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Markers to measure immunomodulation in human nutrition intervention studies

  • Ruud Albers (a1), Jean-Michel Antoine (a2), Raphaëlle Bourdet-Sicard (a2), Philip C. Calder (a3), Michael Gleeson (a4), Bruno Lesourd (a5), Sonia Samartín (a6), Ian R. Sanderson (a7), Jan Van Loo (a8), F. Willem Vas Dias (a9) and Bernhard Watzl (a10)...

Abstract

Normal functioning of the immune system is crucial to the health of man, and diet is one of the major exogenous factors modulating individual immunocompetence. Recently, nutrition research has focused on the role of foods or specific food components in enhancing immune system responsiveness to challenges and thereby improving health and reducing disease risks. Assessing diet-induced changes of immune function, however, requires a thorough methodological approach targeting a large spectrum of immune system parameters. Currently, no single marker is available to predict the outcome of a dietary intervention on the resistance to infection or to other immune system-related diseases. The present review summarises the immune function assays commonly used as markers in human intervention studies and evaluates their biological relevance (e.g. known correlation with clinically relevant endpoints), sensitivity (e.g. within- and between-subject variation), and practical feasibility. Based on these criteria markers were classified into three categories with high, medium or low suitability. Vaccine-specific serum antibody production, delayed-type hypersensitivity response, vaccine-specific or total secretory IgA in saliva and the response to attenuated pathogens, were classified as markers with high suitability. Markers with medium suitability include natural killer cell cytotoxicity, oxidative burst of phagocytes, lymphocyte proliferation and the cytokine pattern produced by activated immune cells. Since no single marker allows conclusions to be drawn about the modulation of the whole immune system, except for the clinical outcome of infection itself, combining markers with high and medium suitability is currently the best approach to measure immunomodulation in human nutrition intervention studies. It would be valuable to include several immune markers in addition to clinical outcome in future clinical trials in this area, as there is too little evidence that correlates markers with global health improvement.

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Corresponding author

*Corresponding author: Dr S. Samartin, fax +32 2 762 00 44, email publications@ilsieurope.be

References

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Albert, MA & Ridker, PM (1999) The role of C-reactive protein in cardiovascular disease risk. Curr Cardiol Rep 1, 99104.
Allsopp, CEM, Nicholls, SJ & Langhorne, J (1998) A flow cytometric method to assess antigen-specific proliferative responses of different subpopulations of fresh and cryopreserved human peripheral blood mononuclear cells. J Immunol Methods 214, 175186.
Ananworanich, J & Shearer, WT (2002) Delayed-type hypersensitivity skin testing.In Manual of Clinical Laboratory Immunology 6th ed. 212219Rose, NR, Hamilton, B, Detrick, B, editors]. Washington, DC ASM Press
Arreaza, EE, Gibbons, JJ, Sisking, GW & Weksler, ME (1993) Lower antibody response to tetanus toxoid associated with higher auto-anti-idiotype antibody in old compared to young humans. Clin Exp Immunol 92, 169176.
Azim, T, Islam, LN, Sarker, MS, Ahmad, SM, Hamadani, JD, Faruque, SM & Salam, MA (2000) Immune response of Bangladeshi children with acute diarrhea who subsequently have persistent diarrhea. J Pediatr Gastroenterol Nutr 31, 528535.
Aziz, M, Akhtar, S & Malik, A (1998) Evaluation of cell-mediated immunity and circulating immune complexes as prognostic indicators in cancer patients. Cancer Detect Prev 22, 8799.
Beery, TA (2003) Sex differences in infection and sepsis. Crit Care Nurs Clin North Am 15, 5562.
Berk, LS, Ton, SA, Nieman, DC & Eby, EC (1986) The suppressive effect of stress from acute exhaustive exercise on T-lymphocyte helper/suppressor ratio in athletes and non-athletes. Med Sci Sports Exerc 18, 706710.
Beutler, B (2004) Innate immunity: an overview. Mol Immunol 40, 845859.
Bienvenu, J, Monneret, G, Fabien, N & Revillard, JP (2000) The clinical usefulness of the measurement of cytokines. Clin Chem Lab Med 38, 267285.
Blannin, AK, Chatwin, LJ, Cave, R & Gleeson, M (1996) Effects of submaximal cycling and long-term endurance training on neutrophil phagocytic activity in middle-aged men. Br J, SportsM, ed 30, 125129.
Blatt, SP, Hendrix, CW, Butzin, CA, Freeman, TM, Ward, WW, Hensley, RE, Melcher, GP, Donovan, DJ & Boswell, RN (1993) Delayed-type hypersensitivity skin testing predicts progression to AIDS in HIV-infected patients. Ann Intern Med 119, 177184.
Bloemena, E, Roos, MT, Van Heijst, JL, Vossen, JM & Schellekens, PT (1989) Whole-blood lymphocyte cultures. J Immunol Methods 122, 161167.
