Caloric restriction reduces age-related and all-cause mortality in rhesus monkeys
Open accessAbstract
Caloric restriction (CR) without malnutrition increases longevity and delays the onset of age-associated disorders in short-lived species, from unicellular organisms to laboratory mice and rats. The value of CR as a tool to understand human ageing relies on translatability of CR’s effects in primates. Here we show that CR significantly improves age-related and all-cause survival in monkeys on a long-term ~30% restricted diet since young adulthood. These data contrast with observations in the 2012 NIA intramural study report, where a difference in survival was not detected between control-fed and CR monkeys. A comparison of body weight of control animals from both studies with each other, and against data collected in a multi-centred relational database of primate ageing, suggests that the NIA control monkeys were effectively undergoing CR. Our data indicate that the benefits of CR on ageing are conserved in primates. Caloric restriction extends the lifespan of various organisms but whether it works in monkeys is controversial. Here, Colman et al.report that caloric restriction reduces all-cause mortality of rhesus macaques, and perform a weight comparison that aims to reconcile their findings with contradictory results from a similar study.
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?
Caloric restriction extends both medium and maximum lifespan and delays the onset of age-related diseases in yeast, C. elegans, rodents and Rhesus monkeys.
“CR has been shown to extend both medium and maximum lifespan and delay the onset of age-related diseases in a variety of species, including yeast (Kaeberlein et al., 2007), C. elegans (Lee et al., 2006), rodents (Masoro, 2009) and Rhesus monkeys (Colman et al., 2014).”
From Role of the mitochondrial DNA replication machinery in mitochondrial DNA mutagenesis, aging and age-related diseases (2017) · cites this paper as Colman et al., 2014
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
Extending Healthy Life Span—From Yeast to Humans
Fontana, L., Partridge, L., & Longo, V. D. (2010) · Science · doi:10.1126/science.1172539 · Cited by 3,023 · see citing works
Caloric Restriction Delays Disease Onset and Mortality in Rhesus Monkeys
Colman, R. J., Anderson, R. M., Johnson, S. C., Kastman, E. K., Kosmatka, K. J., Beasley, T. M., Allison, D. B., Cruzen, C., Simmons, H. A., Kemnitz, J. W., et al. (2009) · Science · doi:10.1126/science.1173635 · Cited by 2,277 · see citing works
Self-citationImpact of caloric restriction on health and survival in rhesus monkeys from the NIA study
Mattison, J. A., Roth, G. S., Beasley, T. M., Tilmont, E. M., Handy, A. M., Herbert, R. L., Longo, D. L., Allison, D. B., Young, J. E., Bryant, M., et al. (2012) · Nature · doi:10.1038/nature11432 · Cited by 1,145 · see citing works
Self-citationWeindruch, R. H., Walford, R. L., Fligiel, S., & Guthrie, D. (1986) · Journal of Nutrition · doi:10.1093/jn/116.4.641 · Cited by 992 · see citing works
Self-citationWeindruch, R. H., & Walford, R. L. (1982) · Science · doi:10.1126/science.7063854 · Cited by 766 · see citing works
