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Interaction between vitamins C and E affects their tissue concentrations, growth, lipid oxidation, and deficiency symptoms in yellow perch (Perca flavescens)

Published online by Cambridge University Press:  09 March 2007

Kyeong-Jun Lee  and
Konrad Dabrowski
Kyeong-Jun Lee
Affiliation:
School of Natural Resources, The Ohio State University, Columbus, OH 43210, USA
Konrad Dabrowski*
Affiliation:
School of Natural Resources, The Ohio State University, Columbus, OH 43210, USA
*
*Corresponding Author: Dr Konrad Dabrowski, fax +1 614 292 7432, email [email protected]
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Abstract

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We have conducted studies with juvenile yellow perch (Perca flavescens) over a period of 20 weeks to address the question of the interaction between water- and lipid-soluble antioxidant vitamins. Fish (2·25±0·14 g) were divided into twelve groups, and triplicate groups were fed one of four casein-based, semi-purified diets formulated to contain low or high vitamin E levels of either 5 or 160 mg/kg without or with vitamin C supplementation (250 mg/kg). Diets were designated as −C−E, −C+E, +C−E, or +C+E, respectively. The fish fed the +C+E diet showed significantly higher weight gain, feed intake, and feed efficiency than the groups fed vitamin C-deficient diets. Total ascorbate concentrations of liver were significantly higher in fish fed vitamin C-supplemented diets than in fish fed the vitamin C-deficient diet after 16 and 20 weeks. The liver α-tocopherol concentrations were increased by supplemental vitamin C in vitamin E-deficient dietary groups which indicates a sparing or regenerating effect of vitamin C on vitamin E. Fish fed vitamin C-deficient diets (−C−E and −C+E) exhibited severe deficiency symptoms, such as scoliosis, lens cataracts, anorexia, and haemorrhages. The cumulative mortality was significantly higher in the −C−E groups. The thiobarbituric acid-reactive substances value was significantly higher in blood plasma of fish fed a diet unsupplemented with both vitamins. The findings in the present study with yellow perch support the hypothesis that vitamin C regenerates and/or spares vitamin E in vivo.

Keywords

Yellow perchVitamin CVitamin EThiobarbituric acid-reactive substancesDeficiency symptoms
Type
Research Article
Information
British Journal of Nutrition , Volume 89 , Issue 5 , May 2003 , pp. 589 - 596
Copyright
Copyright © The Nutrition Society 2003