Bogden, JD, Oleske, JM, Lavenhar, MA, Munves, EM, Kemp, FW, Bruening, KS, Holding, KJ, Denny, TN, Guarino, MA & Holland, BK (1990) Effects of one year supplementation with zinc and other micronutrients on cellular immunity in the elderly. J Am Coll Nutr 9, 214225.
Bogden, JD, Bendich, A, Kemp, FW, Bruening, KS, Skurnick, JH, Denny, T, Baker, H & Louria, DB (1994) Daily micronutrient supplements enhance delayed-hypersensitivity skin test responses in older people. Am J, Clin Nutr 60, 437447.
Bouman, A, Schipper, M, Heineman, MJ & Faas, MM (2004) Gender difference in the non-specific and specific immune response in humans. Am J, Reprod Immunol 52, 1926.
Bovee-Oudenhoven, IM, Lettink-Wissink, ML, Van Doesburg, W, Witteman, BJ, Van, DMeer, R (2003) Diarrhea caused by enterotoxigenic Escherichia coli infection of humans is inhibited by dietary calcium. Gastroenterology 125, 469476.
Brabin, L (2002) Interactions of the female hormone environment, susceptibility to viral infections, and disease progression. AIDS Patient Care STDS 16, 211221.
Bradley, JA, Ledingham, IM & Hamilton, DN (1981) Assessment of host resistance in critically ill surgical patients by the response to recall skin antigens. Intensive Care Med 7, 105108.
Broadbent, DE, Broadbent, MH, Phillpotts, RJ & Wallace, J (1984) Some further studies on the prediction of experimental colds in volunteers by psychological factors. J Psychosom Res 28, 511523.
Bruunsgaard, H, Hartkopp, A, Mohr, T, Konradsen, H, Heron, I, Mordhorst, CH & Pedersen, BK (1997) In vivo cell-mediated immunity and vaccination response following prolonged, intense exercise. Med Sci Sports Exerc 29, 11761181.
Burdge, GC & Calder, PC (2005) Plasma cytokine response during the postprandial period: a potential causal process in vascular disease?. Br J Nutr 93, 39.
Cakman, I, Rohwer, J, Schutz, RM, Kirchner, H & Rink, L (1996) Dysregulation between TH1 and TH2 cell sub-populations in the elderly. Mech Ageing Dev 87, 197209.
Calder, PC & Field, CJ (2002) Fatty acids, inflammation and immunity.In Nutrition and Immune Function pp.5792 [Calder, PC, Field, CJ, Gill, HS, editors]. OxfordCABI Publishing.
Calder, PC & Kew, S (2002) The immune system: a target for functional foods?. Br J Nutr 88 Suppl. 2 S165S177
Ceddia, MA & Woods, J (1999) Exercise suppresses macrophage antigen presentation. J Appl Physiol 87, 22532258.
Chandra, RK (1984) Excessive intake of zinc impairs immune responses. JAMA 52, 14431446.
Chandra, RK (1991) 1990 McCollum Award Lecture: Nutrition and immunity: lessons from the past and new insights into the future. Am J, Clin Nutr 53, 10871101.
Chandra, RK (1992) Effect of vitamin and trace-element supplementation on immune responses and infection in elderly subjects. Lancet 340, 11241127.
Chang, L, Gusewitch, GA, Chritton, DB, Folz, JC, Lebeck, LK, Nehlsen-Cannarella, SL (1993) Rapid flow cytometric assay for the assessment of natural killer cell activity. J Immunol Methods 166, 4554.
Christou, NV, Meakins, JL, Gordon, J, Yee, J, Hassan-Zahraee, M, Nohr, CW, Shizgal, HM, MacLean, LD (1995) The delayed hypersensitivity response and host resistance in surgical patients: 20 years later. Ann Surg 222, 534546.
Cohen, S, Tyrrell, DA & Smith, AP (1991) Psychological stress and susceptibility to the common cold. N Eng J Med 325, 606612.
Cossarizza, A, Ortolani, C & Paganelli, R (1992) Age-related imbalance of virgin (CD45RA + ) and memory (CD45RO + ) cells between CD4 + and CD8 + T lymphocytes in humans: study from newborns to centenarians. J Immunol Res 4, 117126.
Cross, NA, Shetty, G, Nordstrom, JW, Davis, CA & Kramer, TR (1998) Effects of mixed-carotenoid supplementation on plasma carotene concentrations and T lymphocyte immunocompetence in elderly black women. FASEB J 12 A857 Abstr
Cummings, JH, Antoine, J-M & Aspiroz, F (2004) PASSCLAIM – Gut health and immunity. Eur J Nutr 43 Suppl. 2 118173
Curotto de Lafaille, MA & Lafaille, JJ (2002) CD4 (+) regulatory T cells in autoimmunity and allergy. Curr Opin Immunol 14, 771778.
Dandona, P, Aljada, A & Bandyopadhyay, A (2004) Inflammation: the link between insulin resistance, obesity and diabetes. Trends Immunol 25, 47.
Decker, T, Lohmann-Matthes, ML (1988) A quick and simple method for the quantitation of lactate dehydrogenase release in measurements of cellular cytotoxicity and tumor necrosis factor (TNF) activity. J Immunol Methods 115, 6169.
