Computed tomographic measurements of thigh muscle cross-sectional area and attenuation coefficient predict hip fracture: the health, aging, and body composition study
Open accessAbstract
Fatty infiltration of muscle, myosteatosis, increases with age and results in reduced muscle strength and function and increased fall risk. However, it is unknown if increased fatty infiltration of muscle predisposes to hip fracture. We measured the mean Hounsfield unit (HU) of the lean tissue within the midthigh muscle bundle (thigh muscle HU, an indicator of intramuscular fat), its cross-sectional area (CSA, a measure of muscle mass) by computed tomography (CT), bone mineral density (BMD) of the hip and total-body percent fat by dual X-ray absorptiometry (DXA), isokinetic leg extensor strength, and the Short Physical Performance Battery (SPPB) in 2941 white and black women and men aged 70 to 79 years. Sixty-three hip fractures were validated during 6.6 years of follow-up. Proportional hazards regression analysis was used to assess the relative risk (RR) of hip fracture across variations in thigh muscle attenuation, CSA, muscle strength, and physical function for hip fracture. In models adjusted by age, race, gender, body mass index, and percentage fat, decreased thigh muscle HU resulted in increased risk of hip fracture [RR/SD = 1.58; 95% confidence interval (CI) 1.10-1.99], an association that continued to be significant after further adjustment for BMD. In models additionally adjusted by CSA, muscle strength, and SPPB score, decreased thigh muscle HU but none of the other muscle parameters continued to be associated with an increased risk of hip fracture (RR/SD = 1.42; 95% CI 1.03-1.97). Decreased thigh muscle HU, a measure of fatty infiltration of muscle, is associated with increased risk of hip fracture and appears to account for the association between reduced muscle strength, physical performance, and muscle mass and risk of hip fracture. This characteristic captures a physical characteristic of muscle tissue that may have importance in hip fracture etiology.
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?
In both the Health ABC and AGES studies, even when controlling for body composition, muscle attenuation was associated with increased risk of fracture.
“In both studies, even when controlling for body composition, the muscle attenuation was associated with increased risk of fracture (Lang et al., 2010; Johannesdottir et al., 2012; Frank-Wilson et al., 2018).”
From Myosteatosis in the Context of Skeletal Muscle Function Deficit: An Interdisciplinary Workshop at the National Institute on Aging (2020) · cites this paper as Lang et al., 2010
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
Guralnik, J. M., Simonsick, E. M., Ferrucci, L., Glynn, R. J., Berkman, L. F., Blazer, D. G., Scherr, P. A., & Wallace, R. B. (1994) · Journal of Gerontology · doi:10.1093/geronj/49.2.m85 · Cited by 9,792 · see citing works
Goodpaster, B. H., Park, S. W., Harris, T. B., Kritchevsky, S. B., Nevitt, M., Schwartz, A. V., Simonsick, E. M., Tylavsky, F. A., Visser, M., Newman, A. B., et al. (2006) · The Journals of Gerontology Series A: Biological Sciences and Medical Sciences · doi:10.1093/gerona/61.10.1059 · Cited by 3,083 · cited 2× · see citing works
“The chronic disease index((10)) was assessed as the total number of 11 chronic health conditions identified using self-report andmedications brought to the clinic and recorded as part of the examination.”