Self-citationLiao, C., Rikke, B. A., Johnson, T. E., Diaz, V., & Nelson, J. F. (2010) · Aging Cell · doi:10.1111/j.1474-9726.2009.00533.x · Cited by 501 · see citing works
Metabolic reprogramming, caloric restriction and aging
Anderson, R. M., & Weindruch, R. H. (2009) · Trends in Endocrinology and Metabolism · doi:10.1016/j.tem.2009.11.005 · Cited by 300 · see citing works
Self-citationBodkin, N. L., Alexander, T. M., Ortmeyer, H. K., Johnson, E., & Hansen, B. C. (2003) · The Journals of Gerontology Series A · doi:10.1093/gerona/58.3.b212 · Cited by 250 · see citing works
Kemnitz, J. W., Weindruch, R. H., Roecker, E. B., Crawford, K. S., Kaufman, P. L. P., & Ershler, W. B. (1993) · Journal of Gerontology · doi:10.1093/geronj/48.1.b17 · Cited by 224 · see citing works
Self-citationDiet restriction in rhesus monkeys lowers fasting and glucose-stimulated glucoregulatory end points
Lane, M. A., Ball, S. S., Ingram, D. K., Cutler, R. G., Engel, J., Read, V. H., & Roth, G. S. (1995) · American Journal of Physiology-Endocrinology and Metabolism · doi:10.1152/ajpendo.1995.268.5.e941 · Cited by 138 · see citing works
Dietary Interventions to Extend Life Span and Health Span Based on Calorie Restriction
Minor, R. K., Allard, J. S., Younts, C. M., Ward, T. M., & de Cabo, R. (2010) · The Journals of Gerontology Series A · doi:10.1093/gerona/glq042 · Cited by 112 · see citing works
Age-related pathology and biosenescent markers in captive rhesus macaques
Uno, H. (1997) · AGE · doi:10.1007/s11357-997-0001-5 · Cited by 105 · see citing works
Calorie Restriction and Aging in Nonhuman Primates
Kemnitz, J. W. (2011) · ILAR Journal · doi:10.1093/ilar.52.1.66 · Cited by 105 · see citing works
Self-citationThe Development of Small Primate Models for Aging Research
Fischer, K. E., & Austad, S. N. (2011) · ILAR Journal · doi:10.1093/ilar.52.1.78 · Cited by 94 · see citing works
Nonhuman Primate Calorie Restriction
Colman, R. J., & Anderson, R. M. (2010) · Antioxidants and Redox Signaling · doi:10.1089/ars.2010.3224 · Cited by 68 · see citing works
Self-citationRoth, G. S., Lesnikov, V. A., Lesnikov, M., et al. (2001) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jcem.86.7.7655 · Cited by 59 · see citing works
Ramsey, J. J., Laatsch, J. L., & Kemnitz, J. W. (2000) · Journal of Medical Primatology · doi:10.1034/j.1600-0684.2000.290102.x · Cited by 53 · see citing works
Self-citationCandidate Bird Species for Use in Aging Research
Austad, S. N. (2011) · ILAR Journal · doi:10.1093/ilar.52.1.89 · Cited by 45 · see citing works
Age and sex differences in body size and composition during Rhesus monkey adulthood
Hudson, J. C., Baum, S. T., Frye, D. M. D., Roecker, E. B., & Kemnitz, J. W. (1996) · Aging Clinical and Experimental Research · doi:10.1007/bf03339677 · Cited by 39 · see citing works
Self-citationReference Body Composition in Adult Rhesus Monkeys: Glucoregulatory and Anthropometric Indices
Raman, A., Colman, R. J., Cheng, Y., Kemnitz, J. W., Baum, S. T., Weindruch, R. H., & Schoeller, D. A. (2005) · The Journals of Gerontology Series A · doi:10.1093/gerona/60.12.1518 · Cited by 28 · see citing works
Self-citation
Flagged first, then by citations
Cited by