Dean, PA & Elson, CD (1997) Immunology.In Surgery of the Colon and Rectum.pp. 57 [Nicholls, RJ, Dozois, RR, editors]. New York: Churchill Livingstone.
Delacroix, DL, Dive, C, Rambaud, JC & Vaerman, JP (1982) IgA subclasses in various secretions and in serum. Immunology 47, 383385.
Elsasser-Beile, Uvon Kleist, S & Gallati, H (1991) Evaluation of a test system for measuring cytokine production in human whole blood cell cultures. J Immunol Methods 139, 191195.
Faas, M, Bouman, A, Moesa, H, Heineman, MJ, de Leij, L (2000) Schuiling G The immune response during the luteal phase of the ovarian cycle: a TH2-type response. Fertil Steril 74, 10081013.
Fidel, PL Jr (2002) Immunity to Candida. Oral Dis 8 Suppl. 2 6975.
Fietta, A, Merlini, C, Dos, SC, Rovida, S & Grassi, C (1994) Influence of aging on some specific and nonspecific mechanisms of the host defense system in 146 healthy subjects. Gerontology 40, 237245.
Fletcher, MA & Saliou, P (2000) Vaccines and infectious disease. EXS 89, 6988.
Fritscher-Ravens, A & Swain, CP (2002) The wireless capsule: new light in the darkness. Dig Dis 20 Suppl. 2 127133.
Fujiwara, S, Akiyama, M, Yamakido, M, Seyama, T, Kobuke, K, Hakoda, M, Kyoizumi, S & Jones, SL (1986) Cryopreservation of human lymphocytes for assessment of lymphocyte subsets and natural killer cytotoxicity. J Immunol Methods 90, 265273.
Fuller, CJ, Faulkner, H, Bendich, A, Parker, RS & Roe, DA (1992) Effect of β-carotene supplementation on photosuppression of delayed-type hypersensitivity in normal young men. Am J Clin Nutr 56, 684690.
Gaines, H, Andersson, L & Biberfeld, G (1996) A new method for measuring lymphoproliferation at the single-cell level in whole blood cultures by flow cytometry. J Immunol Methods 195, 6372.
Gannon, GA, Rhind, S, Shek, PN & Shephard, RJ (2002) Naïve and memory T cell subsets are differentially mobilized during physical stress. Int J Sports Med 23, 223229.
Gardner, EM & Murasko, DM (2002) Age-related changes in type 1 and type 2 cytokine production in humans. Biogerontology 3, 271290.
Gill, HS & Cross, ML (2002) Probiotics and immune function. In Nutrition and Immune Function, pp. 251272 [Calder, PC, Fields, CJ and Gill, HS, editors]. Oxford: CABI Publishing.
Girardin, SE & Philpott, DJ (2004) Mini-review: the role of peptidoglycan recognition in innate immunity. Eur J Immmunol 34, 17771782.
Gleeson, M (2000) Mucosal immune responses and risk of respiratory illness in elite athletes. Exerc Immunol Rev 6, 542.
Gleeson, M (2004) Immune function and exercise. Eur J Sport Sci 4, 5261.
Gleeson, M & Bishop, NC (1999) Immunology. In Basic and Applied Sciences for Sports Medicine, pp. 199236 [Maughan, RJ, editor]. Oxford: Butterworth Heinemann.
Gordin, FM, Hartigan, PM, Klimas, NG, Zolla-Pazner, SB, Simberkoff, MS & Hamilton, JD (1994) Delayed-type hypersensitivity skin tests are an independent predictor of human immunodeficiency virus disease progression. Department of Veterans Affairs Cooperative Study Group. J Infect Dis 169, 893897.
Graat, JM, Schouten, EG & Kok, FJ (2002) Effect of daily vitamin E and multivitamin-mineral supplementation on acute respiratory tract infections in elderly persons: a randomized control trial. JAMA 288, 715721.
Hamrick, N, Cohen, S & Rodriguez, MS (2002) Being popular can be healthy or unhealthy: stress, social network diversity, and incidence of upper respiratory tract infection. Health Psychol 21, 294298.
Haus, E & Smolensky, MH (1999) Biologic rhythms in the immune system. Chronobiol Int 16, 581622.
Hayek, GM, Mura, C, Wu, D, Beharka, AA, Han, SN, Paulson, E, Hwang, D & Meydani, SN (1997) Enhanced expression of inducible cyclooxygenase with age in murine macrophages. J Immunol 159, 14451451.
Heath, GW, Ford, ES, Craven, TE, Macera, CA, Jackson, KL & Pate, RR (1991) Exercise and the incidence of upper respiratory tract infections. Med Sci Sports Exerc 23, 152157.
Herraiz, LA, Hsieh, WC, Parker, RS, Swanson, JE, Bendich, A & Roe, DA (1998) Effect of UV exposure and β-carotene supplementation on delayed-type hypersensitivity response in healthy older men. J Am Coll Nutr 17, 617624.
