Immune status is more affected by age than by carotenoid depletion-repletion in healthy human subjects
Open accessAbstract
Prospective studies have indicated an age-related impairment of the immune response. Carotenoids have been hypothesised to enhance immune cell function. The aim of the present study was to describe the age-related effects and the impact of in vivo dietary carotenoid depletion and repletion on specific and non-specific immunity. A total of ninety-eight healthy male subjects (aged 20-75 years) received a carotenoid-depleted diet for 3 weeks and were then supplemented daily for 5 weeks with 30 mg β-carotene, 15 mg lycopene and 9 mg lutein. Blood samples were collected at study entry, after depletion and supplementation, and biomarkers of immune status were determined. We found that serum IgA levels were positively correlated with ageing. Lymphocyte phenotyping indicated an increase with age in the memory T-helper cell subpopulation (CD4⁺CD45RO⁺) concomitantly with a decrease in naive T-helper cells (CD4⁺CD45RA⁺). A significant increase in the natural killer cells subpopulation and a small decrease in B lymphocytes were also observed, especially for the oldest volunteers. From ex vivo cell function exploration, a positive correlation was observed between age and IL-2 production of phytohaemagglutinin-stimulated lymphocytes. Neutrophils' bactericidal activity was significantly impaired with age (from 50 years) and was modulated by carotenoid status. An age effect was found on neutrophils' spontaneous migration but not on directed migration. Immune response in healthy human subjects is mostly affected by age rather than by dietary carotenoid depletion and repletion. Even in carefully selected healthy volunteers, some age-related immune changes occur predominantly from 50 years onwards. This immunosenescence could generate a loss in the immune system adjustment capacity.
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
Integrity signals
Registry
Cites
Statistics
Claims the paper makes
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
Claims other papers make about this one
Each is checked against this paper’s own text: does it say what the citing paper says it does?
Older adults supplemented with carotenoids (30 mg β-carotene, 15 mg lycopene and 9 mg lutein) had a shift to T cells expressing a mature phenotype.
“Older adults supplemented with carotenoids (30 mg β-carotene, 15 mg lycopene and 9 mg lutein) had a shift to T cells expressing a mature phenotype”
From Immunosenescence and Its Hallmarks: How to Oppose Aging Strategically? A Review of Potential Options for Therapeutic Intervention (2019) · cites this paper as [137]
Older adults supplemented with carotenoids (30 mg β-carotene, 15 mg lycopene and 9 mg lutein) had an increase in NK cells.
“an increase in NK cells (137)”
From Immunosenescence and Its Hallmarks: How to Oppose Aging Strategically? A Review of Potential Options for Therapeutic Intervention (2019) · cites this paper as [137]
Older adults supplemented with carotenoids (30 mg β-carotene, 15 mg lycopene and 9 mg lutein) had higher IgA serum levels.
“higher IgA serum levels”
From Immunosenescence and Its Hallmarks: How to Oppose Aging Strategically? A Review of Potential Options for Therapeutic Intervention (2019) · cites this paper as [137]
Self-check
Percentages, sums and reported differences re-computed from the paper’s own numbers.
The self-check needs the paper’s full text.
Cites
Beta‐carotene, carotenoids, and disease prevention in humans
Mayne, S. T. (1996) · The FASEB Journal · doi:10.1096/fasebj.10.7.8635686 · Cited by 862 · see citing works
Carotenoid Action on the Immune Response
Chew, B. P., & Park, J. S. (2004) · Journal of Nutrition · doi:10.1093/jn/134.1.257s · Cited by 795 · see citing works
Admission criteria for immunogerontological studies in man: The senieur protocol
Ligthart, G. J., Corberand, J. X., Fournier, C., Galanaud, P., Hijmans, W., Kennes, B., Müller-Hermelink, H. K., & Steinmann, G. G. (1984) · Mechanisms of Ageing and Development · doi:10.1016/0047-6374(84)90152-0 · Cited by 754 · cited 2× · see citing works
“To overcome this problem, volunteers in the present study were recruited according to the SENIEUR protocol developed in 1984 by a collaborative study group as an attempt to define the criteria for selecting truly healthy aged individuals for immunogerontological studies((25)).”