Sorted by citations
Facing up to the global challenges of ageing
Partridge, L., Deelen, J., & Slagboom, P. E. (2018) · Nature · doi:10.1038/s41586-018-0457-8 · Cited by 1,475 · see citing works
Promoting Health and Longevity through Diet: From Model Organisms to Humans
Fontana, L., & Partridge, L. (2015) · Cell · doi:10.1016/j.cell.2015.02.020 · Cited by 1,245 · see citing works
Mitochondrial dysfunction in cell senescence and aging
Miwa, S., Kashyap, S., Chini, E., & von Zglinicki, T. (2022) · Journal of Clinical Investigation · doi:10.1172/jci158447 · Cited by 1,061 · see citing works
Caloric restriction improves health and survival of rhesus monkeys
Mattison, J. A., Colman, R. J., Beasley, T. M., Allison, D. B., Kemnitz, J. W., Roth, G. S., Ingram, D. K., Weindruch, R., de Cabo, R., & Anderson, R. M. (2017) · Nature Communications · doi:10.1038/ncomms14063 · Cited by 838 · see citing works
Self-citationPharmacological modulation of autophagy: therapeutic potential and persisting obstacles
Galluzzi, L., Bravo-San Pedro, J. M., Levine, B., Green, D. R., & Kroemer, G. (2017) · Nature Reviews Drug Discovery · doi:10.1038/nrd.2017.22 · Cited by 842 · see citing works
Impact of Obesity and Metabolic Syndrome on Immunity
Andersen, C. J., Murphy, K. E., & Fernandez, M. L. (2016) · Advances in Nutrition · doi:10.3945/an.115.010207 · Cited by 701 · see citing works
Permissive underfeeding or standard enteral feeding in critically ill adults
Arabi, Y. M., Aldawood, A. S., Haddad, S. H., Al-Dorzi, H. M., Tamim, H. M., Jones, G., Mehta, S., McIntyre, L., Solaiman, O., Sakkijha, M. H., et al. (2015) · New England Journal of Medicine · doi:10.1056/nejmoa1502826 · Cited by 614 · see citing works
Interventions to slow aging in humans: are we ready?
Longo, V. D., Antebi, A., Bartke, A., Barzilai, N., Brown‐Borg, H. M., Caruso, C., Curiel, T. J., Cabo, R., Franceschi, C., Gems, D., et al. (2015) · Aging Cell · doi:10.1111/acel.12338 · Cited by 592 · see citing works
Calorie restriction in humans: An update
Most, J., Tosti, V., Redman, L. M., & Fontana, L. (2017) · Ageing Research Reviews · doi:10.1016/j.arr.2016.08.005 · Cited by 530 · see citing works
Molecular and physiological manifestations and measurement of aging in humans
Khan, S. S., Singer, B. D., & Vaughan, D. E. (2017) · Aging Cell · doi:10.1111/acel.12601 · Cited by 530 · see citing works
Decreased consumption of branched-chain amino acids improves metabolic health
Fontana, L., Cummings, N. E., Arriola Apelo, S. I., Neuman, J. C., Kasza, I., Schmidt, B. A., Cava, E., Spelta, F., Tosti, V., Syed, F. A., et al. (2016) · Cell Reports · doi:10.1016/j.celrep.2016.05.092 · Cited by 466 · see citing works
Ravussin, E., Redman, L. M., Rochon, J., Das, S. K., Fontana, L., Kraus, W. E., Romashkan, S., Williamson, D. A., Meydani, S. N., Villareal, D. T., et al. (2015) · The Journals of Gerontology Series A: Biological Sciences and Medical Sciences · doi:10.1093/gerona/glv057 · Cited by 489 · see citing works
Nutritional considerations for healthy aging and reduction in age-related chronic disease
