Hostname: page-component-cd9895bd7-gxg78 Total loading time: 0 Render date: 2024-12-27T07:01:16.128Z Has data issue: false hasContentIssue false

Modulation of human T-lymphocyte functions by the consumption of carotenoid-rich vegetables

Published online by Cambridge University Press:  09 March 2007

Bernhard Watzl*
Affiliation:
Institute of Nutritional Physiology, Federal Research Centre for Nutrition, Haid-und-Neu-Str. 9, 76131 Karlsruhe, Germany
Achim Bub
Affiliation:
Institute of Nutritional Physiology, Federal Research Centre for Nutrition, Haid-und-Neu-Str. 9, 76131 Karlsruhe, Germany
Birgit R. Brandstetter
Affiliation:
Department of Epidemiology, German Cancer Research Centre, Im Neuenheimer Feld 280, 69120 Heidelberg, Germany
Gerhard Rechkemmer
Affiliation:
Institute of Nutritional Physiology, Federal Research Centre for Nutrition, Haid-und-Neu-Str. 9, 76131 Karlsruhe, Germany
*
*Corresponding author: Dr Bernhard Watzl, fax +49 721 6625 404, email bernhard.watzl@bfe.uni-karlsruhe.de
Rights & Permissions [Opens in a new window]

Abstract

Core share and HTML view are not available for this content. However, as you have access to this content, a full PDF is available via the ‘Save PDF’ action button.

A human intervention study was conducted to determine the effect of the consumption of carotenoid-rich vegetables on the immune system. Subjects, (twenty-three men), who were non-smokers, were not restricted in their daily diet, except that they had to abstain from fruit and vegetables high in carotenoids throughout the whole study period. The study was divided into four periods, each lasting 2 weeks: weeks 1–2: low-carotenoid period; throughout weeks 3–8: daily consumption of 330 ml tomato juice (40 mg lycopene/d, 1·5 mg β-carotene/d) (weeks 3–4), 330 ml carrot juice (21·6 mg β-carotene/d, 15·7 mg α-carotene/d, 0·5 mg lutein/d) (weeks 5–6), 10 g dried spinach powder (11·3 mg lutein/d, 3·1 mg β-carotene/d) (weeks 7–8). Blood was collected weekly from subjects after a 12 h fast. T-lymphocyte functions were assessed by measuring proliferation and secretion of immunoreactive cytokines. The consumption of a low-carotenoid diet resulted in a significantly reduced proliferation of peripheral blood mononuclear cells (PBMC) cultured with concanavalin A. After 2 weeks of tomato juice consumption and until the end of the intervention period lymphocyte proliferation was not significantly changed compared with proliferation at the end of the depletion period. Secretion of cytokines by T-helper-1-like lymphocytes (interleukin (IL)-2) and by T-helper-2-like lymphocytes (IL-4) was influenced by the dietary intervention. IL-2 and IL-4 secretion values were significantly suppressed after the low-carotenoid diet (P <0·001 and P < 0·05 respectively compared with baseline). Tomato juice consumption significantly enhanced IL-2 (P < 0·001) and IL-4 secretion (P < 0·05) compared with the end of depletion period. After carrot juice and spinach powder consumption the cytokine secretion capacity of PBMC was not significantly different from that at the end of the depletion period. In conclusion, the results of the present study indicate that a low-carotenoid diet reduces T-lymphocyte functions and addition of tomato juice restores these functions. This modulation could not be explained by changes in the plasma carotenoid concentrations. The active constituents in tomato juice as well as the biological significance of this immunomodulation remain to be determined.

