Effect of Dietary Protein on Bone Loss in Elderly Men and Women: The Framingham Osteoporosis Study
Abstract
Few studies have evaluated protein intake and bone loss in elders. Excess protein may be associated with negative calcium balance, whereas low protein intake has been associated with fracture. We examined the relation between baseline dietary protein and subsequent 4-year change in bone mineral density (BMD) for 391 women and 224 men from the population-based Framingham Osteoporosis Study. BMD (g/cm2) was assessed in 1988-1989 and in 1992-1993 at the femur, spine, and radius. Usual dietary protein intake was determined using a semiquantitative food frequency questionnaire (FFQ) and expressed as percent of energy from protein intake. BMD loss over 4 years was regressed on percent protein intake, simultaneously adjusting for other baseline factors: age, weight, height, weight change, total energy intake, smoking, alcohol intake, caffeine, physical activity, calcium intake, and, for women, current estrogen use. Effects of animal protein on bone loss also were examined. Mean age at baseline (±SD) of 615 participants was 75 years (±4.4; range, 68-91 years). Mean protein intake was 68 g/day (±24.0; range, 14-175 g/day), and mean percent of energy from protein was 16% (±3.4; range, 7-30%). Proportional protein intakes were similar for men and women. Lower protein intake was significantly related to bone loss at femoral and spine sites (p ≤ 0.04) with effects similar to 10 lb of weight. Persons in the lowest quartile of protein intake showed the greatest bone loss. Similar to the overall protein effect, lower percent animal protein also was significantly related to bone loss at femoral and spine BMD sites (all p < 0.01) but not the radial shaft (p = 0.23). Even after controlling for known confounders including weight loss, women and men with relatively lower protein intake had increased bone loss, suggesting that protein intake is important in maintaining bone or minimizing bone loss in elderly persons. Further, higher intake of animal protein does not appear to affect the skeleton adversely in this elderly population.
Integrity signals
Registry
Cites
Statistics
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?
Several epidemiological studies found a positive correlation between higher dietary protein intake and higher bone mass density, slower rate of bone loss, and muscle mass and strength.
“Several epidemiological studies have found a positive correlation between higher dietary protein intake and higher bone mass density 39e41 ; slower rate of bone loss 42 ; and muscle mass and strength.43”
From Evidence-Based Recommendations for Optimal Dietary Protein Intake in Older People: A Position Paper From the PROT-AGE Study Group (2013) · cites this paper as [42]
Cites
Reproducibility and validity of a semiquantitative food frequency questionnaire
WILLETT, W. C., SAMPSON, L., STAMPFER, M. J., ROSNER, B., BAIN, C., WITSCHI, J., HENNEKENS, C. H., & SPEIZER, F. E. (1985) · American Journal of Epidemiology · doi:10.1093/oxfordjournals.aje.a114086 · Cited by 4,274 · see citing works
Risk Factors for Hip Fracture in White Women
Cummings, S. R., Nevitt, M. C., Browner, W. S., Stone, K., Fox, K. M., Ensrud, K. E., Cauley, J., Black, D., & Vogt, T. M. (1995) · New England Journal of Medicine · doi:10.1056/nejm199503233321202 · Cited by 3,595 · see citing works
Total energy intake: implications for epidemiologic analyses.
WILLETT, W., & STAMPFER, M. J. (1986) · American Journal of Epidemiology · doi:10.1093/oxfordjournals.aje.a114366 · Cited by 2,751 · see citing works
RE: “TOTAL ENERGY INTAKE: IMPLICATIONS FOR EPIDEMIOLOGIC ANALYSES”
Palmgren, J., & Kushi, L. H. (1991) · American Journal of Epidemiology · doi:10.1093/oxfordjournals.aje.a115841 · Cited by 2,712 · see citing works
Kanis, J. А., & Kanis, J. А. (1994) · Osteoporosis International · doi:10.1007/bf01622200 · Cited by 2,532 · see citing works
Epidemiological approaches to heart disease: the Framingham study
Dawber, T. R., Meadors, G. F., & Moore, F. E. (1951) · American Journal of Public Health and the Nations Health · doi:10.2105/ajph.41.3.279 · Cited by 2,148 · see citing works
Rimm, E. B., Giovannucci, E. L., Stampfer, M. J., Colditz, G. A., Litin, L. B., & Willett, W. C. (1992) · American Journal of Epidemiology · doi:10.1093/oxfordjournals.aje.a116211 · Cited by 2,104 · see citing works
Dawber, T. R. (1980) · Harvard University Press eBooks · doi:10.4159/harvard.9780674492097 · Cited by 1,962 · see citing works
Dietary supplementation in elderly patients with fractured neck of the femur
Delmi, M., Rapin, C. H., Bengoa, J., Bonjour, J.-P., Vasey, H., & Delmas, P. D. (1990) · The Lancet · doi:10.1016/0140-6736(90)91073-j · Cited by 825 · see citing works
Some health benefits of physical activity. The Framingham Study
Kannel, W. B. (1979) · Archives of Internal Medicine · doi:10.1001/archinte.139.8.857 · Cited by 783 · see citing works
Risk Factors for Longitudinal Bone Loss in Elderly Men and Women: The Framingham Osteoporosis Study
Hannan, M. T., Felson, D. T., Dawson-Hughes, B. F., Tucker, K. L., Cupples, L. A., Wilson, P. W. F., & Kiel, D. P. (2000) · Journal of Bone and Mineral Research · doi:10.1359/jbmr.2000.15.4.710 · Cited by 767 · see citing works
Self-citationPerspectives: How many women have osteoporosis now?
