appl Physiol 81:222–228
Nieman DC (2000) Carbohydrates and the immune response to prolonged exertion. In: Nieman DC, Pedersen BK (eds) Nutrition and exercise immunology. CRC, Boca Raton, Fla., pp 25–42
Nieman DC, Nehlsen-Cannarella SL (1991) The effect of acute and chronic exercise on immunoglobulins. Sports Med 11(3):183–201
Nieman DC, Henson DA, Butterworth DE, Warren BJ, Davis JM, Fagoaga OR, Nehlsen-Cannarella SL (1997) Vitamin C supplementation does not alter the immune response to 2.5 hours of running. Int J Sport Nutr 7(3):173–184
Nieman DC, Nehlsen-Cannarella SL, Fagoaga OR, Henson DA, Utter A, Davis JM, Williams F, Butterworth DE (1998) Influence of mode and carbohydrate on the cytokine response to heavy exertion. Med Sci Sports Exerc 30:671–678
Nieman DC, Peters EM, Henson DA, Nevines EI, Thompson MM (2000) Influence of vitamin C supplementation on cytokine changes following an ultramarathon. J Interferon Cytokine Res 20:1029–1035
Nieman DC, Henson DA, Fagoaga OR, Utter AC, Vinci DM, Davis M, Nehlsen-Cannarella SL (2001a) Changes in salivary IgA following a competitive marathon race. Int J Sports Med 22:1–7
Nieman DC, Henson DA, Smith LL, Utter AC, Vinci DM, Davis JM, Kaminsky DE, Shute M. (2001b) Cytokine changes after a marathon race. J Appl Physiol 91:109–114
Nieman DC, Henson DA, Mcanulty SR, McAnulty L, Swick NS, Utter AC, Vinci DM, Opiela SJ, Morrow JD (2002) Influence of vitamin C supplementation on oxidative and immune changes following an ultramarathon. J Appl Physiol 92:1970–1977
Niess AM, Sommer M, Schneider M, Angres C, Tschositsch K, Golly IC, Battenfeld N, Northoff H, Biesalski HK, Dickhuth HH, Fehrenbach E (2000) Physical exercise-induced expression of inducible nitric oxide synthase and heme oxygenase-1 in human leukocytes: effects of RRR-α-tocopherol supplementation. Antiox Redox Signal 2:113–126
Peters EM, Anderson R, Theron AJ (2001) Attenuation of the increase in circulating cortisol and enhancement of the acute phase protein response in vitamin C supplemented ultramarathon runners. Int J Sports Med 22:120–126
Petersen EW, Ostrowski K, Ibfelt T, Richelle M, Offord E, Halkjaer-Kristensen J, Pedersen BK (2001) Effect of vitamin supplementation on cytokine response and on muscle damage after strenuous exercise. Am J Physiol 280:C1570–C1575
Piercy RJ, Hinchcliff KW, DiSilvestro RA, Reinhart GA, Baskin CR, Hayek MG, Burr JR, Swenson RA (2000) Effect of dietary supplements containing antioxidants on attenuation of muscle damage in exercising sled dogs. Am J Vet Res 61:1438–1445
Redmann A, Mobius K, Hiller HH, Oelkers W, Bahr V (1995) Ascorbate depletion prevents Aldosterone stimulation by sodium deficiency in the guinea pig. Eur J Endocrinol 133:499–506
Rokitzki L, Logemann E, Sagredos AN, Murphy M, Wezel-Roth W, Keul J (1994) Lipid peroxidation and antioxidative vitamins under extreme endurance stress. Acta Physiol Scand 151:149–158
Sanchez-Quesada JL, Jorba O, Payes A, Otal C, Serra-Grima R, Gonzalez-Sastre F, Ordonez-Llanos J (1998) Ascorbic acid inhibits the increase in low-density lipoprotein (LDL) susceptibility to oxidation and the proportion of electronegative LDL induced by intense aerobic exercise. Coron Art Dis 9:249–255
Sen CK, Roy S (2001) Antioxidant regulation of cell adhesion. Med Sci Sports Exerc 33:377–381
Steerenberg PA, van Asperen IA, van Nieuw Amerongen A, Biewenga A, Mol D, Medema GJ (1997) Salivary levels of immunoglobulin A in triathletes. Eur J Oral Sci 105:305–309
Tanaka M, Muto N, Gohda E, Yamamoto I (1994) Enhancement by ascorbic acid 2-glucoside or repeated additions of ascorbate of mitogen-induced IgM and IgG productions by human peripheral blood lymphocytes. Jpn J Pharmacol 66(4):451–456
Thompson D, Williams C, Kingsley M, Nicholas CW, Lakomy HKA, McArdle F, Jackson MJ (2001) Muscle soreness and damage parameters after prolonged intermittent shuttle-running following acute vitamin C supplementation. Int J Sports Med 22:68–75
Tomasi TB, Trudeau FB, Czerwinski D, Erredge S (1982) Immune parameters in athletes before and after strenuous exercise. J Clin Immunol 2:173–178
Vider J, Lehtmaa J, Kullisaar T, Vihalemm T, Zilmer K, Kairane C, Landor A, Karu T, Zilmer M (2001) Acute immune response in respect to exercise-induced oxidative stress. Pathophysiology 7:263–270
White A, Estrada M, Walker K, Wisnia P, Filgueira G, Valdes F, Araneda O, Behn C, Martinez R (2001) Role of exercise and ascorbate on plasma antioxidant capacity in thoroughbred race horses. Comp Biochem Physiol A Mol Integr Physiol 128:99–104
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This research was supported by a grant from Gatorade Sports Science Institute and by NIH grants GM 15431, CA 77839, DK 48831, and DK 26657. J.D. Morrow is the recipient of a Burroughs Wellcome Clinical Scientist Award in Translational Research.
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Palmer, F.M., Nieman, D.C., Henson, D.A. et al. Influence of vitamin C supplementation on oxidative and salivary IgA changes following an ultramarathon. Eur J Appl Physiol 89, 100–107 (2003). https://doi.org/10.1007/s00421-002-0756-4
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DOI: https://doi.org/10.1007/s00421-002-0756-4