References

Association of Official Analytical Chemists (1995) Official Methods of Analysis, 16th ed, Arlington, VA: AOAC.Google Scholar
Bendich, A, D'Aploito, P, Gabriel, E & Machlin, LK (1984) Interaction of dietary vitamin E on guinea pig immune responses to mitogens. Journal of Nutrition 114 1588–1593.CrossRefGoogle ScholarPubMed
Brown, PB, Dabrowski, K & Garling, DL (1996) Nutrition and feeding of yellow perch (Perca flavescens). Journal of Applied Ichthyology 12 171–174.CrossRefGoogle Scholar
Buettner, GR (1993) The pecking order of free radicals and antioxidants: lipid peroxidation, α-tocopherol, and ascorbate. Archives of Biochemistry and Biophysics 300 535–543.CrossRefGoogle ScholarPubMed
Burton, GW, Joyce, A & Ingold, KU (1983) Is vitamin E the only lipid-soluble, chain-breaking antioxidant in human blood plasma and erythrocyte in human blood plasma and erythrocyte membranes? Archives of Biochemistry and Biophysics 221 281–290.CrossRefGoogle ScholarPubMed
Burton, GW, Wronska, U, Stone, L, Foster, DO & Ingold, KU (1990) Biokinetics of dietary RRR-α-tocopherol in the male guinea pig at three dietary levels of vitamin C and two levels of vitamin E. Evidence that vitamin C does not "spare" vitamin E in vivo. Lipids 25 199–210.CrossRefGoogle Scholar
Chan, AC (1993) Partners in defense, vitamin E and vitamin C. Canadian Journal of Physiology and Pharmacology 71 725–731.CrossRefGoogle ScholarPubMed
Chen, LH (1981) An increase in vitamin E requirement induced by high supplementation of vitamin C in rats. American Journal of Clinical Nutrition 34 1036–1041.CrossRefGoogle ScholarPubMed
Collins, BK, Collier, LL & Collins, JS (1993) Retinal and lenticular lesions in vitamin-C-deficient juvenile red drum, Sciaenops ocellatus (L.). Journal of Fish Diseases 16 229–237.CrossRefGoogle Scholar
Cort, WM, Vicente, TS, Waysek, EH & Williams, BD (1983) Vitamin E content of feedstuffs determined by high performance liquid chromatographic fluorescence. Journal of Agricultural and Food Chemistry 31 1330–1333.CrossRefGoogle Scholar
Dabrowski, K (1990) Gulonolactone oxidase is missing in teleost fish–the direct spectrophotometric assay. Biological Chemistry Hoppe-Seyler 371 207–214.CrossRefGoogle ScholarPubMed
Dabrowski, K (1994) Primitive Actinopterigian fishes can synthesize ascorbic acid. Experientia 51 745–748.CrossRefGoogle Scholar
Dabrowski, K (2001) Ascorbic Acid in Aquatic Organisms–Status and Perspectives, [Dabrowski, K, editor]. Boca Raton, FL: CRC Press Inc.Google Scholar
Dabrowski, K & Hinterleitner, S (1989) Simultaneous analysis of ascorbic acid, dehydroascorbic acid and ascorbic sulphate in biological materials. Analyst 114 83–87.CrossRefGoogle ScholarPubMed
Dabrowski, K & Wieser, W (1990) Effect of species differences and dietary vitamin C on the concentration of ascorbate- and acid-soluble thiol in fish eye. Experimental Eye Research 51 637–643.CrossRefGoogle ScholarPubMed
Dabrowski, K, El-fiky, N, Kock, G & Wieser, W (1990) Requirement and utilization of ascorbic acid and ascorbic sulfate in juvenile rainbow trout. Aquaculture 91 317–337.CrossRefGoogle Scholar
Dabrowski, K, Moreau, R & El-saidy, D (1996) Ontogenetic sensitivity of channel catfish to ascorbic acid deficiency. Journal of Aquatic Animal Health 8 22–27.2.3.CO;2>CrossRefGoogle Scholar
de Zwart, LL, Meerman, JHN, Commandeur, JNM & Vermeulen, NPE (1999) Biomarkers of free radical damage: applications in experimental animals and in humans. Free Radical Biology and Medicine 26 202–226.CrossRefGoogle ScholarPubMed
Fournier, V, Gouillou-Coustans, MF & Kaushik, SJ (2000) Hepatic ascorbic acid saturation is the most stringent response criterion for determining the vitamin C requirement of juvenile European sea bass (Dicentrarchus labrax). Journal of Nutrition 130 617–620.CrossRefGoogle ScholarPubMed
Fracalossi, DM, Allen, ME, Nichols, DK & Oftedal, OT (1998) Oscars, Astronotus ocellatus, have a dietary requirement for vitamin C. Journal of Nutrition 128 1745–1751.CrossRefGoogle ScholarPubMed
Frei, B, Stocker, R, England, L & Ames, BN (1990) Ascorbate: the most effective antioxidant in human blood plasma. Advances in Experimental Medicine and Biology 264 155–163.CrossRefGoogle ScholarPubMed