MethodMarkers to measure immunomodulation in human nutrition intervention studies
Albers, R., Antoine, J., Bourdet‐Sicard, R., Calder, P. C., Gleeson, M., Lesourd, B., Samartı́n, S., Sanderson, I. R., Loo, J. V., Dias, F. W. V., et al. (2005) · British Journal Of Nutrition · doi:10.1079/bjn20051469 · Cited by 284 · see citing works
Walrand, S., Valeix, S., Rodriguez, C., Ligot, P., CHASSAGNE, J., & Vasson, M. (2003) · Clinica Chimica Acta · doi:10.1016/s0009-8981(03)00086-x · Cited by 211 · see citing works
Self-citationOlmedilla‐Alonso, B., Granado, F., Southon, S., Wright, A. J. A., Blanco, I., Gil-Martinez, E., van den Berg, H., Corridan, B. M., Roussel, A., Chopra, M., et al. (2001) · British Journal Of Nutrition · doi:10.1079/bjn2000248 · Cited by 210 · see citing works
Oral beta-carotene can increase the number of OKT4+ cells in human blood
ALEXANDER, M., Newmark, H. L., & MILLER, R. (1985) · Immunology Letters · doi:10.1016/0165-2478(85)90036-7 · Cited by 172 · see citing works
Natural killer cell activity in elderly men is enhanced by beta-carotene supplementation
Santos, M., Meydani, S., Leka, L., Wu, D., Fotouhi, N., Meydani, M., Hennekens, C., & Gaziano, J. (1996) · The American Journal of Clinical Nutrition · doi:10.1093/ajcn/64.5.772 · Cited by 163 · see citing works
Watson, R., Prabhala, R., Plezia, P., & Alberts, D. (1991) · The American Journal of Clinical Nutrition · doi:10.1093/ajcn/53.1.90 · Cited by 158 · see citing works
Paganelli, R., Quinti, I., Fagiolo, U., Cossarizza, A., ORTOLANI, C., GUERRA, E., Sansoni, P., Pucillo, L. P., Scala, E., Cozzi, E., et al. (1992) · Clinical & Experimental Immunology · doi:10.1111/j.1365-2249.1992.tb07954.x · Cited by 156 · see citing works
Carotenoids and genomic stability
Collins, A. R. (2001) · Mutation research. Fundamental and molecular mechanisms of mutagenesis · doi:10.1016/s0027-5107(01)00071-9 · Cited by 152 · see citing works
Cooper, D. A. (2004) · Journal of Nutrition · doi:10.1093/jn/134.1.221s · Cited by 147 · see citing works
Dietary carotenoids and human immune function
Hughes, D. A. (2001) · Nutrition · doi:10.1016/s0899-9007(01)00638-4 · Cited by 147 · see citing works
β-Carotene and the immune response
Bendich, A. (1991) · Proceedings of The Nutrition Society · doi:10.1079/pns19910036 · Cited by 124 · see citing works
Girodon, F., Blache, D., Monget, A. L., Lombart, M., Brunet-Lecompte, P., Arnaud, J., Richard, M., & Galan, P. (1997) · Journal of the American College of Nutrition · doi:10.1080/07315724.1997.10718698 · Cited by 122 · see citing works
The immune S ystem in the elderly
Ginaldi, L., Martinis, M. D., D’Ostitio, A., Marini, L., Loreto, M. F., Corsi, M., & Quaglino, D. (1999) · Immunologic Research · doi:10.1007/bf02786466 · Cited by 117 · see citing works
Lyan, B., Azaı̈s-Braesco, V., Cardinault, N., Tyssandier, V., Borel, P., Alexandre-Gouabau, M. C., & Grolier, P. (2001) · Journal of Chromatography B Biomedical Sciences and Applications · doi:10.1016/s0378-4347(00)00488-6 · Cited by 112 · see citing works
Modulation of human T-lymphocyte functions by the consumption of carotenoid-rich vegetables
Watzl, B., Bub, A., Brandstetter, B. R., & Rechkemmer, G. (1999) · British Journal Of Nutrition · doi:10.1017/s0007114599001634 · Cited by 106 · see citing works
ASTLEY, S. B., Elliott, R. M., Archer, D. B., & Southon, S. (2004) · British Journal Of Nutrition · doi:10.1079/bjn20031001 · Cited by 101 · see citing works