Hofmann, B, Bygbjerg, I, Dickmeiss, E, Faber, V, Frederiksen, B, Gaub, J, Gerstoft, J, Jakobsen, BK, Jakobsen, KD & Lindhardt, BO (1989) Prognostic value of immunologic abnormalities and HIV antigenemia in asymptomatic HIV-infected individuals: proposal of immunologic staging. Scand J Infect Dis 21, 633643.
Hutchinson, P, Divola, LA & Holdsworth, SR (1999) Mitogen-induced T-cell CD69 expression is a less sensitive measure of T-cell function than [3H]-thymidine uptake. Cytometry 38, 244249.
Imai, K, Matsuyama, S, Miyake, S, Suga, K & Nakachi, K (2000) Natural cytotoxic activity of peripheral-blood lymphocytes and cancer incidence: an 11-year follow-up study of a general population. Lancet 356, 17951799.
Isaacs, D, Webster, ADB & Valman, HB (1984) Immunoglobulin levels and function in preschool children with recurrent respiratory infections. Clin Exp Immunol 58, 335340.
Janeway, CA, Travers, P, Walport, M & Shlomchik, M (2005) Immunobiology, 6th ed. London: Garland Publishing.
Jemmott, JB, Borysenko, JZ, Borysenko, M, McClelland, DC, Chapman, R, Meyer, D & Benson, H (1983) Academic stress, power motivation, and decrease in secretion rate of salivary secretory immunoglobulin A. Lancet 1, 14001402.
Jewett, MA, Gupta, S, Hansen, JA, Cunningham-Rundles, S, Siegal, FP, Good, RA & Dupont, B (1976) The use of cryopreserved lymphocytes for longitudinal studies of immune function and enumeration of subpopulations. Clin Exp Immunol 25, 449454.
Keil, D, Luebke, RW & Pruett, SB (2001) Quantifying the relationship between multiple immunological parameters and host resistance: probing the limits of reductionism. J Immunol 167, 45434552.
Komatsu, M, Kobayashi, D, Saito, K, Furuya, D, Yagihashi, A, Araake, H, Tsuji, N, Sakamaki, S, Niitsu, Y & Watanabe, N (2001) Tumor necrosis factor-a in serum of patients with inflammatory bowel disease as measured by a highly sensitive immuno-PCR. Clin Chem 47, 12971301.
Konjevic, G, Jurisic, V & Spuzic, I (1997) Corrections to the original lactate dehydrogenase (LDH) release assay for the evaluation of NK cell cytotoxicity. J Immunol Methods 200, 199201.
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. Am J Clin Nutr 65, 871875.
Kruse, N & Rieckmann, P (2002) Molecular analysis of cytokines and cytokine receptors. In Manual of Clinical Laboratory Immunology, 6th ed. 347356 [Rose, NR, Hamilton, B and Detrick, B, editors]. Washington, DC: ASM Press.
Kuritzkes, DR (2000) Neutropenia, neutrophil dysfunction, and bacterial infection in patients with human immunodeficiency virus disease: the role of granulocyte colony-stimulating factor. Clin Infect Dis 30, 256260.
Lancaster, GL, Halson, SL, Khan, Q, Drysdale, P, Jeukendrup, AE, Drayson, MT & Gleeson, M (2003 a) Effect of acute exhaustive exercise and a 6-day period of intensified training on immune function in cyclists. J Physiol 548, O96.
Lancaster, GL, Halson, SL, Khan, Q, Drysdale, P, Jeukendrup, AE, Drayson, MT & Gleeson, M (2003 b) Effect of exhaustive exercise and intensified training on human T-lymphocyte CD45RO expression. J Physiol 548, O97.
Lancaster, GL, Khan, Q, Drysdale, P, Jeukendrup, AE, Drayson, MT & Gleeson, M (2003 c) The effect of exercise on the expression and function of human monocyte toll-like receptors. J Physiol 555, C112.
Lehmann, AK, Sornes, S & Halstensen, A (2000) Phagocytosis: measurement by flow cytometry. J Immunol Methods 243, 229242.
Leroux-Roels, G, Van Hecke, E, Michielsen, W, Voet, P, Hauser, P & Petre, J (1994) Correlation between in vivo humoral and in vitro cellular immune responses following immunization with hepatitis B surface antigen (HBsAg) vaccines. Vaccine 12, 812818.
Lesourd, B (1999) Immune responses during diseases and recovery in the elderly. Proc Nutr Soc 58, 114.
Lesourd, B (2000) Undernutrition: a factor of accelerated ageing in healthy and diseased aged persons. In Handbook of Nutrition in the Aged Persons, pp. 145158 [Watson, RR, editor]. New York: CRC Press.
Lesourd, BM, Wang, A & Moulias, R (1985) Serial delayed cutaneous hypersensitivity skin testing with multiple recall antigens in healthy volunteers: booster effect study. Ann Allergy 55, 729735.
Lesourd, BM, Mazari, L & Ferry, M (1998) The role of nutrition in immunity in the aged. Nutr Rev 56, S113S125.