Type
Research Article
Copyright
Copyright © The Nutrition Society 1999

References

Abdel-Fattah, G, Watzl, B, Huang, DS & Watson, RR (1993) Beta-carotene in vitro stimulates tumor necrosis factor alpha and interleukin-1 alpha secretion by human peripheral blood mononuclear cells. Nutrition Research 13, 863871.CrossRefGoogle Scholar
Bendich, A (1989) Carotenoids and the immune response. Journal of Nutrition 119, 112115.CrossRefGoogle ScholarPubMed
Bendich, A (1991) Beta-carotene and the immune response. Proceedings of the Nutrition Society 50, 263274.CrossRefGoogle ScholarPubMed
Bendich, A (1996) Antioxidant vitamins and human immune responses. Vitamins and Hormones 52, 3562.CrossRefGoogle ScholarPubMed
Block, G, Patterson, B & Subar, A (1992) Fruit, vegetables, and cancer prevention: a review of the epidemiological evidence. Nutrition and Cancer 18, 129.CrossRefGoogle ScholarPubMed
Boeing, H, Bohlscheid-Thomas, S, Voss, S, Schneeweiss, S & Wahrendorf, J (1997) The relative validity of vitamin intakes derived from a food frequency questionnaire compared to 24-hour recalls and biological measurements: results from the EPIC pilot study in Germany. European Prospective Investigation into Cancer and Nutrition. International Journal of Epidemiology 26, Suppl. 1, S82–S90.CrossRefGoogle ScholarPubMed
Bone, RA, Landrum, JT, Friedes, LM, Gomez, CM, Kilburn, MD, Menendez, E, Vidal, I & Wang, W (1997) Distribution of lutein and zeaxanthin stereoisomers in the human retina. Experimental Eye Research 64, 211218.CrossRefGoogle ScholarPubMed
Bundesinstitut für gesundheitlichen Verbraucherschutz and Veterinärmedizin (1994) German Food Code and Nutrition Data Base Version II.2. Berlin: Nutri-Science.Google Scholar
Burri, BJ (1997) Beta-carotene and human health: a review of current research. Nutrition Research 17, 547580.CrossRefGoogle Scholar
Chew, BP, Wong, MW & Wong, TS (1996) Effects of lutein from marigold extract on immunity and growth of mammary tumors in mice. Anticancer Research 16, 36893694.Google ScholarPubMed
Clevidence, BA, Khachik, F, Brown, ED, Nair, PP, Wiley, ER, Prior, RL, Cao, G, Morel, DW, Stone, W, Gross, M & Kramer, T (1997) Human consumption of carotenoid-rich vegetables. In Antioxidant Methodology: in Vivo and in Vitro Concepts, pp. 5362 [Aruoma, OI and Cuppett, SL, editors]. Champaign, IL: AOCS Press.Google Scholar
Daudu, PA, Kelly, DS, Taylor, PC, Burri, BJ & Wu, MM (1994) Effect of a low beta-carotene diet on the immune functions of adult women. American Journal of Clinical Nutrition 60, 969972.CrossRefGoogle ScholarPubMed
Fotouhi, N, Meydani, M, Santos, MS, Meydani, SM, Hennekens, CH & Gaziano, JM (1996) Carotenoid and tocopherol concentrations in plasma, peripheral blood mononuclear cells, and red blood cells after long-term β-carotene supplementation in men. American Journal of Clinical Nutrition 63, 553558.CrossRefGoogle ScholarPubMed
Gardner, EM, Bernstein, ED, Dorfman, M, Abrutyn, E & Murasko, DM (1997) The age-associated decline in immune function of healthy individuals is not related to changes in plasma concentrations of β-carotene, retinol, α-tocopherol or zinc. Mechanisms of Aging and Development 94, 5569.CrossRefGoogle ScholarPubMed
Gerster, H (1997) The potential role of lycopene for human health. Journal of the American College of Nutrition 16, 109126.CrossRefGoogle ScholarPubMed
Hughes, DA, Wright, AJA, Finglas, PM, Peerless, ACJ, Bailey, AL, Astley, SB, Pinder, AC & Southon, S (1997 a) The effect of beta-carotene supplementation on the immune function of blood monocytes from healthy male nonsmokers. Journal of Laboratory and Clinical Medicine 129, 309317.CrossRefGoogle ScholarPubMed
Hughes, DA, Wright, AJA, Finglas, PM, Peerless, ACJ, Bailey, AL, Astley, SB, Pinder, AC & Southon, S (1997 b) Comparison of effects of beta-carotene and lycopene supplementation on the expression of functionally associated molecules on human monocytes. Biochemical Society Transactions 25, 206S.CrossRefGoogle ScholarPubMed
Iyonouchi, H, Sun, S, Mizokami, M & Gross, MD (1996) Effect of various carotenoids on cloned, effector-stage T-helper cell activity. Nutrition and Cancer 26, 313324.CrossRefGoogle Scholar
Kazi, N, Radvany, R, Oldham, T, Keshavarzian, A, Frommel, TO, Libertin, C & Mobarhan, S (1997) Immunomodulatory effect of beta-carotene on T lymphocyte subsets in patients with resected colonic polyps and cancer. Nutrition and Cancer 28, 140145.CrossRefGoogle Scholar