Shlisky, J., Bloom, D. E., Beaudreault, A. R., Tucker, K. L., Keller, H. H., Freund-Levi, Y., Fielding, R. A., Cheng, F. W., Jensen, G. L., Wu, D., et al. (2017) · Advances in Nutrition · doi:10.3945/an.116.013474 · Cited by 462 · see citing works
Healthy aging: The ultimate preventative medicine
Kaeberlein, M., Rabinovitch, P. S., & Martin, G. M. (2015) · Science · doi:10.1126/science.aad3267 · Cited by 341 · see citing works
Repairing mitochondrial dysfunction in disease
Sorrentino, V., Menzies, K. J., & Auwerx, J. (2018) · Annual Review of Pharmacology and Toxicology · doi:10.1146/annurev-pharmtox-010716-104908 · Cited by 337 · see citing works
Immune aging, dysmetabolism, and inflammation in neurological diseases
Deleidi, M., Jäggle, M., & Rubino, G. (2015) · Frontiers in Neuroscience · doi:10.3389/fnins.2015.00172 · Cited by 260 · see citing works
Regulators of health and lifespan extension in genetically diverse mice on dietary restriction
Di Francesco, A., Deighan, A. G., Litichevskiy, L., Chen, Z., Luciano, A., Robinson, L., Garland, G., Donato, H., Schott, W., Wright, K. M., et al. (2023) · doi:10.1101/2023.11.28.568901 · Cited by 194 · see citing works
vel Szic, K. S., Declerck, K., Vidaković, M., & Vanden Berghe, W. (2015) · Clinical Epigenetics · doi:10.1186/s13148-015-0068-2 · Cited by 192 · see citing works
Senescence in Wound Repair: Emerging Strategies to Target Chronic Healing Wounds
Wilkinson, H. N., & Hardman, M. J. (2020) · Frontiers in Cell and Developmental Biology · doi:10.3389/fcell.2020.00773 · Cited by 173 · see citing works
DeBalsi, K. L., Hoff, K. E., & Copeland, W. C. (2017) · Ageing Research Reviews · doi:10.1016/j.arr.2016.04.006 · Cited by 180 · see citing works
Pak, H. H., Haws, S. A., Green, C. L., Koller, M., Lavarias, M. T., Richardson, N. E., Yang, S. E., Dumas, S. N., Sonsalla, M., Bray, L., et al. (2021) · Nature Metabolism · doi:10.1038/s42255-021-00466-9 · Cited by 171 · see citing works
Santos, A. L., Sinha, S., & Lindner, A. B. (2018) · Oxidative Medicine and Cellular Longevity · doi:10.1155/2018/1941285 · Cited by 168 · see citing works
A null mutation in <i>SERPINE1</i> protects against biological aging in humans
Khan, S. S., Shah, S. J., Klyachko, E., Baldridge, A. S., Eren, M., Place, A. T., Aviv, A., Puterman, E., Lloyd-Jones, D. M., Heiman, M., et al. (2017) · Science Advances · doi:10.1126/sciadv.aao1617 · Cited by 157 · see citing works
Aging and Caloric Restriction Research: A Biological Perspective with Translational Potential
Balasubramanian, P., Howell, P. R., & Anderson, R. M. (2017) · EBioMedicine · doi:10.1016/j.ebiom.2017.06.015 · Cited by 148 · see citing works
Self-citationDietary restriction.; mitochondrial function and aging: From yeast to humans
Ruetenik, A., & Barrientos, A. (2015) · Biochimica et Biophysica Acta (BBA) - Bioenergetics · doi:10.1016/j.bbabio.2015.05.005 · Cited by 139 · see citing works
Choi, I. Y., Lee, C., & Longo, V. D. (2017) · Molecular and Cellular Endocrinology · doi:10.1016/j.mce.2017.01.042 · Cited by 133 · see citing works
Mouse models of ageing and their relevance to disease
Kõks, S., Dogan, S., Tuna, B. G., González-Navarro, H., Potter, P., & Vandenbroucke, R. E. (2016) · Mechanisms of Ageing and Development · doi:10.1016/j.mad.2016.10.001 · Cited by 125 · see citing works