Frischknecht, R, Wahli, T & Meier, W (1994) Comparison of pathological changes due to deficiency of vitamin C, vitamin E and combinations of vitamins C and E in rainbow trout, Oncorhynchus mykiss (Walbaum). Journal of Fish Diseases 17 31–45.CrossRefGoogle Scholar
Gatlin, DM, Poe, WE, Wilson, RP, Ainsworth, AJ & Bowser, PR (1986) Effects of stocking density and vitamin C status on vitamin E-adequate and vitamin E-deficient fingerling channel catfish. Aquaculture 56 187–195.CrossRefGoogle Scholar
Halver, JE (1988) The vitamins. In Fish Nutrition, 2nd ed., [Halver, JE, editor]. San Diego, CA: Academic Press, Inc.Google Scholar
Halver, JE, Ashley, LM & Smith, RR (1969) Ascorbic acid requirements of coho salmon and rainbow trout. Transactions of American Fisheries Society 90 762–771.CrossRefGoogle Scholar
Halver, JE, Smith, RR, Tolbert, BM & Baker, EM (1975) Utilization of ascorbic acid in fish. Annals of The New York Academy of Sciences 258 81–102.CrossRefGoogle ScholarPubMed
Hamilton, IMJ, Gilmore, WS, Benzie, IF, Mulholland, CW & Strain, JJ (2000) Interaction between vitamins C and E in human subjects. British Journal of Nutrition 84 261–267.CrossRefGoogle Scholar
Hamre, K, Waagbo, R, Berge, RK & Lie, O (1997) Vitamin C and E interact in juvenile Atlantic salmon. Free Radical Biology and Medicine 22 137–149.CrossRefGoogle Scholar
Harats, D, Ben-Naim, M, Dabach, Y, Hollander, G, Havivi, E, Stein, O & Stein, Y (1990) Effect of vitamin C and E supplementation on susceptibility of plasma lipoproteins to peroxidant induced by acute smoking. Atherosclerosis 85 47–54.CrossRefGoogle Scholar
Hardie, LJ, Fletcher, TC & Secombes, CJ (1991) The effect of dietary vitamin C on the immune response of the Atlantic salmon. Aquaculture 95 201–214.CrossRefGoogle Scholar
Hilton, JW, Cho, CY & Slinger, SJ (1977) Evaluation of ascorbic acid status of rainbow trout (Salmo gairdneri). Journal of the Fisheries Research Board of Canada 34 2207–2210.CrossRefGoogle Scholar
Ho, CT & Chan, AC (1992) Regeneration of vitamin E in rat polymorphonuclear leukocytes. FEBS Letters 306 269–272.CrossRefGoogle Scholar
Igarashi, O, Yonekawa, Y & Fujiyama-Fujihara, Y (1991) Synergistic action of vitamin E and vitamin C in vivo using a new mutant of Wistar-strain rats, ODS, unable to synthesize vitamin C. Journal of Nutritional Science and Vitaminology 37 359–369.CrossRefGoogle ScholarPubMed
Jacob, RA, Kutnink, MA, Csallany, S, Daroszewska, M & Burton, GW (1996) Vitamin C nutriture has little short-term effect on vitamin E concentrations in healthy women. Journal of Nutrition 126 2268–2277.CrossRefGoogle ScholarPubMed
Jacob, RA, Ottadovec, CL & Russell, RM (1988) Vitamin C status and nutrient interactions in a healthy elderly population. American Journal of Clinical Nutrition 48 1436–1442.CrossRefGoogle Scholar
Lee, K-J, Kim, K-W & Bai, SC (1998) Effects of different dietary levels of L-ascorbic acid on growth and tissue vitamin C concentration in juvenile Korean rockfish, Sebastes schlegeli (Hilgendorf). Aquaculture Research 29 237–244.Google Scholar
Lim, C & Lovell, RT (1978) Pathology of vitamin C deficiency syndrome in channel catfish Ictalurus punctatus. Journal of Nutrition 108 1137–1146.CrossRefGoogle ScholarPubMed
Liu, J-F & Lee, Y-W (1998) Vitamin C supplementation restores the impaired vitamin E status of guinea pigs fed oxidized frying oil. Journal of Nutrition 128 116–122.CrossRefGoogle ScholarPubMed
McCay, PB (1985) Vitamin E: Interactions with free radicals and ascorbate. Annual Review of Nutrition 5 323–340.CrossRefGoogle ScholarPubMed
Moreau, R & Dabrowski, K (1996) Feeding stimulants in semipurified diets for juvenile lake sturgeon, Acipenser fulvescens Rafinesque. Aquaculture Research 27 953–957.Google Scholar
Moreau, R & Dabrowski, K (1998) Body pool and synthesis of ascorbic acid in adult sea lamprey (Petromyzon marinus): An agnathan fish with gulonolactone oxidase activity. Proceedings of the National Academy of Sciences, USA 95 10279–10282.CrossRefGoogle ScholarPubMed
Moreau, R, Dabrowski, K, Czesny, S & Cihla, F (1999) Vitamin C- vitamin E interaction in juvenile lake sturgeon (Acipenser fulvescens R.), a fish able to synthesize ascorbic acid. Journal of Applied Ichthyology 15 250–257.CrossRefGoogle Scholar