Lesourd, B, Raynaud-Simon, A & Mazari, L (2002) Nutrition and ageing of the immune system. In Nutrition and Immune Function, pp. 357374 [Calder, PC, Field, CJ and Gill, HS, editors]. Oxford: CABI Publishing.
Levy, SM, Herberman, RB, Lee, J, Whiteside, T, Beadle, M, Heiden, L & Simons, A (1991) Persistently low natural killer cell activity, age, and environmental stress as predictors of infectious morbidity. Nat Immun Cell Growth Regul 10, 289307.
Liebmann, PM, Reibnegger, G, Lehofer, M, Moser, M, Purstner, P, Mangge, H & Schauenstein, K (1998) Circadian rhythm of the soluble p75 tumor necrosis factor (sTNF-R75) receptor in humans – a possible explanation for the circadian kinetics of TNF-α effects. Int Immunol 10, 13931396.
Liew, FY (2002) T(H)1 and T(H)2 cells: a historical perspective. Nature Rev Immunol 2, 5560.
Ligthart, GJ, Corberand, JX, Fournier, C, Galanaud, P, Hijmans, W, Kennes, B, Muller-Hermelink, HK & Steinmann, GG (1984) Admission criteria for immunogerontological studies in man: the SENIEUR protocol. Mech Ageing Dev 28, 4755.
Lord, JM, Butcher, S, Killampali, V, Lascelles, D & Salmon, M (2001) Neutrophil ageing and immunesenescence. Mech Ageing Dev 122, 15211535.
Lyons, AB (2000) Analysing cell division in vivo and in vitro using flow cytometric measurement of CFSE dye dilution. J Immunol Methods 243, 147154.
Mackinnon, LT (1999) Advances in Exercise and Immunology Champaign, IL Human Kinetics
MacLean, LD (1988) Delayed type hypersensitivity testing in surgical patients Surg Gynecol Obstet 166, 285293.
MacLennan, ICM & Drayson, MT (1999) Normal lymphocytes and non-neoplastic lymphocyte disorders. In Postgraduate Haematology 4th ed. 296298 [Hoffbrand, AV, Lewis, SM, Tuddenham, EGDOxford: Butterworth Heinemann.
Maloy, KJ & Powrie, F (2001) Regulatory T cells in the control of immune pathology. Nat Immunol 2,, 816822.
Maloy, KJ, Salaun, L, Cahill, R, Dougan, G, Saunders, NJ & Powrie, F (2003) CD4 + CD25 + T(R) cells suppress innate immune pathology through cytokine-dependent mechanisms. J Exp Med 197, 111119.
Mann, DR, Akinbami, MA, Gould, KG & Ansari, AA (2000) Seasonal variation in cytokine expression and cell-mediated immunity in male rhesus monkeys. Cell Immunol 200, 105115.
Marrie, TJ, Johnson, S & Durant, H (1988) Cell-mediated immunity of healthy adult Nova Scotians in various age groups compared with nursing home and hospitalized senior citizens. J Allergy Clin Immunol 81, 836843.
Martinon, F, Rabian, C, Loiseau, P, Ternynck, TAvrameas, S & Colombani, J (1987) In vitro proliferation of human lymphocytes measured by an enzyme immunoassay using an anti-5-bromo-2-deoxyuridine monoclonal antibody. J Clin Lab Immunol 23, 153159.
Matthews, CE, Ockene, IS, Freedson, PS, Rosal, MC, Merriam, PA & Hebert, JR (2002) Moderate to vigorous physical activity and the risk of upper-respiratory tract infection. Med Sci Sports Exerc 34, 12421248.
Mazari, L & Lesourd, B (1998) Nutritional influence on immune response in healthy aged persons. Mech Ageing Dev 100, 1732.
Messele, T, Roos, MT, Hamann, D, Koot, M, Fontanet, AL, Miedema, F, Schellekens, PT & Rinke de Wit, TF (2000) Nonradioactive techniques for measurement of in vitro T-cell proliferation: alternatives to the [3 H]thymidine incorporation assay. Clin Diagn Lab Immunol 7, 687692.
Meyaard, L, Kuiper, H, Otto, SA, Wolthers, KC, Van Lier, RA & Miedema, F (1995) Evidence for intact costimulation via CD28 and CD27 molecules in hyporesponsive T cells from human immunodeficiency virus-infected individuals. Eur J Immunol 25, 232237.
Meydani, SN, Barklund, MP, Liu, S, Meydani, M, Miller, RA, Cannon, JG, Morrow, FD, Rocklin, R & Blumberg, JB (1990) Vitamin E supplementation enhances cell-mediated immunity in healthy elderly subjects. Am J, Clin Nutr 52, 557563.
Meydani, SN, Meydani, M, Blumberg, JB, Lekal, S, Siber, G, Loszewski, R, Thompson, C, Pedrosa, C, Diamond, RD & Stollar, BD (1997) Vitamin E supplementation and in vivo immune responses in healthy elderly individuals. JAMA 277, 13801386.
