The DOI matches its Crossref record; 35 of the 35 references it cites were found in a registry or an index.
Relationship of Interleukin-6 and Tumor Necrosis Factor- With Muscle Mass and Muscle Strength in Elderly Men and Women: The Health ABC Study
Abstract
BACKGROUND: A decline in muscle mass and muscle strength characterizes normal aging. As clinical and animal studies show a relationship between higher cytokine levels and low muscle mass, the aim of this study was to investigate whether markers of inflammation are associated with muscle mass and strength in well-functioning elderly persons. METHODS: We used baseline data (1997-1998) of the Health, Aging, and Body Composition (Health ABC) Study on 3075 black and white men and women aged 70-79 years. Midthigh muscle cross-sectional area (computed tomography), appendicular muscle mass (dual-energy x-ray absorptiometry), isokinetic knee extensor strength (KinCom), and isometric grip strength were measured. Plasma levels of interleukin-6 (IL-6) and tumor necrosis factor-alpha (TNF-alpha) were assessed by enzyme-linked immunosorbent assay (ELISA). RESULTS: Higher cytokine levels were generally associated with lower muscle mass and lower muscle strength. The most consistent relationship across the gender and race groups was observed for IL-6 and grip strength: per SD increase in IL-6, grip strength was 1.1 to 2.4 kg lower (p <.05) after adjustment for age, clinic site, health status, medications, physical activity, smoking, height, and body fat. An overall measure of elevated cytokine level was created by combining the levels of IL-6 and TNF-alpha. With the exception of white men, elderly persons having high levels of IL-6 (>1.80 pg/ml) as well as high levels of TNF-alpha (>3.20 pg/ml) had a smaller muscle area, less appendicular muscle mass, a lower knee extensor strength, and a lower grip strength compared to those with low levels of both cytokines. CONCLUSIONS: Higher plasma concentrations of IL-6 and TNF-alpha are associated with lower muscle mass and lower muscle strength in well-functioning older men and women. Higher cytokine levels, as often observed in healthy older persons, may contribute to the loss of muscle mass and strength that accompanies aging.
Overview
Integrity signals
Registry
Cites
Statistics
Verification
Claims the paper makes
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?
In the citing paper
“higher levels of inflammatory markers in blood are associated with a greater loss of muscle mass and strength, accelerated loss of mobility, lower-extremity performance and physical activity, and depression in older individuals”
From Inflammageing: chronic inflammation in ageing, cardiovascular disease, and frailty (2018) · cites this paper as [226]
In the citing paper
“Adipose tissue secretes proinflammatory cytokines such as interleukin 6 (IL-6), interleukin 1 (IL-1), and tumor necrosis factor alpha (TNF-α).20”
From Imaging of Sarcopenia in Type 2 Diabetes Mellitus (2024) · cites this paper as [20]
In the citing paper
“Altered adipose tissue growth and function lead to fluctuations in the concentrations of adipokines and cytokines, causing chronic inflammation, mitochondrial impairment, disruption of the insulin signaling pathway in the skeletal muscle, and eventual muscular atrophy.”
From Imaging of Sarcopenia in Type 2 Diabetes Mellitus (2024) · cites this paper as [20]
In the citing paper
“Other factors that are known to contribute to sarcopenia include reductions in circulating sex hormones [8], physical inactivity [9], low grade inflammation [10,11], impairments to neuromuscular junctions [12], and reduced muscle stem cell (i.e., satellite cell) number and function [13].”
From Potential Roles of n-3 PUFAs during Skeletal Muscle Growth and Regeneration (2018) · cites this paper as [10]
In the citing paper
“For instance, circulating growth factors, such as GDF11 and myostatin, as well as inflammatory markers, such as TNF-α and IL-6, increase with age, impairing the regenerative capacity of satellite cells in human skeletal muscle [10,115].”
From Potential Roles of n-3 PUFAs during Skeletal Muscle Growth and Regeneration (2018) · cites this paper as [10]
In the citing paper
“Circulating systemic factors, such as hormones and inflammatory marker, can positively and negatively influence satellite cell activation.”