BackgroundMethodSelf-citationGuralnik, J. M., Ferrucci, L., Pieper, C. F., Leveille, S. G., Markides, K. S., Ostir, G. V., Studenski, S., Berkman, L. F., & Wallace, R. B. (2000) · The Journals of Gerontology Series A: Biological Sciences and Medical Sciences · doi:10.1093/gerona/55.4.m221 · Cited by 2,898 · see citing works
(1987) · PubMed · Cited by 2,657 · see citing works
Visser, M., Goodpaster, B. H., Kritchevsky, S. B., Newman, A. B., Nevitt, M., Rubin, S. M., Simonsick, E. M., Harris, T. B., & Study, F. T. H. A. (2005) · The Journals of Gerontology Series A: Biological Sciences and Medical Sciences · doi:10.1093/gerona/60.3.324 · Cited by 1,403 · see citing works
Self-citationAttenuation of skeletal muscle and strength in the elderly: the Health ABC Study
Goodpaster, B. H., Carlson, C. L., Visser, M., Kelley, D. E., Scherzinger, A., Harris, T. B., Stamm, E., & Newman, A. B. (2001) · Journal of Applied Physiology · doi:10.1152/jappl.2001.90.6.2157 · Cited by 1,226 · see citing works
Self-citationMuscle weakness and falls in older adults: a systematic review and meta-analysis
Moreland, J. D., Richardson, J. A., Goldsmith, C. H., & Clase, C. M. (2004) · Journal of the American Geriatrics Society · doi:10.1111/j.1532-5415.2004.52310.x · Cited by 988 · see citing works
Goodpaster, B. H., Kelley, D. E., Thaete, F. L., He, J., & Ross, R. (2000) · Journal of Applied Physiology · doi:10.1152/jappl.2000.89.1.104 · Cited by 956 · see citing works
Visser, M., Kritchevsky, S. B., Goodpaster, B. H., Newman, A. B., Nevitt, M., Stamm, E., & Harris, T. B. (2002) · Journal of the American Geriatrics Society · doi:10.1046/j.1532-5415.2002.50217.x · Cited by 845 · see citing works
Self-citationObesity, Regional Body Fat Distribution, and the Metabolic Syndrome in Older Men and Women
Goodpaster, B. H., Krishnaswami, S., Harris, T. B., Katsiaras, A., Kritchevsky, S. B., Simonsick, E. M., Nevitt, M., Holvoet, P., & Newman, A. B. (2005) · Archives of Internal Medicine · doi:10.1001/archinte.165.7.777 · Cited by 637 · see citing works
Self-citationHsu, Y.-H., Venners, S. A., Terwedow, H. A., Feng, Y., Niu, T., Li, Z., Laird, N., Brain, J. D., Cummings, S. R., Bouxsein, M. L., et al. (2006) · The American Journal of Clinical Nutrition · doi:10.1093/ajcn/83.1.146 · Cited by 537 · see citing works
Self-citationSimonsick, E. M., Newman, A. B., Nevitt, M. C., Kritchevsky, S. B., Ferrucci, L., Guralnik, J. M., Harris, T. B., & for the Health ABC Study Group (2001) · The Journals of Gerontology Series A · doi:10.1093/gerona/56.10.m644 · Cited by 478 · see citing works
Self-citationAdipogenesis and aging: does aging make fat go MAD
Kirkland, J. L., Tchkonia, T., Pirtskhalava, T., Han, J., & Karagiannides, I. (2002) · Experimental Gerontology · doi:10.1016/s0531-5565(02)00014-1 · Cited by 339 · see citing works
Visser, M., Deeg, D. J. H., Lips, P., Harris, T. B., & Bouter, L. M. (2000) · Journal of the American Geriatrics Society · doi:10.1111/j.1532-5415.2000.tb04694.x · Cited by 323 · see citing works
Self-citationMuscle, bone, and the Utah paradigm: a 1999 overview
Frost, H. M. (2000) · Medicine & Science in Sports & Exercise · doi:10.1097/00005768-200005000-00006 · Cited by 158 · see citing works
Cardiovascular diseases and future risk of hip fracture in women