Mukai, K, Nishimura, M & Kikuchi, S (1991) Stopped-flow investigation of the reaction of vitamin C with tocopheroxyl radical in aqueous Triton X-100 micellar solutions – The structure-activity relationship of the regeneration reaction of tocopherol by vitamin C. Journal of Biological Chemistry 266 274–278.CrossRefGoogle ScholarPubMed
Mulholland, CW, Strain, JJ & Trinick, TR (1996) Serum antioxidant potential, and lipoprotein oxidation in female smokers following vitamin C supplementation. International Journal of Food Sciences and Nutrition 47 227–231.CrossRefGoogle ScholarPubMed
Naidoo, D & Lux, O (1998) The effect of vitamin C and E supplementation on lipid and urate oxidation products in plasma. Nutrition Research 18 953–961.CrossRefGoogle Scholar
National Research Council (1993) Nutritional Requirements of Fish. Washington, DC: National Academy Press.Google Scholar
Niki, E, Tsuchiya, J, Tanimura, R & Kamiya, T (1982) Regeneration of vitamin E from radical by glutathione and vitamin C. Chemistry Letters 6 789–792.CrossRefGoogle Scholar
Nyyssonen, K, Poulsen, HE, Hayn, M, Agerbo, P, Porkkala-Sarataho, E, Kaikkonen, J, Salonen, R & Salonen, JT (1997) Effect of supplementation of smoking men with plain or slow-release ascorbic acid on lipoprotein oxidation. European Journal of Clinical Nutrition 51 154–163.CrossRefGoogle ScholarPubMed
Packer, JE, Slater, TF & Willson, RL (1979) Direct observation of a free radical interaction between vitamin E and vitamin C. Nature 278 737–738.CrossRefGoogle ScholarPubMed
Poston, HA (1967) Effect of dietary L-ascorbic acid on immature brook trout. Fisheries Research Bulletin 31 45–51.Google Scholar
Sakuma, N, Iwata, S, Hibino, T, Tamai, N, Sasai, K, Yoshimata, T, Kamiya, Y, Kawagichi, M & Fuginami, T (1997) Effects of vitamin C and vitamin E on plasma levels of lipid hydroperoxides and thiobarbituric acid reactive substance in humans. Current Therapeutic Research – Clinical and Experimental 58 317–322.CrossRefGoogle Scholar
Shiau, S-Y & Hsu, T-S (1999) Quantification of vitamin C requirement for juvenile hybrid tilapia, Oreochromis niloticus × Oreochromis aureus, with L-ascorbyl-2-monophosphate-Na and L-ascorbyl-2-monophosphate-Mg. Aquaculture 175 317–326.CrossRefGoogle Scholar
Stickney, RR (ed) (1993) Yellow perch. In Culture of Nonsalmonid Freshwater Fishes, 2nd ed., Boca Raton, FL: CRC Press, Inc.Google Scholar
Stoyanovsky, DA, Goldman, R, Darrow, RM, Organisciak, DT & Kagan, VE (1995) Endogenous ascorbate regenerates vitamin E in the retina directly and in combination with exogenous dihydrolipoic acid. Current Eye Research 14 181–189.CrossRefGoogle ScholarPubMed
Tanaka, K, Hashimoto, T, Tokumaru, S, Iguchi, H & Kojo, S (1997) Interactions between vitamin C and vitamin E are observed in tissues of inherently scorbutic rats. Journal of Nutrition 127 2060–2064.CrossRefGoogle ScholarPubMed
Tappel, AL (1968) Will antioxidant nutrients slow aging processes? Geriatrics 23 97–105.Google ScholarPubMed
Tatum, VL, Changchit, C & Chow, CK (1990) Measurement of malondialdehyde by high performance liquid chromatography with fluorescence detection. Lipids 25 226–229.CrossRefGoogle Scholar
Twibell, RG & Brown, PB (2000) Dietary choline requirement of juvenile yellow perch (Perca flavescens). Journal of Nutrition 130 95–99.CrossRefGoogle ScholarPubMed
Twibell, RG, Wilson, KA & Brown, PB (2000) Dietary sulfur amino acid requirement of juvenile yellow perch fed the maximum cystine replacement value for methionine. Journal of Nutrition 130 612–616.CrossRefGoogle ScholarPubMed
Wahli, T, Verlhac, V, Gabaudan, J, Schuep, W & Meler, W (1998) Influence of combined vitamins C and E on non-specific immunity and disease resistance of rainbow trout, Oncorhynchus mykiss (Walbaum). Journal of Fish Diseases 21 127–137.CrossRefGoogle Scholar
Wantanowicz, M, Panczenko-Kresowska, B & Ziemlanski, S (1984) The effect of α-tocopherol and ascorbic acid on the serum lipid peroxide level in elderly people. Annals of Nutrition and Metabolism 28 186–191.CrossRefGoogle Scholar
Zaspel, BJ & Csallany, AS (1983) Determination of α-tocopherol in tissues and plasma by high-performance liquid chromatography. Analytical Biochemistry 130 145–150.CrossRefGoogle ScholarPubMed