Attenuation of sarcopenia by dietary restriction in rhesus monkeys
Open accessAbstract
Sarcopenia, the loss of muscle mass with normal aging, devastates quality of life-and related healthcare expenditures are enormous. The prevention or attenuation of sarcopenia would be an important medical advance. Dietary restriction (DR) is the only dietary intervention that consistently extends median and maximum life span, as well as health span in rodents. Evidence suggests that DR will have a similar effect in primates. Furthermore, DR opposes sarcopenia in rodents. We tested the hypothesis that DR will reduce age-related sarcopenia in a nonhuman primate. Thirty adult male rhesus monkeys, half fed a normal calorie intake and half reduced by 30% in caloric intake, were examined over 17 years for changes in dual-energy X-ray absorptiometry-estimated skeletal muscle mass. Body weight-adjusted skeletal muscle mass declined somewhat in both groups but was far more rapid in the control group. We have shown that moderate, adult-onset DR can attenuate sarcopenia in a nonhuman primate model.
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?
CR delays age-associated muscle dysfunction in D. melanogaster and rhesus monkeys, and delays the onset of sarcopenia in rhesus monkeys.
“Thus, despite the marked LBM reduction following CR in some species, CR delays age-associated muscle dysfunction in D. melanogaster [44] and rhesus monkeys [45], and delays the onset of sarcopenia in the latter [46].”
From Resistance Training Prevents Muscle Loss Induced by Caloric Restriction in Obese Elderly Individuals: A Systematic Review and Meta-Analysis (2018) · cites this paper as [46]
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
Invited Review: Aging and sarcopenia
Doherty, T. J. (2003) · Journal of Applied Physiology · doi:10.1152/japplphysiol.00347.2003 · Cited by 1,764 · see citing works
The healthcare costs of sarcopenia in the United States
Janssen, I., Shepard, D. S., Katzmarzyk, P. T., & Roubenoff, R. (2004) · Journal of the American Geriatrics Society · doi:10.1111/j.1532-5415.2004.52014.x · Cited by 1,546 · see citing works
The retardation of aging and disease by dietary restriction
(1989) · Choice Reviews Online · doi:10.5860/choice.26-5101 · Cited by 1,477 · see citing works
Skeletal Muscle Cutpoints Associated with Elevated Physical Disability Risk in Older Men and Women
Janssen, I. (2004) · American Journal of Epidemiology · doi:10.1093/aje/kwh058 · Cited by 1,190 · see citing works
Morley, J. E., Baumgartner, R., Roubenoff, R., Mayer, J., & Nair, K. S. (2001) · Journal of Laboratory and Clinical Medicine · doi:10.1067/mlc.2001.113504 · Cited by 938 · see citing works
Katznelson, L., Finkelstein, J. S., Schoenfeld, D. A., Rosenthal, D. I., Anderson, E. J., & Klibanski, A. (1996) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jcem.81.12.8954042 · Cited by 791 · see citing works
Effects of diet restriction on life span and age-related changes in dogs
Kealy, R. D., Lawler, D. F., Ballam, J. M., Mantz, S. L., Biery, D. N., Greeley, E. H., Lust, G., Segre, M., Smith, G. K., & Stowe, H. D. (2002) · Journal of the American Veterinary Medical Association · doi:10.2460/javma.2002.220.1315 · Cited by 617 · see citing works
Muscle tissue changes with aging
Volpi, E., Nazemi, R., & Fujita, S. (2004) · Current Opinion in Clinical Nutrition and Metabolic Care · doi:10.1097/01.mco.0000134362.76653.b2 · Cited by 569 · see citing works
Satellite cell content is specifically reduced in type II skeletal muscle fibers in the elderly
Verdijk, L. B., Koopman, R., Schaart, G., Meijer, K., Savelberg, H. H. C. M., & van Loon, L. J. C. (2007) · American Journal of Physiology-Endocrinology and Metabolism · doi:10.1152/ajpendo.00278.2006 · Cited by 489 · see citing works
Brodsky, I. G., Balagopal, P., & Nair, K. S. (1996) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jcem.81.10.8855787 · Cited by 444 · see citing works
Insulin resistance of muscle protein metabolism in aging
Rasmussen, B. B., Fujita, S., Wolfe, R. R., Mittendorfer, B., Roy, M., Rowe, V. L., & Volpi, E. (2006) · The FASEB Journal · doi:10.1096/fj.05-4607fje · Cited by 402 · see citing works
Apoptosis in skeletal muscle with aging
Dirks, A., & Leeuwenburgh, C. (2002) · American Journal of Physiology-Regulatory, Integrative and Comparative Physiology · doi:10.1152/ajpregu.00458.2001 · Cited by 377 · see citing works
Interventions for sarcopenia and muscle weakness in older people
Borst, S. E. (2004) · Age and Ageing · doi:10.1093/ageing/afh201 · Cited by 349 · see citing works
Skeletal muscle apoptosis, sarcopenia and frailty at old age
Marzetti, E., & Leeuwenburgh, C. (2006) · Experimental Gerontology · doi:10.1016/j.exger.2006.08.011 · Cited by 346 · see citing works
Catabolism of aging: is it an inflammatory process?