From Potential Roles of n-3 PUFAs during Skeletal Muscle Growth and Regeneration (2018) · cites this paper as [10]
Citations
Cites
Compendium of Physical Activities: Classification of energy costs of human physical activities
AINSWORTH, B. E., HASKELL, W. L., LEON, A. S., JACOBS, D. R., MONTOYE, H. J., SALLIS, J. F., & PAFFENBARGER, R. S. (1993) · Medicine & Science in Sports & Exercise · doi:10.1249/00005768-199301000-00011 · Cited by 4,102
Elevated C-reactive protein levels in overweight and obese adults
Visser, M. (1999) · JAMA · doi:10.1001/jama.282.22.2131 · Cited by 2,494
Self-citationSubcutaneous Adipose Tissue Releases Interleukin-6, But Not Tumor Necrosis Factor-α,in Vivo1
Mohamed‐Ali, V., Goodrick, S., Rawesh, A., Katz, D. R., Miles, J. M., Yudkin, J. S., Klein, S., & Coppack, S. W. (1997) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jcem.82.12.4450 · Cited by 2,030
Associations of elevated interleukin-6 and C-reactive protein levels with mortality in the elderly
Harris, T. B., Ferrucci, L., Tracy, R. P., Corti, M. C., Wacholder, S., Ettinger, W. H., Heimovitz, H., Cohen, H. J., & Wallace, R. (1999) · The American Journal of Medicine · doi:10.1016/s0002-9343(99)00066-2 · Cited by 1,488
Self-citationMidlife Hand Grip Strength as a Predictor of Old Age Disability
Rantanen, T. (1999) · JAMA · doi:10.1001/jama.281.6.558 · Cited by 1,481
Bastard, J., Jardel, C., Bruckert, É., Blondy, P., Capeau, J., Laville, M., Vidal, H., & Hainque, B. (2000) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jcem.85.9.6839 · Cited by 1,123
Tracy, R. P., Lemaitre, R. N., Psaty, B. M., Ives, D. G., Evans, R. W., Cushman, M., Meilahn, E. N., & Kuller, L. H. (1997) · Arteriosclerosis, Thrombosis, and Vascular Biology · doi:10.1161/01.atv.17.6.1121 · Cited by 836
Serum IL‐6 Level and the Development of Disability in Older Persons
Ferrucci, L., Harris, T. B., Guralnik, J. M., Tracy, R. P., Corti, M., Cohen, H. J., Penninx, B., Pahor, M., Wallace, R., & Havlik, R. J. (1999) · Journal of the American Geriatrics Society · doi:10.1111/j.1532-5415.1999.tb01583.x · Cited by 809
Self-citationSubcutaneous Adipose Tissue Releases Interleukin-6, But Not Tumor Necrosis Factor- , in Vivo
Mohamed-Ali, V. (1997) · Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jc.82.12.4196 · Cited by 717
Roubenoff, R., Roubenoff, R., Cannon, J. G., Kehayias, J. J., Zhuang, H., Dawson‐Hughes, B., Dinarello, C. A., & Rosenberg, I. H. (1994) · Journal of Clinical Investigation · doi:10.1172/jci117244 · Cited by 583
Plasma interleukin-6, tumour necrosis factor α and blood cytokine production in type 2 diabetes
Pickup, J. C., Chusney, G. D., Thomas, S. M., & Burt, D. (2000) · Life Sciences · doi:10.1016/s0024-3205(00)00622-6 · Cited by 566
Tracy, R. P., Psaty, B. M., Macy, E., Bovill, E. G., Cushman, M., Cornell, E. S., & Kuller, L. H. (1997) · Arteriosclerosis, Thrombosis, and Vascular Biology · doi:10.1161/01.atv.17.10.2167 · Cited by 539
Schols, A. M. W. J., Buurman, W. A., den Brekel, A. J. S.-V., Dentener, M. A., & Wouters, E. F. �. (1996) · Thorax · doi:10.1136/thx.51.8.819 · Cited by 520
Drug data coding and analysis in epidemiologic studies
Pahor, M., Chrischilles, E. A., Guralnik, J. M., Brown, S. L., Wallace, R. B., & Carbonin, P. (1994) · European Journal of Epidemiology · doi:10.1007/bf01719664 · Cited by 490
Self-citationThe Association of Plasma IL-6 Levels With Functional Disability in Community-Dwelling Elderly
Cohen, H. J., Pieper, C. F., Harris, T., Rao, K. M. K., & Currie, M. S. (1997) · The Journals of Gerontology Series A: Biological Sciences and Medical Sciences · doi:10.1093/gerona/52a.4.m201 · Cited by 476
Self-citationResistance exercise decreases skeletal muscle tumor necrosis factor α in frail elderly humans