Nutritional influences on immune response in healthy aged persons
Mazari, L., & Lesourd, B. (1998) · Mechanisms of Ageing and Development · doi:10.1016/s0047-6374(98)00047-5 · Cited by 99 · see citing works
Beta-carotene's effects on serum lipoproteins and immunologic indices in humans
Ringer, T., DeLoof, M. J., Winterrowd, G. E., Francom, S., Gaylor, S., Ryan, J., Sanders, M. P. J., & Gs, H. (1991) · American Journal of Clinical Nutrition · doi:10.1093/ajcn/53.3.688 · Cited by 99 · see citing works
Watzl, B., Bub, A., Briviba, K., & Rechkemmer, G. (2003) · Annals of Nutrition and Metabolism · doi:10.1159/000072397 · Cited by 94 · see citing works
HUGHES, D. A., Wright, A. J. A., Finglas, P. M., PEERLESS, A. C. J., Bailey, A. L., ASTLEY, S. B., Pinder, A. C., & Southon, S. (1997) · Journal of Laboratory and Clinical Medicine · doi:10.1016/s0022-2143(97)90179-7 · Cited by 91 · see citing works
Olmedilla‐Alonso, B., Granado, F., Southon, S., Wright, A. J. A., Blanco, I., Gil-Martinez, E., BERG, H. V. D., Thurnham, D. I., Corridan, B. M., Chopra, M., et al. (2002) · Clinical Science · doi:10.1042/cs1020447 · Cited by 89 · see citing works
β-Carotene and selenium supplementation enhances immune response in aged humans
Wood, S. M., Beckham, C. J., Yosioka, A., Darban, H., & WATSON, R. R. (2000) · Integrative medicine · doi:10.1016/s1096-2190(00)00009-3 · Cited by 88 · see citing works
Walrand, S., Moreau, K., Caldefie, F., Tridon, A., CHASSAGNE, J., Portefaix, G., Cynober, L., Beaufrère, B., Vasson, M., & Boirie, Y. (2001) · American Journal of Clinical Nutrition · doi:10.1093/ajcn/74.5.670 · Cited by 87 · see citing works
Self-citationLesourd, B., & Meaume, S. (1994) · Immunology Letters · doi:10.1016/0165-2478(94)00062-x · Cited by 86 · see citing works
Immune Function and Vaccine Responses in Healthy Advanced Elderly Patients
Carson, P. J., Nichol, K. L., O'Brien, J., Hilo, P., & Janoff, E. N. (2000) · Archives of Internal Medicine · doi:10.1001/archinte.160.13.2017 · Cited by 79 · see citing works
Mobarhan, S. M., Bowen, P. E., Andersen, B. R., Evans, M., Stacewicz‐Sapuntzakis, M., Sugerman, S., Simms, P. E., Lucchesi, D., & Friedman, H. (1990) · Nutrition and Cancer · doi:10.1080/01635589009514094 · Cited by 78 · see citing works
Effects of Aging on Immune Function
Stowe, R. P., & Goodwin, J. S. (2011) · Springer eBooks · doi:10.1007/978-1-4419-6999-6_4 · Cited by 68 · see citing works
Santos, M. S., Gaziano, J. M., Leka, L. S., Beharka, A. A., Hennekens, C. H., & Meydani, S. N. (1998) · American Journal of Clinical Nutrition · doi:10.1093/ajcn/68.1.164 · Cited by 63 · see citing works
Santos, M., Leka, L. S., Ribaya‐Mercado, J. D., Russell, R., Meydani, M., Hennekens, C. H., Gaziano, J., & Meydani, S. N. (1997) · American Journal of Clinical Nutrition · doi:10.1093/ajcn/66.4.917 · Cited by 60 · see citing works
Stracke, B. A., Rüfer, C. E., Bub, A., Briviba, K., Seifert, S., Kunz, C., & Watzl, B. (2008) · British Journal Of Nutrition · doi:10.1017/s0007114508116269 · Cited by 60 · see citing works
Dixon, Z., Burri, B. J., Clifford, A. J., Frankel, E. N., Schneeman, B. O., Parks, E. J., Keim, N. L., BARBIERI, T. F., Wu, M.-M., Fong, A. K. H., et al. (1994) · Free Radical Biology and Medicine · doi:10.1016/0891-5849(94)90093-0 · Cited by 58 · see citing works
Mitochondrial uncoupling proteins (UCPs) and obesity.