Roubenoff, R. (2003) · Current Opinion in Clinical Nutrition & Metabolic Care · doi:10.1097/01.mco.0000068965.34812.62 · Cited by 307 · see citing works
Sarcopenia: Effects on Body Composition and Function
Roubenoff, R. (2003) · The Journals of Gerontology Series A: Biological Sciences and Medical Sciences · doi:10.1093/gerona/58.11.m1012 · Cited by 282 · see citing works
Insulin resistance: a contributing factor to age-related muscle mass loss?
Guillet, C., & Boirie, Y. (2005) · Diabetes & Metabolism · doi:10.1016/s1262-3636(05)73648-x · Cited by 237 · see citing works
Dietary restriction increases insulin sensitivity and lowers blood glucose in rhesus monkeys
Kemnitz, J. W., Roecker, E. B., Weindruch, R. H., Elson, D. F., Baum, S. T., & Bergman, R. N. (1994) · American Journal of Physiology-Endocrinology and Metabolism · doi:10.1152/ajpendo.1994.266.4.e540 · Cited by 236 · see citing works
Self-citationKemnitz, 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-citationWeindruch, R. H. (1996) · Scientific American · doi:10.1038/scientificamerican0196-46 · Cited by 216 · see citing works
Self-citationApoptosis in muscle atrophy: Relevance to sarcopenia
Dupont‐Versteegden, E. E. (2005) · Experimental Gerontology · doi:10.1016/j.exger.2005.04.003 · Cited by 207 · see citing works
Dietary restriction and aging in rhesus monkeys: the University of Wisconsin study
Ramsey, J. J., Colman, R. J., Binkley, N., Christensen, J. D., Gresl, T. A., Kemnitz, J. W., & Weindruch, R. H. (2000) · Experimental Gerontology · doi:10.1016/s0531-5565(00)00166-2 · Cited by 199 · see citing works
Self-citationThe Evolution of the Antiaging Action of Dietary Restriction: A Hypothesis
Masoro, E. J., & Austad, S. N. (1996) · The Journals of Gerontology Series A · doi:10.1093/gerona/51a.6.b387 · Cited by 192 · see citing works
Dirks, A. J., & Leeuwenburgh, C. (2004) · Free Radical Biology and Medicine · doi:10.1016/j.freeradbiomed.2003.10.003 · Cited by 190 · see citing works
Mitochondrial DNA mutations, energy metabolism and apoptosis in aging muscle
Dirks, A. J., Hofer, T., Marzetti, E., Pahor, M., & Leeuwenburgh, C. (2006) · Ageing Research Reviews · doi:10.1016/j.arr.2006.03.002 · Cited by 169 · see citing works
Alway, S. E., Degens, H., Krishnamurthy, G., & Smith, C. A. S. (2002) · American Journal of Physiology-Cell Physiology · doi:10.1152/ajpcell.00598.2001 · Cited by 164 · see citing works
Caloric restriction reduces fiber loss and mitochondrial abnormalities in aged rat muscle
Aspnes, L. E., Lee, C. M., Weindruch, R. H., Chung, S. S., Roecker, E. B., & Aiken, J. M. (1997) · The FASEB Journal · doi:10.1096/fasebj.11.7.9212081 · Cited by 163 · see citing works
Self-citationThe Role of Apoptosis in Age-Related Skeletal Muscle Atrophy
Dirks, A. J., & Leeuwenburgh, C. (2005) · Sports Medicine · doi:10.2165/00007256-200535060-00002 · Cited by 153 · see citing works
Yu, B. (1998) · CRC Press eBooks · doi:10.1201/b14256 · Cited by 147 · see citing works
Holloszy, J. O. (2000) · PubMed · Cited by 117 · see citing works
Melton, L. J., Khosla, S., & Riggs, B. L. (2000) · Mayo Clinic Proceedings · doi:10.1016/s0025-6196(19)30635-4 · Cited by 114 · see citing works
Early‐onset calorie restriction conserves fiber number in aging rat skeletal muscle
McKiernan, S. H., Bua, E. A., McGorray, J., & Aiken, J. M. (2004) · The FASEB Journal · doi:10.1096/fj.03-0667fje · Cited by 89 · see citing works
CAT scans, PET scans, and genomic scans
Rao, D. C. (1998) · Genetic Epidemiology · doi:10.1002/(sici)1098-2272(1998)15:1 · Cited by 80 · see citing works
Muscle mass loss in Rhesus monkeys: Age of onset