Caloric restriction: Beneficial effects on brain aging and Alzheimer’s disease
Van Cauwenberghe, C., Vandendriessche, C., Libert, C., & Vandenbroucke, R. E. (2016) · Mammalian Genome · doi:10.1007/s00335-016-9647-6 · Cited by 121 · see citing works
Most, J., Gilmore, L. A., Smith, S. R., Han, H., Ravussin, E., & Redman, L. M. (2018) · American Journal of Physiology-Endocrinology and Metabolism · doi:10.1152/ajpendo.00261.2017 · Cited by 117 · see citing works
Cunha-Santos, J., Duarte-Neves, J., Carmona, V., Guarente, L., Pereira de Almeida, L., & Cavadas, C. (2016) · Nature Communications · doi:10.1038/ncomms11445 · Cited by 109 · see citing works
Temporal inhibition of autophagy reveals segmental reversal of ageing with increased cancer risk
Cassidy, L. D., Young, A. R. J., Young, C. N. J., Soilleux, E. J., Fielder, E., Weigand, B. M., Lagnado, A., Brais, R., Ktistakis, N. T., Wiggins, K. A., et al. (2020) · Nature Communications · doi:10.1038/s41467-019-14187-x · Cited by 108 · see citing works
Neuroprotective effects of dietary restriction: Evidence and mechanisms
Pani, G. (2015) · Seminars in Cell & Developmental Biology · doi:10.1016/j.semcdb.2015.03.004 · Cited by 103 · see citing works
Napoleão, A., Fernandes, L., Miranda, C., & Marum, A. P. (2021) · Nutrients · doi:10.3390/nu13041302 · Cited by 103 · see citing works
Bartley, J. M., Zhou, X., Kuchel, G. A., Weinstock, G. M., & Haynes, L. (2017) · Frontiers in Immunology · doi:10.3389/fimmu.2017.01164 · Cited by 87 · see citing works
Nutrition and longevity—From mechanisms to uncertainties
Ekmekcioglu, C. (2020) · Critical Reviews in Food Science and Nutrition · doi:10.1080/10408398.2019.1676698 · Cited by 87 · see citing works
Benjamin, D. I., Both, P., Benjamin, J. S., Nutter, C. W., Tan, J. H., Kang, J., Machado, L. A., Klein, J. D. D., de Morree, A., Kim, S., et al. (2022) · Cell Metabolism · doi:10.1016/j.cmet.2022.04.012 · Cited by 79 · see citing works
Brandhorst, S., Levine, M. E., Wei, M., Shelehchi, M., Morgan, T. E., Nayak, K. S., Dorff, T., Hong, K., Crimmins, E. M., Cohen, P., et al. (2024) · Nature Communications · doi:10.1038/s41467-024-45260-9 · Cited by 71 · see citing works
Molecular and cellular aspects of age-related cognitive decline and Alzheimer’s disease
Hullinger, R., & Puglielli, L. (2017) · Behavioural Brain Research · doi:10.1016/j.bbr.2016.05.008 · Cited by 68 · see citing works
Dietary Restriction and Neuroinflammation: A Potential Mechanistic Link
Bok, E., Jo, M., Lee, S., Lee, B.-R., Kim, J., & Kim, H.-J. (2019) · International Journal of Molecular Sciences · doi:10.3390/ijms20030464 · Cited by 53 · see citing works
Nutrition modulation of human aging: The calorie restriction paradigm
Das, S. K., Balasubramanian, P., & Weerasekara, Y. K. (2017) · Molecular and Cellular Endocrinology · doi:10.1016/j.mce.2017.04.011 · Cited by 51 · see citing works
The force is strong with this one: metabolism (Over)powers stem cell fate
Wei, P., Dove, K. K., Bensard, C., Schell, J. C., & Rutter, J. (2018) · Trends in Cell Biology · doi:10.1016/j.tcb.2018.02.007 · Cited by 47 · see citing works
The Geroscience Hypothesis: Is It Possible to Change the Rate of Aging?