Sennerby, U., Farahmand, B. Y., Ahlbom, A., et al. (2007) · Osteoporosis International · doi:10.1007/s00198-007-0386-0 · Cited by 143 · see citing works
Ducher, G., Courteix, D., Même, S., Magni, C., Viala, J., & Benhamou, C. L. (2005) · Bone · doi:10.1016/j.bone.2005.05.014 · Cited by 140 · see citing works
Diabetes, fracture, and bone fragility
Schwartz, A. V., & Sellmeyer, D. E. (2007) · Current Osteoporosis Reports · doi:10.1007/s11914-007-0025-x · Cited by 102 · see citing works
Rooks, R. N., Simonsick, E. M., Miles, T. P., Newman, A. B., Kritchevsky, S. B., Schulz, R., & Harris, T. B. (2002) · The Journals of Gerontology Series B · doi:10.1093/geronb/57.4.s247 · Cited by 96 · see citing works
Self-citationLang, T., Koyama, A. K., Li, C., Li, J., Lu, Y., Saeed, I., Gazze, E., Keyak, J. H., Harris, T. B., & Cheng, X. (2007) · Bone · doi:10.1016/j.bone.2007.12.002 · Cited by 93 · see citing works
Self-citationDucher, G., Jaffré, C., Arlettaz, A., et al. (2005) · Canadian Journal of Applied Physiology · doi:10.1139/h05-101 · Cited by 83 · see citing works
Study, F. T. H. A., Houston, D. K., Ding, J., Nicklas, B. J., Harris, T. B., Lee, J. S., Nevitt, M. C., Rubin, S. M., Tylavsky, F. A., & Kritchevsky, S. B. (2007) · International Journal of Obesity · doi:10.1038/sj.ijo.0803652 · Cited by 59 · see citing works
Self-citationFat mass and skeletal muscle mass in hip-fracture women: A cross-sectional study
Monaco, M. D., Vallero, F., Monaco, R. D., Tappero, R., & Cavanna, A. (2006) · Maturitas · doi:10.1016/j.maturitas.2006.11.003 · Cited by 26 · see citing works
Cardiovascular diseases and future risk of hip fracture in women. Osteoporos Int
Sennerby, U., Farahmand, B. Y., Ahlbom, A., et al. (2007) · Cited by 23 · see citing works
Fat body mass, leptin and femur bone mineral density in hip-fractured women
Monaco, M. D., Vallero, F., Monaco, R. D., Mautino, F., & Cavanna, A. (2003) · Journal of Endocrinological Investigation · doi:10.1007/bf03349154 · Cited by 22 · see citing works
Flagged first, then by citations
Cited by
Sorted by citations
Sarcopenia with limited mobility: an international consensus
Morley, J. E., Abbatecola, A. M., Argiles, J. M., Baracos, V., Bauer, J., Bhasin, S., Cederholm, T., Stewart Coats, A. J., Cummings, S. R., Evans, W. J., et al. (2011) · Journal of the American Medical Directors Association · doi:10.1016/j.jamda.2011.04.014 · Cited by 1,125 · see citing works
Self-citationMeasurement of skeletal muscle radiation attenuation and basis of its biological variation
Aubrey, J., Esfandiari, N., Baracos, V. E., Buteau, F. A., Frenette, J., Putman, C. T., & Mazurak, V. C. (2014) · Acta Physiologica · doi:10.1111/apha.12224 · Cited by 720 · see citing works
Intermuscular fat: a review of the consequences and causes
Addison, O., Marcus, R. L., LaStayo, P. C., & Ryan, A. S. (2014) · International Journal of Endocrinology · doi:10.1155/2014/309570 · Cited by 656 · see citing works
Cadore, E. L., Casas-Herrero, A., Zambom-Ferraresi, F., Idoate, F., Millor, N., Gómez, M., Rodriguez-Mañas, L., & Izquierdo, M. (2014) · AGE · doi:10.1007/s11357-013-9586-z · Cited by 526 · see citing works
Does nutrition play a role in the prevention and management of sarcopenia?