Melton, J. L. (1995) · Journal of Bone and Mineral Research · doi:10.1002/jbmr.5650100202 · Cited by 596 · see citing works
The Effect of Postmenopausal Estrogen Therapy on Bone Density in Elderly Women
Felson, D. T., Zhang, Y., Hannan, M. T., Kiel, D. P., Wilson, P. W. F., & Anderson, J. J. (1993) · New England Journal of Medicine · doi:10.1056/nejm199310143291601 · Cited by 584 · see citing works
Self-citationSebastián, A., Harris, S. T., Ottaway, J. H., Todd, K., & Morris, R. C. (1994) · New England Journal of Medicine · doi:10.1056/nejm199406233302502 · Cited by 578 · see citing works
Schurch, M.-A., Rizzoli, R., Slosman, D., Vadas, L., Vergnaud, P., & Bonjour, J.-P. (1998) · Annals of Internal Medicine · doi:10.7326/0003-4819-128-10-199805150-00002 · Cited by 572 · see citing works
Prospective study of dietary protein intake and risk of hip fracture in postmenopausal women
Munger, R. G., Cerhan, J. R., & Chiu, B. C. ‐. (1999) · American Journal of Clinical Nutrition · doi:10.1093/ajcn/69.1.147 · Cited by 381 · see citing works
Jacques, P. F., Sulsky, S., Sadowski, J., Phillips, J., Rush, D., & Willett, W. C. (1993) · American Journal of Clinical Nutrition · doi:10.1093/ajcn/57.2.182 · Cited by 306 · see citing works
McDowell, M., BRIEFEL, R. R., Alaimo, K., Bischof, A. M., CAUGHMAN, C., Carroll, M. D., Loria, C. M., & Johnson, C. L. (1994) · PubMed · Cited by 274 · see citing works
Nutrition in orthopaedic surgery.
Jensen, J. E., Jensen, T. G., Smith, T. K., Johnston, D. A., & Dudrick, S. J. (1982) · Journal of Bone and Joint Surgery · doi:10.2106/00004623-198264090-00001 · Cited by 272 · see citing works
Bone mineral density in elderly men and women: Results from the framingham osteoporosis study
Hannan, M. T., Felson, D. T., & Anderson, J. J. (1992) · Journal of Bone and Mineral Research · doi:10.1002/jbmr.5650070511 · Cited by 270 · see citing works
Self-citationNutritional aspects of hip fractures
Bonjour, J. ‐., Schürch, M.-A., & Rizzoli, R. (1996) · Bone · doi:10.1016/8756-3282(95)00494-7 · Cited by 268 · see citing works
Increased protein requirements in elderly people: new data and retrospective reassessments
Campbell, W. W., Crim, M. C., Dallal, G., Young, V. R., & Evans, W. (1994) · American Journal of Clinical Nutrition · doi:10.1093/ajcn/60.4.501 · Cited by 267 · see citing works
Bastow, M. D., Rawlings, J., & Allison, S. P. (1983) · The Lancet · doi:10.1016/s0140-6736(83)92754-x · Cited by 260 · see citing works
Nutritional Factors in Osteoporosis
Heaney, R. P. (1993) · Annual Review of Nutrition · doi:10.1146/annurev.nu.13.070193.001443 · Cited by 257 · see citing works
Cross-cultural association between dietary animal protein and hip fracture: A hypothesis
Abelow, B. J., Holford, T. R., & Insogna, K. L. (1992) · Calcified Tissue International · doi:10.1007/bf00297291 · Cited by 250 · see citing works
Alcohol Intake and Bone Mineral Density in Elderly Men and Women
Felson, D. T., Zhang, Y., Hannan, M. T., Kannel, W. B., & Kiel, D. P. (1995) · American Journal of Epidemiology · doi:10.1093/oxfordjournals.aje.a117664 · Cited by 246 · see citing works
Self-citationBenefits of oral protein supplementation in elderly patients with fracture of the proximal femur.
Tkatch, L. S., Rapin, C. H., Rizzoli, R., Slosman, D. O., Nydegger, V., Vasey, H., & Bonjour, J. ‐. (1992) · Journal of the American College of Nutrition · doi:10.1080/07315724.1992.10718256 · Cited by 233 · see citing works
Protein depletion and metabolic stress in elderly patients who have a fracture of the hip.
Patterson, B. M., Cornell, C., Carbone, B., Levine, B., & Chapman, D. (1992) · Journal of Bone and Joint Surgery. American volume · doi:10.2106/00004623-199274020-00011 · Cited by 227 · see citing works
Dietary intake and bone mineral density.