Moynihan, JA, Callahan, TA, Kelley, SP & Campbell, LM (1998) Adrenal hormone modulation of type 1 and type 2 cytokine production by spleen cells: dexamethasone and dehydroepiandrosterone suppress interleukin-2, interleukin-4, and interferon-gamma production in vitro. Cell Immunol 184, 5864.
Murasko, DM, Weiner, P & Kaye, D, (1987) Decline in mitogen induced proliferation of lymphocytes with increasing age. Clin Exp Immunol 70, 440448.
Mylonaki, M, Fritscher-Ravens, A & Swain, P, (2003) Wireless capsule endoscopy: a comparison with push enteroscopy in patiens with gastroscopy and colonoscopy negative gastrointestinal bleeding. Gut 52, 11221126.
Myrianthefs, P, Karatzas, S, Venetsanou, K, Grouzi, E, Evagelopoulou, P, Boutzouka, E, Fildissis, G, Splilotopoulou, I & Baltopoulos, G (2003) Seasonal variation in whole blood cytokine production after LPS stimulation in normal individuals. Cytokine 24, 286292.
Nagao, F, Yabe, T, Xu, M, Yokoyama, K, Saito, K & Okumura, K (1996) Application of non-radioactive europium (Eu 3+ ) release assay to a measurement of human natural killer activity of healthy and patient populations. Immunol Invest 25, 507518.
Nelson, RJ (2004) Seasonal immune function and sickness responses. Trends Immunol 25, 187192.
Nelson, RJ & Demas, GE (1996) Seasonal changes in immune function. Q Rev Biol 71, 511548.
Nieman, DC (1994) Exercise, infection and immunity. Int J, Sports M ed 15, S131S141.
Nieman, DC, Johansen, LM, Lee, JW & Arabatzis, K (1990) Infectious episodes in runners before and after the Los Angeles Marathon. J Sports Med Phys Fitness 30, 316328.
Niess, AM, Dickhuth, H-H, Northoff, H & Fehrenbach, E (1999) Free radicals and oxidative stress in exercise – immunological aspects. Exerc Immunol Rev 5, 2256.
Nisbet-Brown, ER, Lee, JW, Cheung, RK & Gelfand, EW (1987) Antigen-specific and -nonspecific mitogenic signals in the activation of human T cell clones. J Immunol 138, 37133719.
Northoff, H, Berg, A & Weinstock, C (1998) Similarities and differences of the immune response to exercise and trauma: the IFN-γ concept. Can J Physiol Pharmacol 76, 497504.
O'Gorman, MRG (2002) Evaluation of phagocytic cell function. In Manual of Clinical Laboratory Immunology, 6th ed., pp. 265273 [Rose, NR, Hamilton, B and Detrick, B, editors]. Washington, DC: ASM Press.
Ogata, K, An, E, Shioi, Y, Nakamura, K, Luo, S, Yokose, N, Minami, S & Dan, K (2001) Association between natural killer cell activity and infection in immunologically normal elderly people. Clin Exp Immunol 124, 392397.
Ouellette, AJ & Bevins, CL (2000) Development of innate immunity in the small intestine. In Development of the Gastrointestinal Tract, pp. 147164 [Sanderson, IR and Walker, WA, editors]. Hamilton, BC: Decker.
Paavonen, T (1994) Hormonal regulation of immune responses. Ann Med 26, 255258.
Pallast, EG, Schouten, EGDe Waart, FG, Fonk, HC, Doekes, G, von Blomberg, BM & Kok, FJ (1999) Effect of 50- and 100-mg vitamin E supplements on cellular immune function in noninstitutionalized elderly persons. Am J Clin Nutr 69, 12731281.
Pawelec, G, Barnett, Y & Forsey, R (2002) T cells and aging, January 2002 update. Front Biosci 1, 10561283.
Pawelec, G, Akbar, A, Caruso, C, Effros, R, Grubeck-Loebenstein, B & Wikby, A (2004) Is immunosenescence infectious?. Trends Immunol 25, 406410.
Pedersen, BK & Bruunsgaard, H (1995) How physical exercise influences the establishment of infections. Sports Med 19, 393400.
Peters, EM & Bateman, ED (1983) Ultramarathon running and URTI: an epidemiological survey. S A Med J 64, 582584.
Peters, EM, Goetzsche, JM, Grobbelaar, B & Noakes, TD (1993) Vitamin C supplementation reduces the incidence of post-race symptoms of upper respiratory tract infection in ultramarathon runners. Am J, Clin Nutr 57, 170174.
Peters, EM, Goetzsche, JM, Joseph, LE & Noakes, TD (1996) Vitamin C as effective as combinations of anti-oxidant nutrients in reducing symptoms of upper respiratory tract infections in ultramarathon runners. S A J Sports Med 11, 2327.
Petersen, EW & Pedersen, BK (2002) Exercise and immune function Nutrition and Immune Function 347355 [Calder, PC, Fields, CJ, Gill, HS], Oxford: CABI Publishing
Provinciali, M, Di Stefano, G & Fabris, N (1992) Optimization of cytotoxic assay by target cell retention of the fluorescent dye carboxyfluorescein diacetate (CFDA) and comparison with conventional 51 Cr release assay. J Immunol Methods 155, 1924.