Robinson, S. M., Reginster, J. Y., Rizzoli, R., Shaw, S. C., Kanis, J. A., Bautmans, I., Bischoff-Ferrari, H., Bruyère, O., Cesari, M., Dawson-Hughes, B., et al. (2018) · Clinical Nutrition · doi:10.1016/j.clnu.2017.08.016 · Cited by 491 · see citing works
Correa-de-Araujo, R., Addison, O., Miljkovic, I., Goodpaster, B. H., Bergman, B. C., Clark, R. V., Elena, J. W., Esser, K. A., Ferrucci, L., Harris-Love, M. O., et al. (2020) · Frontiers in Physiology · doi:10.3389/fphys.2020.00963 · Cited by 468 · see citing works
Preserving Healthy Muscle during Weight Loss
Cava, E., Yeat, N. C., & Mittendorfer, B. (2017) · Advances in Nutrition · doi:10.3945/an.116.014506 · Cited by 452 · see citing works
Fatty infiltration of skeletal muscle: mechanisms and comparisons with bone marrow adiposity
Hamrick, M. W., McGee-Lawrence, M. E., & Frechette, D. M. (2016) · Frontiers in Endocrinology · doi:10.3389/fendo.2016.00069 · Cited by 372 · see citing works
Aging human body: changes in bone, muscle and body fat with consequent changes in nutrient intake
JafariNasabian, P., Inglis, J. E., Reilly, W., Kelly, O. J., & Ilich, J. Z. (2017) · Journal of Endocrinology · doi:10.1530/joe-16-0603 · Cited by 310 · see citing works
Obesity and fracture in men and women: an epidemiologic perspective
Nielson, C. M., Srikanth, P., & Orwoll, E. S. (2012) · Journal of Bone and Mineral Research · doi:10.1002/jbmr.1486 · Cited by 253 · see citing works
Liu, C., Wong, P. Y., Chung, Y. L., Chow, S. K., Cheung, W. H., Law, S. W., Chan, J. C. N., & Wong, R. M. Y. (2023) · Obesity Reviews · doi:10.1111/obr.13534 · Cited by 247 · see citing works
Interactions between Muscle and Bone—Where Physics Meets Biology
Herrmann, M., Engelke, K., Ebert, R., Müller-Deubert, S., Rudert, M., Ziouti, F., Jundt, F., Felsenberg, D., & Jakob, F. (2020) · Biomolecules · doi:10.3390/biom10030432 · Cited by 197 · see citing works
Quantitative imaging techniques for the assessment of osteoporosis and sarcopenia
Guerri, S., Mercatelli, D., Aparisi Gómez, M. P., Napoli, A., Battista, G., Guglielmi, G., & Bazzocchi, A. (2018) · Quantitative Imaging in Medicine and Surgery · doi:10.21037/qims.2018.01.05 · Cited by 169 · see citing works
Miljkovic, I., Kuipers, A. L., Cauley, J. A., Prasad, T., Lee, C. G., Ensrud, K. E., Cawthon, P. M., Hoffman, A. R., Dam, T.-T., Gordon, C. L., et al. (2015) · The Journals of Gerontology Series A: Biological Sciences and Medical Sciences · doi:10.1093/gerona/glv027 · Cited by 144 · see citing works
Self-citationLipid metabolism in sarcopenia
Al Saedi, A., Debruin, D. A., Hayes, A., & Hamrick, M. (2022) · Bone · doi:10.1016/j.bone.2022.116539 · Cited by 140 · see citing works
The advantages and limitations of cross-sectional body composition analysis
MacDonald, A. J., Greig, C. A., & Baracos, V. (2011) · Current Opinion in Supportive & Palliative Care · doi:10.1097/spc.0b013e32834c49eb · Cited by 101 · see citing works
Ilich, J. Z., Inglis, J. E., Kelly, O. J., & McGee, D. L. (2015) · Osteoporosis International · doi:10.1007/s00198-015-3186-y · Cited by 100 · see citing works
Martinikorena, I., Martínez-Ramírez, A., Gómez, M., Lecumberri, P., Casas-Herrero, A., Cadore, E. L., Millor, N., Zambom-Ferraresi, F., Idoate, F., & Izquierdo, M. (2016) · Journal of the American Medical Directors Association · doi:10.1016/j.jamda.2015.09.015 · Cited by 97 · see citing works
Prospective views for whey protein and/or resistance training against age-related sarcopenia
Liao, Y., Peng, Z., Chen, L., Zhang, Y., Cheng, Q., Nüssler, A. K., Bao, W., Liu, L., & Yang, W. (2019) · Aging and Disease · doi:10.14336/ad.2018.0325 · Cited by 68 · see citing works
Anderson, D. E., Quinn, E., Parker, E., Allaire, B. T., Muir, J. W., Rubin, C. T., Magaziner, J., Hannan, M. T., Bouxsein, M. L., & Kiel, D. P. (2016) · The Journals of Gerontology Series A: Biological Sciences and Medical Sciences · doi:10.1093/gerona/glv185 · Cited by 67 · see citing works