Colman, R. J., McKiernan, S. H., Aiken, J. M., & Weindruch, R. H. (2005) · Experimental Gerontology · doi:10.1016/j.exger.2005.05.001 · Cited by 64 · see citing works
Self-citationThe effect of dietary restriction on body composition in adult male and female rhesus macaques
Colman, R. J., Roecker, E. B., Ramsey, J. J., & Kemnitz, J. W. (1998) · Aging Clinical and Experimental Research · doi:10.1007/bf03339642 · Cited by 58 · see citing works
Self-citationBua, E. A., McKiernan, S. H., & Aiken, J. M. (2004) · The FASEB Journal · doi:10.1096/fj.03-0668fje · Cited by 57 · see citing works
Nuttall, G. A., Santrach, P. J., Oliver, W. C., et al. (2000) · Mayo Clinic Proceedings · doi:10.4065/75.1.10 · Cited by 54 · see citing works
Body Fat Distribution With Long-Term Dietary Restriction in Adult Male Rhesus Macaques
Colman, R. J., Ramsey, J. J., Roecker, E. B., Havighurst, T. C., Hudson, J. C., & Kemnitz, J. W. (1999) · The Journals of Gerontology Series A · doi:10.1093/gerona/54.7.b283 · Cited by 47 · see citing works
Self-citationAndrogen replacement therapy to reverse and/or prevent age-associated sarcopenia in men
Tenover, J. L. (1998) · Baillière s Clinical Endocrinology and Metabolism · doi:10.1016/s0950-351x(98)80153-5 · Cited by 40 · see citing works
Androgens and body composition in the aging male.
Moretti, C., Frajese, G. V., Guccione, L., Wannenes, F., Martino, M. U. D., Fabbri, A., & Frajese, G. (2005) · PubMed · Cited by 39 · see citing works
Beck, C. S. (2000) · Mayo Clinic Proceedings · doi:10.4065/75.1.3 · Cited by 27 · see citing works
Flagged first, then by citations
Research works printed but not linked: 2
- Allison DB, Beasley M. Method and computer program for control- ling the family-wise alpha rate in gene association studies involving multiple phenotypes. Genet Epidemiol. 1998;15:87-101.
- Morley JE, Baumgartner RN, Roubenoff R, Mayer J, Nair KS. Sarcopenia. J Lab Clin Med. 2001;137:231-243.
Cited by
Sorted by citations
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-citationAutophagy and the cell biology of age-related disease
Leidal, A. M., Levine, B., & Debnath, J. (2018) · Nature Cell Biology · doi:10.1038/s41556-018-0235-8 · Cited by 424 · see citing works
Of mice and men: the benefits of caloric restriction, exercise, and mimetics
Mercken, E. M., Carboneau, B. A., Krzysik-Walker, S. M., & de Cabo, R. (2012) · Ageing Research Reviews · doi:10.1016/j.arr.2011.11.005 · Cited by 318 · see citing works
Calorie restriction and prevention of age‐associated chronic disease
Omodei, D., & Fontana, L. (2011) · FEBS Letters · doi:10.1016/j.febslet.2011.03.015 · Cited by 293 · see citing works
Caloric Restriction and Aging: Studies in Mice and Monkeys
Anderson, R. M., Shanmuganayagam, D., & Weindruch, R. (2009) · Toxicologic Pathology · doi:10.1177/0192623308329476 · Cited by 276 · see citing works
Self-citationCalorie Restriction and Aging in Humans
Flanagan, E. W., Most, J., Mey, J. T., & Redman, L. M. (2020) · Annual Review of Nutrition · doi:10.1146/annurev-nutr-122319-034601 · Cited by 239 · see citing works
Martens, C. R., Rossman, M. J., Mazzo, M. R., Jankowski, L. R., Nagy, E. E., Denman, B. A., Richey, J. J., Johnson, S. A., Ziemba, B. P., Wang, Y., et al. (2020) · GeroScience · doi:10.1007/s11357-020-00156-6 · Cited by 182 · see citing works
Optimal body weight for health and longevity: bridging basic, clinical, and population research
Fontana, L., & Hu, F. B. (2014) · Aging Cell · doi:10.1111/acel.12207 · Cited by 157 · see citing works
Sardeli, A. V., Komatsu, T. R., Mori, M. A., Gáspari, A. F., & Chacon-Mikahil, M. P. T. (2018) · Nutrients · doi:10.3390/nu10040423 · Cited by 138 · see citing works
“melanogaster [44] and rhesus monkeys [45], and delays the onset of sarcopenia in the latter [46].”