Key, TJA, Thorogood, M, Appleby, PN & Burr, ML (1996) Dietary habits and mortality in 11 000 vegetarians and health conscious people: results of a 17 year follow up. British Medical Journal 313, 775779.CrossRefGoogle ScholarPubMed
Kramer, TR & Burri, BJ (1997) Modulated mitogenic proliferative responsiveness of lymphocytes in whole-blood cultures after a low-carotene diet and mixed-carotenoid supplementation in women. American Journal of Clinical Nutrition 65, 871875.CrossRefGoogle ScholarPubMed
Mangels, AR, Holden, JM, Beecher, GR, Forman, MR & Lanza, E (1993) Carotenoid content of fruits and vegetables: an evaluation of analytic data. Journal of the American Dietetic Association 93, 284296.CrossRefGoogle ScholarPubMed
Mayne, ST (1996) Beta-carotene, carotenoids, and disease prevention in humans. FASEB Journal 10, 690701.CrossRefGoogle ScholarPubMed
Meydani, SN, Santos, MS, Ribaya-Mercado, JD, Leka, L, Han, SN & Russell, RM (1995 a) Effect of β-carotene on the immune response of elderly women. FASEB Journal 9, A170 Abstr.Google Scholar
Meydani, SN, Wu, D, Santos, MS & Hayek, MG (1995 b) Antioxidants and immune response in aged persons: overview of present evidence. American Journal of Clinical Nutrition 62, 1462S1476S.CrossRefGoogle ScholarPubMed
Moriguchi, S, Okishima, N, Sumida, S, Okamura, K, Tatsuya, D & Kishino, Y (1996) Beta-carotene supplementation enhances lymphocyte proliferation with mitogens in human peripheral blood lymphocytes. Nutrition Research 16, 211218.CrossRefGoogle Scholar
Mosmann, TR & Sad, S (1996) The expanding universe of T-cell subsets: Th1, Th2 and more. Immunology Today 17, 138146.CrossRefGoogle ScholarPubMed
Müller, H, Bub, A, Watzl, B & Rechkemmer, G (1999) Plasma concentrations of carotenoids in healthy volunteers after intervention with carotenoid-rich foods. European Journal of Nutrition 38, 3544.Google ScholarPubMed
Ness, AR & Powles, JW (1997) Fruit and vegetables, and cardiovascular disease: a review. International Journal of Epidemiology 26, 113.CrossRefGoogle ScholarPubMed
Omenn, GS, Goodman, GE, Thornquist, MD, Balmes, J, Cullen, MR, Glass, A, Keogh, JP, Meyskens, F, Valaris, B, Williams, JH, Barnhart, S & Hammer, S (1996) Effects of a combination of beta-carotene and vitamin A on lung cancer and cardiovascular disease. New England Journal of Medicine 334, 11501155.CrossRefGoogle ScholarPubMed
Pelz, R, Schmidt-Faber, B & Heseker, H (1998) Die Carotinoidzufuhr in der Nationalen Verzehrsstudie (Carotenoid intake in the German National Food Consumption Survey). Zeitschrift für Ernährungswissenschaft 37, 319327.CrossRefGoogle ScholarPubMed
Pool-Zobel, BL, Bub, A, Müller, H, Wollowski, I & Rechkemmer, G (1997) Consumption of vegetables reduces genetic damage in humans: first results of a human intervention trial with carotenoid-rich foods. Carcinogenesis 18, 18471850.CrossRefGoogle ScholarPubMed
Ringer, TV, DeLoof, MJ, Winterrowd, GE, Francom, SF, Gaylor, SK, Ryan, JA, Sanders, ME & Hughes, GS (1991) Beta-carotene's effects on serum lipoproteins and immunologic indices in humans. American Journal of Clinical Nutrition 53, 688694.CrossRefGoogle ScholarPubMed
Santos, MS, Meydani, SN, Leka, L, Wu, D, Fotouhi, N, Meydani, M, Hennekens, CH & Gaziano, JM (1996) Natural killer cell activity in elderly men is enhanced by beta-carotene supplementation. American Journal of Clinical Nutrition 64, 772777.CrossRefGoogle ScholarPubMed
Stahl, W & Sies, H (1996) Lycopene: a biologically important carotenoid for humans? Archives of Biochemistry and Biophysics 336, 19.CrossRefGoogle ScholarPubMed
Steinmetz, KA & Potter, JD (1991) Vegetables, fruit, and cancer: II. Mechanisms. Cancer Causes and Control 2, 427442.CrossRefGoogle ScholarPubMed
The Alpha-Tocopherol, Beta-Carotene Cancer Prevention Study Group (1994) The effect of vitamin E and beta carotene on the incidence of lung cancer and other cancers in male smokers. New England Journal of Medicine 330, 10291035.CrossRefGoogle Scholar
Watson, RR, Prabhala, RH, Plezia, PM & Alberts, DS (1991) Effects of beta-carotene on lymphocyte subpopulations in elderly humans: evidence for dose-response relationship. American Journal of Clinical Nutrition 53, 9094.CrossRefGoogle ScholarPubMed