Pyne, DB (1994) Regulation of neutrophil function during exercise. Sports Med 17, 245258.
Remick, DG (2002) Protein analysis and bioassays of cytokines and cytokine receptors. In Manual of Clinical Laboratory Immunology, 6th ed., pp. 320337 [Rose, NR, Hamilton, B and Detrick, B, editors]. Washington, DC: ASM Press.
Renshaw, M, Rockwell, J, Englemann, C, Gerwirtz, A, Katz, J & Sambhara, S (2002) Cutting edge: impaired toll-like receptor expression and function in aging. J Immunol 169, 46974701.
Robson, PJ, Blannin, AK, Walsh, NP, Castell, LM & Gleeson, M (1999) Effects of exercise intensity, duration and recovery on in vitro neutrophil function in male athletes. Int J Sports Med 20, 128135.
Roller, M, Rechkemmer, G & Watzl, B (2004) Prebiotic inulin enriched with oligofructose in combination with the probiotics Lactobacillus rhamnosus and Bifidobacterium lactis modulates intestinal immune functions in rats. J Nutr 134, 153156.
Ronsen, O, Pedersen, BK, Oritsland, TR & Bahr, RKjeldsen-Kragh, J (2001) Leukocyte counts and lymphocyte responsiveness associated with repeated bouts of strenuous endurance exercise. J Appl Physiol 91, 425434.
Samartin, S & Chandra, RK (2001) Obesity, overnutrition and the immune system. Nutr Rev 21, 243262.
Sapolsky, RM, Krey, LC & McEwen, BS (1986) The neuroendocrinology of stress and aging: the glucocorticoid cascade hypothesis. Endocr Rev 7, 284301.
Schellekens, PT, Roos, MT, De Wolf, F, Lange, JM & Miedema, F (1990) Low T-cell responsiveness to activation via CD3/TCR is a prognostic marker for acquired immunodeficiency syndrome (AIDS) in human immunodeficiency virus-1 (HIV-1)-infected men. J Clin Immunol 10, 121127.
Schnare, M, Barton, GM, Holt, AC, Takeda, K, Akira, S & Medzhitov, R (2001) Toll-like receptors control activation of adaptive immune responses. Nat Immunol 2, 947950.
Scrimshaw, NS & SanGiovanni, JP (1997) Synergism of nutrition, infection and immunity: an overview. Am J Clin Nutr 66, 464S477S.
Shephard, RJ (1997) Physical Activity, Training and the Immune Response Carmel, IN: Cooper.
Shephard, RJ & Shek, PN (1999) Effects of exercise and training on natural killer cell counts and cytolytic activity: a meta-analysis. Sports Med 28, 177195.
Sherman, AR (1992) Zinc, copper and iron nutriture and immunity. J Nutr 122, 604609.
Sleijffers, A, Garssen, J, de Gruijl, FR, Boland, GJ, Van Hattum, J, Van Vloten, WA & Van Loveren, H (2001) Influence of ultraviolet B exposure on immune responses following hepatitis B vaccination in human volunteers. J Invest Dermatol 117, 11441150.
Smith, DS, Helzner, EC, Nuttall, CE Jr, Collins, M, Rofman, BA, Ginsberg, D, Goswick, CB & Magner, A (1989) Failure of zinc gluconate in treatment of upper respiratory tract infections. Antimicrob Agents Chemother 33, 646648.
Smith, JK, Chi, DS, Krish, G, Reynolds, S & Cambron, G (1990) Effect of exercise on complement activity. Ann Allergy 65, 304310.
Spirer, Z, Roifman, CM & Branski, D (1993) Pediatric Immunology. Pediatric and Adolescent Medicine, vol. 3. Basel: Karger.
Starkie, RL, Rolland, J, Angus, DJ, Anderson, MJ & Febbraio, M (2001) Circulating monocytes are not the source of elevations in plasma IL-6 and TNF-α levels after prolonged running. Am J Physiol Cell Physiol 280, C769C774.
Steensberg, A, Van Hall, G, Osada, T, Sacchetti, M, Saltin, B & Pedersen, BK (2000) Production of interleukin-6 in contracting human skeletal muscles can account for the exercise-induced increase in plasma interleukin-6. J Physiol 529, 237242.
Swain, P (2003) Wireless capsule: endoscopy. Gut 52, Suppl. 44850.
Tacket, CO, Binion, SB, Bostwick, E, Losonsky, G, Roy, MJ & Edelman, R (1992) Efficacy of bovine milk immunoglobulin concentrate in preventing illness after Shigella flexneri challenge. Am J Trop Med Hyg 47, 276283.
Tollerud, DJ, Morris Brown, L, Clark, JW, Neuland, CY, Mann, DL, Pankiw-Trost, LK & Blattner, WA (1991) Cryopreservation and long-term liquid nitrogen storage of peripheral blood mononuclear cells for flow cytometry analysis: effects on subsets proportions and fluorescence intensity. J Clin Lab Anal 5, 255261.