GREIWE, J. S., CHENG, B., RUBIN, D. C., YARASHESKI, K. E., & SEMENKOVICH, C. F. (2001) · The FASEB Journal · doi:10.1096/fj.00-0274com · Cited by 454
Increase of plasma IL-6 concentration with age in healthy subjects
Wei, J., Xu, H., Davies, J. L., & Hemmings, G. P. (1992) · Life Sciences · doi:10.1016/0024-3205(92)90112-3 · Cited by 402
Anker, S. D. (1999) · European Heart Journal · doi:10.1053/euhj.1998.1446 · Cited by 374
Seidell, J. C., Oosterlee, A., Thijssen, M. A. O., Burema, J., Deurenberg, P., Hautvast, J. G. A. J., & Ruijs, J. H. J. (1987) · American Journal of Clinical Nutrition · doi:10.1093/ajcn/45.1.7 · Cited by 315
Erren, M., Reinecke, H., Junker, R., Fobker, M., Schulte, H., Schurek, J. O., Kropf, J., Kerber, S., BREITHARDT, G. E., Assmann, G., et al. (1999) · Arteriosclerosis Thrombosis and Vascular Biology · doi:10.1161/01.atv.19.10.2355 · Cited by 306
Interleukin-6 Induces Skeletal Muscle Protein Breakdown in Rats
Goodman, M. N. (1994) · Experimental Biology and Medicine · doi:10.3181/00379727-205-43695 · Cited by 296
Visser, M., Harris, T. B., Langlois, J. A., Hannan, M. T., Roubenoff, R., Felson, D. T., Wilson, P. W. F., & Kiel, D. P. (1998) · The Journals of Gerontology Series A · doi:10.1093/gerona/53a.3.m214 · Cited by 259
Self-citationTumor necrosis factor induces skeletal muscle protein breakdown in rats
Goodman, M. N. (1991) · American Journal of Physiology-Endocrinology and Metabolism · doi:10.1152/ajpendo.1991.260.5.e727 · Cited by 250
C-Reactive Protein, Cardiovascular Risk Factors, and Mortality in a Prospective Study in the Elderly
Strandberg, T. E., & Tilvis, R. S. (2000) · Arteriosclerosis Thrombosis and Vascular Biology · doi:10.1161/01.atv.20.4.1057 · Cited by 246
Longitudinal changes in adult fat-free mass: influence of body weight
Forbes, G. B. (1999) · The American Journal of Clinical Nutrition · doi:10.1093/ajcn/70.6.1025 · Cited by 183
Interleukin-6 and selected plasma proteins in healthy persons of different ages
Häger, K., Machein, U., Krieger, S., Platt, D., Seefried, G., & Bauer, J. (1994) · Neurobiology of Aging · doi:10.1016/0197-4580(94)90066-3 · Cited by 172
Role of cytokines, acute-phase proteins, and chemokinesin the progression of rheumatoid arthritis
Badolato, R., & Oppenheim, J. J. (1996) · Seminars in Arthritis and Rheumatism · doi:10.1016/s0049-0172(96)80041-2 · Cited by 162
Garc�a-Mart�nez, C., López-Soriano, F. J., & Argilés, J. M. A. (1993) · Molecular and Cellular Biochemistry · doi:10.1007/bf00926829 · Cited by 160
Depressed Mood and Body Mass Index as Predictors of Muscle Strength Decline in Old Men
Rantanen, T., Penninx, B. W. J. H., Masaki, K., Lintunen, T., Foley, D., & Guralnik, J. M. (2000) · Journal of the American Geriatrics Society · doi:10.1111/j.1532-5415.2000.tb04717.x · Cited by 122
Charters, Y., & Grimble, R. F. (1989) · Biochemical Journal · doi:10.1042/bj2580493 · Cited by 102
Rao, K. M. K., Pieper, C. F., Currie, M. S., & Cohen, H. J. (1994) · American Journal of Clinical Pathology · doi:10.1093/ajcp/102.6.802 · Cited by 98
Haslett, P. A. J., Hempstead, M., Seidman, C. E., et al. (1997) · AIDS Research and Human Retroviruses · doi:10.1089/aid.1997.13.1047 · Cited by 90
Body composition and metabolic rate in rat during a continuous infusion of cachectin
Hoshino, E., Pichard, C., Greenwood, C. E., Kuo, G. C., Cameron, R., Kurian, R., Kearns, J. P., Allard, J. P., & Jeejeebhoy, K. N. (1991) · American Journal of Physiology-Endocrinology and Metabolism · doi:10.1152/ajpendo.1991.260.1.e27 · Cited by 67
Serum Levels of IL‐6 and Development of Disability in Older Persons
Kuller, L. H. (1999) · Journal of the American Geriatrics Society · doi:10.1111/j.1532-5415.1999.tb01604.x · Cited by 26
Effects of tumor necrosis factor alpha on skeletal muscle amino acid metabolism studied in-vivo.