Rock, E., Winklhofer-Roob, B. M., Ribalta, J., Scotter, M., Vasson, M., Brtko, J., Brigelius‐Flohé, R., Bronner, A., & Azaı̈s-Braesco, V. (2001) · PubMed · Cited by 54 · see citing works
Self-citationHughes, D. A., Wright, A. J. A., Finglas, P. M., Polley, A. C. J., Bailey, A. L., ASTLEY, S. B., & Southon, S. (2000) · The Journal of Infectious Diseases · doi:10.1086/315910 · Cited by 49 · see citing works
Corridan, B. M., O’Donoghue, M., HUGHES, D. A., & Morrissey, P. (2001) · European Journal of Clinical Nutrition · doi:10.1038/sj.ejcn.1601187 · Cited by 44 · see citing works
Wolvers, D. A. W., Broekmans, W. M. R., Logman, M. H., van der Wielen, R. P. J., & Albers, R. (2006) · Nutrition Journal · doi:10.1186/1475-2891-5-28 · Cited by 43 · see citing works
Walrand, S., Farges, M. ‐., Dehaese, O., Cardinault, N., Minet‐Quinard, R., Grolier, P., Bouteloup‐Demange, C., Ribalta, J., Winklhofer‐Roob, B. M., Rock, E., et al. (2004) · European Journal of Nutrition · doi:10.1007/s00394-004-0501-3 · Cited by 41 · see citing works
Self-citationGossage, C. P., Deyhim, M., Moser‐Veillon, P. B., Douglas, L. W., & Kramer, T. R. (2000) · American Journal of Clinical Nutrition · doi:10.1093/ajcn/71.4.950 · Cited by 32 · see citing works
Effect of a lowβ-carotene diet on the immune functions of adult women
Daudu, P., Kelley, D., Taylor, P., Burri, B., & Wu, M. (1994) · American Journal of Clinical Nutrition · doi:10.1093/ajcn/60.6.969 · Cited by 28 · see citing works
Moriguchi, S., Okishima, N., Sumida, S., Okamura, K., Doi, T., & Kishino, Y. (1996) · Nutrition Research · doi:10.1016/0271-5317(96)00005-x · Cited by 21 · see citing works
Neutrophils are immune cells preferentially targeted by retinoic acid in elderly subjects
Minet‐Quinard, R., Farges, M. ‐., Thivat, É., Deleine, C., Mayot, G., Brtko, J., Ribalta, J., Winklhofer‐Roob, B. M., Rock, E., & Vasson, M. (2010) · Immunity & Ageing · doi:10.1186/1742-4933-7-10 · Cited by 20 · see citing works
Self-citationEffects of Aging on Immune Function
Burns, E. A., & Goodwin, J. S. (2001) · Springer eBooks · doi:10.1007/978-1-4757-3432-4_4 · Cited by 16 · see citing works
Azaı̈s-Braesco, V., Winklhofer‐Roob, B. M., Ribalta, J., Hanley, B., Vasson, M., Brtko, J., Brigeluis-Flohe, R., & Bronner, A. (2000) · PubMed · Cited by 6 · see citing works
Self-citation
Flagged first, then by citations
1 of the 46 references couldn’t be matched to a known paper.