Touloumi, G, Pantazis, N, Karafoulidou, A, Mandalaki, T, Goedert, JJ, Kostrikis, LG & Hatzakis, A (2004) Changes in T cell receptor excision DNA circle (TREC) levels in HIV type 1-infected subjects pre- and post-highly active antiretroviral therapy. AIDS Res Hum Retroviruses 20, 4754.
Turner, RB & Cetnarowski, WE (2000) Effect of treatment with zinc gluconate or zinc acetate on experimental and natural colds. Clin Infect Dis 31, 12021208.
Turner, RB, Riker, DK & Gangemi, JD (2000) Ineffectiveness of echinacea for prevention of experimental rhinovirus colds. Antimicrob Agents Chemother 44, 17081709.
Van Loveren, H, Germolec, D, Koren, HS, Luster, MI, Nolan, C, Repetto, R, Smith, E, Vos, JG & Vogt, RF (1999) Report of the Bilthoven Symposium: Advancement of epidemiological studies in assessing the human health effects of immunotoxic agents in the environment and the workplace. Biomarkers 4, 135157.
Van Loveren, H, Van Amsterdam, JG, Vandebriel, RJ, Kimman, TG, Rumke, HC, Steerenberg, PS & Vos, JG (2001) Vaccine-induced antibody responses as parameters of the influence of endogenous and environmental factors. Environ Health Perspect 109, 757764.
Verde, TJ, Thomas, SG, Moore, RW, Shek, P & Shephard, RJ (1992) Immune responses and increased training of the elite athlete. J Appl Physiol 73, 14941499.
Vignali, DA (2000) Multiplexed particle-based flow cytometric assays. J Immunol Methods 243, 243255.
Walker, LS (2004) CD4 + CD25 + Treg: divide and rule? Immunology 111, 129137.
Walrand, S, Moreau, K, Caldefie, F, Tridon, A, Chassagne, J, Portefaix, G, Cynober, L, Beaufrère, B, Vasson, M-P & Boirie, Y (2001) Specific and nonspecific immune responses to fasting and refeeding differ in young adult and elderly persons. Am J Clin Nutr 74, 670678.
Watzl, B & Watson, RR (1992) Role of alcohol abuse in nutritional immunosuppression. J Nut 122, 733737.
Weksler, ME (1995) Immune senescence: deficiency or dysregulation? Nutr Rev 53, Suppl., S1S7.
Westermann, J & Pabst, R (1990) Lymphocyte subsets in the blood: a diagnostic window on the lymphoid system? Immunol Today 11, 406410.
Whiteside, TL, Bryant, J, Day, R & Herberman, RB (1990) Natural killer cytotoxicity in the diagnosis of immune dysfunction: criteria for a reproducible assay. J Clin Lab Anal 4, 102114.
Wiedermann, U, Kundi, M, Vollmann, U, Kollaritsch, H, Ebner, C & Wiedermann, G (2000) Different HBs antibody versus lymphoproliferative responses after application of a monovalent (hepatitis B) or combined (hepatitis A+hepatitis B) vaccine. Int Arch Allergy Immunol 123, 349353.
Wilder, RL (1998) Hormones, pregnancy, and autoimmune diseases. Ann N Y Acad Sci 840, 4550.
Wolf, R (2004) Essential Pediatric Allergy, Asthma and Immunology. New York: McGraw-Hill.
Woods, J, Lu, Q, Ceddia, MA & Lowder, T (2000) Special feature for the Olympics: effects of exercise on the immune system: exercise-induced modulation of macrophage function. Immunol Cell Biol 78, 545553.
Yaqoob, P, Newsholme, EA & Calder, PC (1999) Comparison of cytokine production in cultures of whole human blood and purified mononuclear cells. Cytokine 11, 600605.
Ye, P & Kirshner, DE (2002) Measuring emigration of human thymocytes by T-cell receptor excision circles. Crit Rev Immunol 22, 483497.
Zaman, K, Baqui, AH, Yunus, M, Sack, RB, Chowdhury, HR & Black, RE (1997) Malnutrition, cell-mediated immune deficiency and acute upper respiratory infections in rural Bangladeshi children. Acta Paediatr 86, 923927.
Zeidel, A, Beilin, B, Yardeni, I, Mayburd, E, Smirnov, G & Bessler, H (2002) Immune response in asymptomatic smokers. Acta Anaesthesiol Scand 46, 959964.

Keywords

Markers to measure immunomodulation in human nutrition intervention studies

  • Ruud Albers (a1), Jean-Michel Antoine (a2), Raphaëlle Bourdet-Sicard (a2), Philip C. Calder (a3), Michael Gleeson (a4), Bruno Lesourd (a5), Sonia Samartín (a6), Ian R. Sanderson (a7), Jan Van Loo (a8), F. Willem Vas Dias (a9) and Bernhard Watzl (a10)...

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