Tayek, J. A. (1996) · Journal of the American College of Nutrition · doi:10.1080/07315724.1996.10718583 · Cited by 26
Research works printed but not linked: 3
- 1991, American Journal of Physiology -- Legacy Content, 260, E27
- 1991, American Journal of Physiology -- Legacy Content, 260, E727
- Bastard, 2000, Journal of Clinical Endocrinology & Metabolism, 85, 3338, 10.1210/jc.85.9.3338 · DOI
Cited by
Sorted by citations
Fried, L. P., Ferrucci, L., Darer, J., Williamson, J. D., & Anderson, G. (2004) · The Journals of Gerontology Series A: Biological Sciences and Medical Sciences · doi:10.1093/gerona/59.3.m255 · Cited by 4,032
Inflammageing: chronic inflammation in ageing, cardiovascular disease, and frailty
Ferrucci, L., & Fabbri, E. (2018) · Nature Reviews Cardiology · doi:10.1038/s41569-018-0064-2 · Cited by 3,690
Sarcopenia: Aging-Related Loss of Muscle Mass and Function
Larsson, L., Degens, H., Li, M., Salviati, L., Lee, Y. I., Thompson, W., Kirkland, J. L., & Sandri, M. (2019) · Physiological Reviews · doi:10.1152/physrev.00061.2017 · Cited by 1,797
Newman, A. B., Kupelian, V., Visser, M., Simonsick, E. M., Goodpaster, B. H., Kritchevsky, S. B., Tylavsky, F. A., Rubin, S. M., Harris, T. B., & on Behalf of the Health, A. A. B. C. S. I. (2006) · The Journals of Gerontology Series A: Biological Sciences and Medical Sciences · doi:10.1093/gerona/61.1.72 · Cited by 1,692
Self-citationSarcopenic obesity in older adults: aetiology, epidemiology and treatment strategies
Batsis, J. A., & Villareal, D. T. (2018) · Nature Reviews Endocrinology · doi:10.1038/s41574-018-0062-9 · Cited by 1,382
Metadata
- Authors
- Visser, M., Pahor, M., Taaffe, D. R., Goodpaster, B. H., Simonsick, E. M., Newman, A. B., Nevitt, M., & Harris, T. B.
- Affiliations
- Amsterdam UMC Location Vrije Universiteit Amsterdam (NL)
- Vrije Universiteit Amsterdam (NL)
- Corresponding author
- Visser, M.
- Venue
- The Journals of Gerontology Series A: Biological Sciences and Medical Sciences
- Publisher
- Oxford University Press (OUP)
- Published
- 2002-05-01
- Volume
- 57
- Issue
- 5
- Pages
- M326-M332
- ISSN
- 1079-5006 (ISSN-L)
- 1758-535X
- OpenAlex
- W2137646952
- Cited by
- 1,294
- References
- 35
- Citations by year
- 2026: 39 · 2025: 50 · 2024: 67 · 2023: 67 · 2022: 76 · 2021: 82 · 2020: 97 · 2019: 77 · 2018: 75 · 2017: 56 · 2016: 54 · 2015: 61 · 2014: 59 · 2013: 41 · 2012: 49
- FWCI
- 18.41
- Type
- journal article
- Language
- en
- Open access
- closed
- Locations
- The Journals of Gerontology Series A (publishedVersion)
- PubMed (publishedVersion)
- Data Archiving and Networked Services (DANS) (submittedVersion)
- Funders
- National Institutes of Health (5k01ag000851-04)
- National Institute on Aging (N01‐AG‐6–2101, K01-AG-00851, P60AG010484, P60 AG-10484, N01AG62106, N01-AG-62103)
- Topics
- Health Sciences › Medicine › Physiology (medical) › Nutrition and Health in Aging
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Muscle Physiology and Disorders
- Health Sciences › Medicine › Physiology (medical) › Exercise and Physiological Responses
- Keywords
- interleukin-6, TNF-α, muscle mass, muscle strength, aging, inflammation, cytokines, grip strength, quadriceps strength, appendicular skeletal muscle mass, older adults, sex differences, racial differences
- MeSH terms
- Aged, Aging, Female, Humans, Knee, Male, Tumor Necrosis Factor-alpha, Interleukin-6, Muscle, Skeletal, Hand Strength, Black People, White People
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