Research works printed but not linked: 1
- a,b,c Mean values with unlike superscript letters were significantly different (P, 0•05 for the same carotenoid studied). * Repeated-measures ANOVA þ Newman-Keuls test were used. References
Cited by
Sorted by citations
Aiello, A., Farzaneh, F., Candore, G., Caruso, C., Davinelli, S., Gambino, C. M., Ligotti, M. E., Zareian, N., & Accardi, G. (2019) · Frontiers in Immunology · doi:10.3389/fimmu.2019.02247 · Cited by 693 · see citing works
Toti, E., Chen, O., Palmery, M., Villaño, D., & Peluso, I. (2018) · Oxidative Medicine and Cellular Longevity · doi:10.1155/2018/4637861 · Cited by 171 · see citing works
Gonçalves-Mendes, N., Talvas, J., Dualé, C., Guttmann, A., Corbin, V., Marceau, G., Sapin, V., Brachet, P., Evrard, B., Laurichesse, H., et al. (2019) · Frontiers in Immunology · doi:10.3389/fimmu.2019.00065 · Cited by 142 · see citing works
Self-citationMelzer, S., Zachariae, S., Bocsi, J., Engel, C., Löffler, M., & Tárnok, A. (2015) · Cytometry Part B Clinical Cytometry · doi:10.1002/cyto.b.21234 · Cited by 93 · see citing works
Nutrition, diet and immunosenescence
Maijó, M., Clements, S. J., Ivory, K., Nicoletti, C., & Carding, S. R. (2014) · Mechanisms of Ageing and Development · doi:10.1016/j.mad.2013.12.003 · Cited by 85 · see citing works
Determinants of Serum Immunoglobulin Levels: A Systematic Review and Meta-Analysis
Khan, S. R., van der Burgh, A. C., Peeters, R. P., van Hagen, P. M., Dalm, V. A. S. H., & Chaker, L. (2021) · Frontiers in Immunology · doi:10.3389/fimmu.2021.664526 · Cited by 83 · see citing works
Metabolites Produced by Fungi against Fungal Phytopathogens: Review, Implementation and Perspectives
Rodrigo, S. M., García‐Latorre, C., & Santamaria, O. (2021) · Plants · doi:10.3390/plants11010081 · Cited by 61 · see citing works
Talvas, J., Garrait, G., Gonçalves-Mendes, N., Rouanet, J., Vergnaud, J., Kwiatkowski, F., Bachmann, P., Bouteloup, C., Bienvenu, J., & Vasson, M. (2014) · Clinical Nutrition · doi:10.1016/j.clnu.2014.12.002 · Cited by 53 · see citing works
Self-citationVasson, M., Farges, M., Gonçalves-Mendes, N., Talvas, J., Ribalta, J., Winklhofer‐Roob, B. M., Rock, E., & Rossary, A. (2013) · Immunity & Ageing · doi:10.1186/1742-4933-10-38 · Cited by 30 · see citing works
Self-citationSharma, R., Diwan, B., Sharma, A., & Witkowski, J. M. (2022) · Biogerontology · doi:10.1007/s10522-022-09995-6 · Cited by 29 · see citing works
Sharma, R., & Padwad, Y. S. (2020) · Ageing Research Reviews · doi:10.1016/j.arr.2020.101141 · Cited by 27 · see citing works
Garnica, M., Aiello, A., Ligotti, M. E., Accardi, G., Arasanz, H., Bocanegra, A., Blanco, E., Calabrò, A., Chocarro, L., Echaide, M., et al. (2022) · International Journal of Molecular Sciences · doi:10.3390/ijms23179797 · Cited by 19 · see citing works
Nutrition as a Tool to Reverse Immunosenescence?