BackgroundCaloric 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
Autophagy as a Potential Target for Sarcopenia: AUTOPHAGY REGULATION IN SARCOPENIA
Fan, J., Kou, X., Jia, S., Yang, X., Yang, Y., & Chen, N. (2016) · Journal of Cellular Physiology · doi:10.1002/jcp.25260 · Cited by 101 · see citing works
Kastman, E. K., Willette, A. A., Coe, C. L., Bendlin, B. B., Kosmatka, K. J., McLaren, D. G., Xu, G., Canu, E., Field, A. S., Alexander, A. L., et al. (2010) · Journal of Neuroscience · doi:10.1523/jneurosci.0835-10.2010 · Cited by 85 · see citing works
Self-citationRegulation of mRNA Translation as a Conserved Mechanism of Longevity Control
Mehta, R., Chandler-Brown, D., Ramos, F. J., Shamieh, L. S., & Kaeberlein, M. (2010) · Advances in Experimental Medicine and Biology · doi:10.1007/978-1-4419-7002-2_2 · Cited by 44 · see citing works
Kastman, E. K., Willette, A. A., Coe, C. L., Bendlin, B. B., Kosmatka, K. J., McLaren, D. G., Xu, G., Canu, E., Field, A. S., Alexander, A. L., et al. (2012) · The Journal of Neuroscience · doi:10.1523/jneurosci.2553-12.2012 · Cited by 40 · see citing works
Self-citation
- Authors
- Colman, R. J., Beasley, T. M., Allison, D. B., & Weindruch, R.
- Affiliations
- University of Wisconsin–Madison (US)
- University of Alabama at Birmingham (US)
- William S. Middleton Memorial Veterans Hospital (US)
- Corresponding author
- Colman, R. J.
- Venue
- The Journals of Gerontology Series A: Biological Sciences and Medical Sciences
- Publisher
- Oxford University Press (OUP)
- Published
- 2008-06-01
- Volume
- 63
- Issue
- 6
- Pages
- 556-559
- ISSN
- 1079-5006 (ISSN-L)
- 1758-535X
- PMC
- PMC2812805
- OpenAlex
- W2121234713
- Cited by
- 141
- References
- 41
- Citations by year
- 2026: 2 · 2024: 3 · 2023: 4 · 2022: 2 · 2021: 2 · 2020: 9 · 2019: 7 · 2018: 11 · 2017: 6 · 2016: 5 · 2015: 5 · 2014: 8 · 2013: 14 · 2012: 12
- FWCI
- 11.35
- Type
- journal article
- Language
- en
- Open access
- bronze
- doi.org
- Locations
- The Journals of Gerontology Series A (publishedVersion)
- PubMed (publishedVersion)
- PubMed Central (acceptedVersion)
- Funders
- University of Wisconsin-Madison (RR020141-01, RR15459-01)
- National Institute on Aging (P01AG011915)
- National Center for Research Resources (C06RR020141, RR 15459-01, C06RR015459, RR 020141-01, P51RR000167)
- Topics
- Health Sciences › Medicine › Physiology › Nutrition and Health in Aging
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Aging › Genetics, Aging, and Longevity in Model Organisms
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Muscle Physiology and Disorders
- Keywords
- sarcopenia, dietary restriction, caloric restriction, rhesus monkeys, skeletal muscle mass, aging, nonhuman primate model, muscle mass loss, healthspan
- MeSH terms
- Animals, Body Composition, Macaca mulatta, Male, Muscle, Skeletal, 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