Austad, S. N. (2016) · Advances in Geroscience · doi:10.1007/978-3-319-23246-1_1 · Cited by 43 · see citing works
Nutrigenomics at the Interface of Aging, Lifespan, and Cancer Prevention
Riscuta, G. (2016) · The Journal of Nutrition · doi:10.3945/jn.116.235119 · Cited by 37 · see citing works
Aging and the Biological Response to Liver Injury
Marzioni, M., Pinto, C., Ninfole, E., Gaggiano, L., Benedetti, A., & Maroni, L. (2020) · Seminars in Liver Disease · doi:10.1055/s-0039-3402033 · Cited by 36 · see citing works
Martin, S. A., DeMuth, T. M., Miller, K. N., Pugh, T. D., Polewski, M. A., Colman, R. J., Eliceiri, K. W., Beasley, T. M., Johnson, S. C., & Anderson, R. M. (2016) · Aging Cell · doi:10.1111/acel.12418 · Cited by 32 · see citing works
Self-citationRadler, M. E., Wright, B. J., Walker, F. R., Hale, M. W., & Kent, S. (2015) · Neuroscience · doi:10.1016/j.neuroscience.2014.11.014 · Cited by 31 · see citing works
Beyond Calories: An Integrated Approach to Promote Health, Longevity, and Well-Being
Bertozzi, B., Tosti, V., & Fontana, L. (2017) · Gerontology · doi:10.1159/000446346 · Cited by 25 · see citing works
Influence of calorie reduction on DNA repair capacity of human peripheral blood mononuclear cells
Matt, K., Burger, K., Gebhard, D., & Bergemann, J. (2016) · Mechanisms of Ageing and Development · doi:10.1016/j.mad.2016.02.008 · Cited by 17 · see citing works
Mulvey, L., Sands, W. A., Salin, K., Carr, A. E., & Selman, C. (2017) · Molecular and Cellular Endocrinology · doi:10.1016/j.mce.2016.09.001 · Cited by 16 · see citing works
- Authors
- Colman, R. J., Beasley, T. M., Kemnitz, J. W., Johnson, S. C., Weindruch, R., & Anderson, R. M.
- Affiliations
- University of Wisconsin–Madison (US)
- University of Alabama (US)
- Corresponding author
- Anderson, Rozalyn M.
- Venue
- Nature Communications
- Published
- 2014-04-01
- Volume
- 5
- Issue
- 1
- Pages
- 3557-3557
- ISSN
- 2041-1723 (ISSN-L)
- PMC
- PMC3988801
- OpenAlex
- W2098343475
- Cited by
- 711
- References
- 20
- Citations by year
- 2026: 16 · 2025: 40 · 2024: 40 · 2023: 41 · 2022: 52 · 2021: 57 · 2020: 50 · 2019: 56 · 2018: 83 · 2017: 99 · 2016: 81 · 2015: 66 · 2014: 27 · 2013: 1
- FWCI
- 31.12
- Type
- journal article
- Language
- en
- Open access
- hybrid
- doi.org
- Licence
- Locations
- Nature Communications (publishedVersion, cc-by-nc-nd)
- Europe PMC (PubMed Central) (publishedVersion, cc-by-nc-nd)
- PubMed Central (publishedVersion, cc-by-nc-nd)
- PubMed (publishedVersion)
- RePEc: Research Papers in Economics (submittedVersion)
- Funders
- University of Wisconsin-Madison (P51OD011106)
- National Institutes of Health (P51RR000167/P51OD011106, P51OD011106)
- National Institute on Aging (R01AG037000, P50AG033514, R01AG040178, P01AG011915)
- National Center for Research Resources (P51RR000167/P51OD011106, P51RR000167)
- Office of Research Infrastructure Programs, National Institutes of Health (P51 OD011106, P51RR000167)
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Aging › Genetics, Aging, and Longevity in Model Organisms
- Health Sciences › Medicine › Physiology › Dietary Effects on Health
- Health Sciences › Medicine › Geriatrics and Gerontology › Sirtuins and Resveratrol in Medicine
- Keywords
- caloric restriction, rhesus monkeys, longevity, all-cause mortality, age-related mortality, aging, body weight
- MeSH terms
- Aging, Animals, Body Weight, Disease Models, Animal, Female, Humans, Longevity, Macaca mulatta, Male, Mortality, Survival Analysis, Caloric Restriction
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