Larbi, A., Cexus, O., & Bosco, N. (2017) · Elsevier eBooks · doi:10.1016/b978-0-12-805417-8.00026-3 · Cited by 14 · see citing works
Kumaresan, S., Karthi, V., Senthilkumar, V., & Stephen, A. O. (2015) · Cited by 13 · see citing works
Schmieder, H., Leischner, C., Piotrowsky, A., Marongiu, L., Venturelli, S., & Burkard, M. (2025) · Immunity & Ageing · doi:10.1186/s12979-025-00501-3 · Cited by 12 · see citing works
Gené‐Morales, J., Juesas, Á., Saez-Berlanga, Á., Martin, E. G., Garrigues-Pelufo, L., Sandoval-Camargo, B. S., Martin-Rivera, F., Chulvi‐Medrano, I., Jiménez‐Martínez, P., Alix‐Fages, C., et al. (2025) · Nutrients · doi:10.3390/nu17091431 · Cited by 11 · see citing works
A sustained high fat diet for two years decreases IgM and IL-1 beta in ageing Wistar rats
Pongratz, G., Lowin, T., Kob, R., Buettner, R., Bertsch, T., & Bollheimer, L. C. (2015) · Immunity & Ageing · doi:10.1186/s12979-015-0040-1 · Cited by 10 · see citing works
An Evidence-Based Systematic Review of Lutein by the Natural Standard Research Collaboration
Ulbricht, C. E. (2015) · Journal of Dietary Supplements · doi:10.3109/19390211.2014.988577 · Cited by 4 · see citing works
Immunostimulatory Potential of Natural Compounds and Extracts: A Review
Stroe, A. C., & Oancea, S. (2019) · Current Nutrition & Food Science · doi:10.2174/1573401315666190301154200 · Cited by 4 · see citing works
(2021) · Frontiers research topics · doi:10.3389/978-2-88966-718-5 · Cited by 3 · see citing works
Can Nutritional Intervention Counteract Immunosenescence in the Elderly?
Clements, S. J., & Carding, S. R. (2016) · Elsevier eBooks · doi:10.1016/b978-0-12-801816-3.00028-5
Duan, X., Qiao, S., Wang, L., Wang, Q., & Zhu, X. (2024) · doi:10.22541/au.170665470.04276891/v1
- Authors
- Farges, M.-C., Minet-Quinard, R., Walrand, S., Thivat, E., Ribalta, J., Winklhofer-Roob, B., Rock, E., & Vasson, M.-P.
- Affiliations
- Université Clermont Auvergne (FR)
- Universitat Rovira i Virgili (ES)
- Unité de Nutrition Humaine (FR)
- Corresponding author
- Vasson, Marie-Paule
- Venue
- British Journal Of Nutrition
- Publisher
- Cambridge University Press (CUP)
- Published
- 2012-03-08
- Volume
- 108
- Issue
- 11
- Pages
- 2054-2065
- ISSN
- 0007-1145 (ISSN-L)
- 1475-2662
- OpenAlex
- W1976796872
- Cited by
- 22
- References
- 46
- Citations by year
- 2025: 2 · 2024: 1 · 2022: 2 · 2021: 3 · 2020: 1 · 2019: 3 · 2018: 1 · 2017: 1 · 2016: 1 · 2015: 4 · 2014: 1 · 2013: 2
- FWCI
- 1.57
- Type
- journal article
- Language
- en
- Open access
- bronze
- doi.org
- Locations
- British Journal Of Nutrition (publishedVersion)
- PubMed (publishedVersion)
- HAL (submittedVersion)
- Rovira & Virgili repository (submittedVersion, cc-by)
- Topics
- Health Sciences › Medicine › Biochemistry › Antioxidant Activity and Oxidative Stress
- Health Sciences › Medicine › Rehabilitation › Exercise and Physiological Responses
- Life Sciences › Immunology and Microbiology › Immunology › T-cell and B-cell Immunology
- Keywords
- immunosenescence, age-related immune decline, carotenoids, beta-carotene, lycopene, lutein, serum IgA, T helper cell subsets, memory T cells, natural killer cells, B cells, IL-2 production, neutrophil bactericidal activity, neutrophil migration, immune status
- MeSH terms
- Adult, Aged, Aging, Antioxidants, Carotenoids, France, Humans, Hypersensitivity, Delayed, Immunoglobulin A, Leukopenia, Male, Middle Aged, Neutrophils, Phagocyte Bactericidal Dysfunction, Severity of Illness Index, Vitamin A Deficiency, Lymphocyte Subsets, IgA Deficiency, Reactive Oxygen Species, Dietary Supplements, Young Adult
About these checks
Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.
Statistics and arithmetic are recomputed, not judged.
Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.
What counts as a claim ›How we measure confidence ›How we check this ›
Are you an author, or do you see a problem with this page? Request a review