Marcus, R. L., Addison, O., & LaStayo, P. C. (2013) · The Journal of nutrition, health and aging · doi:10.1007/s12603-012-0377-5 · Cited by 65 · see citing works
Perna, S., Spadaccini, D., Nichetti, M., Avanzato, I., Faliva, M. A., & Rondanelli, M. (2018) · Journal of Aging Research · doi:10.1155/2018/6147426 · Cited by 65 · see citing works
Idoate, F., Cadore, E. L., Casas-Herrero, A., Zambom-Ferraresi, F., Marcellán, T., de Gordoa, A. R., Rodriguez-Mañas, L., Bastarrika, G., Marques, M. C., Martínez-Velilla, N., et al. (2015) · European Radiology · doi:10.1007/s00330-014-3555-5 · Cited by 56 · see citing works
Zhao, Q., Zmuda, J. M., Kuipers, A. L., Jonnalagadda, P., Bunker, C. H., Patrick, A. L., Youk, A. O., & Miljkovic, I. (2016) · Age and Ageing · doi:10.1093/ageing/afw062 · Cited by 38 · see citing works
Frank-Wilson, A. W., Chalhoub, D., Figueiredo, P., Jónsson, P. V., Siggeirsdóttir, K., Sigurdsson, S., Eiriksdottir, G., Guðnason, V., Launer, L., Harris, T. B., et al. (2018) · The Journals of Gerontology Series A · doi:10.1093/gerona/glx262 · Cited by 37 · see citing works
Self-citationIlich, J. Z. (2017) · Journal of the American Medical Directors Association · doi:10.1016/j.jamda.2017.05.001 · Cited by 15 · see citing works
Organotypic cultures as aging associated disease models
Sanchez, M. M., Bagdasarian, I. A., Darch, W., & Morgan, J. T. (2022) · Aging · doi:10.18632/aging.204361 · Cited by 12 · see citing works
- Authors
- Lang, T., Cauley, J. A., Tylavsky, F., Bauer, D., Cummings, S., & Harris, T. B.
- Affiliations
- University of California, San Francisco (US)
- University of Pittsburgh (US)
- University of Tennessee Health Science Center (US)
- California Pacific Medical Center (US)
- National Institutes of Health (US)
- Corresponding author
- Lang, Thomas
- Venue
- Journal of Bone and Mineral Research
- Publisher
- Oxford University Press (OUP)
- Published
- 2010-01-27
- Volume
- 25
- Issue
- 3
- Pages
- 513-519
- ISSN
- 0884-0431 (ISSN-L)
- 1523-4681
- PMC
- PMC3153392
- OpenAlex
- W2057527999
- Cited by
- 371
- References
- 25
- Citations by year
- 2026: 13 · 2025: 16 · 2024: 13 · 2023: 15 · 2022: 32 · 2021: 29 · 2020: 27 · 2019: 26 · 2018: 26 · 2017: 29 · 2016: 30 · 2015: 25 · 2014: 25 · 2013: 25 · 2012: 14
- FWCI
- 13.64
- Type
- journal article
- Language
- en
- Open access
- green
- www.ncbi.nlm.nih.gov
- Licence
- Locations
- Journal of Bone and Mineral Research (publishedVersion)
- Europe PMC (PubMed Central) (publishedVersion, cc-by)
- PubMed Central (publishedVersion, cc-by)
- PubMed (publishedVersion)
- D-Scholarship@Pitt (University of Pittsburgh) (acceptedVersion)
- eScholarship (California Digital Library) (submittedVersion)
- eScholarship (California Digital Library) (submittedVersion, cc-by)
- Funders
- National Institutes of Health
- National Institute on Aging (N01‐AG‐6–2101, N01AG62106, N01-AG-62103)
- Topics
- Health Sciences › Medicine › Orthopedics and Sports Medicine › Bone health and osteoporosis research
- Health Sciences › Medicine › Physiology › Nutrition and Health in Aging
- Health Sciences › Medicine › Surgery › Hip and Femur Fractures
- Keywords
- hip fracture, thigh muscle cross-sectional area, intramuscular fat, myosteatosis, Hounsfield units, muscle attenuation, muscle mass, muscle strength, physical performance, bone mineral density, older adults, fall risk, aging
- MeSH terms
- Age Factors, Aged, Body Composition, Female, Health, Hip Fractures, Humans, Male, Predictive Value of Tests, Prognosis, Risk Factors, Tomography, X-Ray Computed, Absorptiometry, Photon, Bone Density, Body Mass Index, Muscle, Skeletal, Body Size
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