Angus, R. M., Sambrook, P. N., POCOCK, N. A., & Eisman, J. A. (1988) · PubMed · Cited by 226 · see citing works
ALCOHOL CONSUMPTION AND HIP FRACTURES: THE FRAMINGHAM STUDY
Felson, D. T., Kiel, D. P., Anderson, J. J., & Kannel, W. B. (1988) · American Journal of Epidemiology · doi:10.1093/oxfordjournals.aje.a115052 · Cited by 225 · see citing works
Self-citationProtein-induced hypercalciuria: a longer term study
Allen, L., Oddoye, E. A., & Margen, S. (1979) · American Journal of Clinical Nutrition · doi:10.1093/ajcn/32.4.741 · Cited by 216 · see citing works
CAFFEINE AND THE RISK OF HIP FRACTURE: THE FRAMINGHAM STUDY
Kiel, D. P., Felson, D. T., Hannan, M. T., Anderson, J. J., & Wilson, P. W. F. (1990) · American Journal of Epidemiology · doi:10.1093/oxfordjournals.aje.a115709 · Cited by 216 · see citing works
Self-citationFreudenheim, J. L., Johnson, N., & Smith, E. (1986) · American Journal of Clinical Nutrition · doi:10.1093/ajcn/44.6.863 · Cited by 209 · see citing works
Dietary protein affects intestinal calcium absorption
Kerstetter, J. E., O'Brien, K. O., & Insogna, K. L. (1998) · American Journal of Clinical Nutrition · doi:10.1093/ajcn/68.4.859 · Cited by 193 · see citing works
Johnson, N. E., Alcantara, E. N., & Linkswiler, H. (1970) · Journal of Nutrition · doi:10.1093/jn/100.12.1425 · Cited by 188 · see citing works
Gersovitz, M., Motil, K. J., Munro, H. N., Scrimshaw, N. S., & Young, V. R. (1982) · American Journal of Clinical Nutrition · doi:10.1093/ajcn/35.1.6 · Cited by 174 · see citing works
The influence of dietary protein intake on specific renal functions in normal man.
Pullman, T. N., Alving, A. S., Dern, R. J., & Landowne, M. (1954) · PubMed · Cited by 169 · see citing works
Relationship between bone mineral density and dietary intakes in the elderly
Geinoz, G., Rapin, C. H., Rizzoli, R., Kraemer, R., Buchs, B., Slosman, D. O., Michel, J.-P., & Bonjour, J. ‐. (1993) · Osteoporosis International · doi:10.1007/bf01623827 · Cited by 167 · see citing works
Studies in calcium metabolism. I. The calciuretic effect of dietary protein
Margen, S., Chu, J., KAUFMANN, N. A., & Calloway, D. H. (1974) · American Journal of Clinical Nutrition · doi:10.1093/ajcn/27.6.584 · Cited by 166 · see citing works
Estimates of Animal and Plant Protein Intake in US Adults
Smit, E., Nieto, F. J., Crespo, C. J., & MITCHELL, P. (1999) · Journal of the American Dietetic Association · doi:10.1016/s0002-8223(99)00193-5 · Cited by 148 · see citing works
Correlates of mid-radius bone density among postmenopausal women: a community study
Sowers, M., Wallace, R., & Lemke, J. (1985) · American Journal of Clinical Nutrition · doi:10.1093/ajcn/41.5.1045 · Cited by 148 · see citing works
Effect of Protein Intake on Calcium Balance of Young Men Given 500 mg Calcium Daily
Anand, C. R., & Linkswiler, H. (1974) · Journal of Nutrition · doi:10.1093/jn/104.6.695 · Cited by 135 · see citing works
Calcium Retention in the Adult Human Male as Affected by Protein Intake
Walker, R. M., & Linkswiler, H. (1972) · Journal of Nutrition · doi:10.1093/jn/102.10.1297 · Cited by 134 · see citing works
Effect of diet and lifestyle on bone mass in Asian young women
Hirota, T., Nara, M., Ohguri, M., Manago, E., & Hirota, K. (1992) · American Journal of Clinical Nutrition · doi:10.1093/ajcn/55.6.1168 · Cited by 125 · see citing works
Kerstetter, J., Caseria, D. M., Mitnick, M., Ellison, A., Gay, L. A., Liskov, T. A. P., Carpenter, T. O., & Insogna, K. L. (1997) · American Journal of Clinical Nutrition · doi:10.1093/ajcn/66.5.1188 · Cited by 122 · see citing works
Dietary factors in bone health of elderly lactoovovegetarian and omnivorous women
Tylavsky, F., & Anderson, J. (1988) · American Journal of Clinical Nutrition · doi:10.1093/ajcn/48.3.842 · Cited by 119 · see citing works
Habitual physical activity is not associated with knee osteoarthritis: the Framingham Study.
Hannan, M. T., Felson, D. T., Anderson, J. J., & Naimark, A. (1993) · PubMed · Cited by 117 · see citing works
Self-citationCALCIUM REQUIREMENT OF MAINTENANCE IN MAN
SHERMAN, H. C., Rose, A., & Rose, M. S. (1920) · Journal of Biological Chemistry · doi:10.1016/s0021-9258(18)86268-8 · Cited by 115 · see citing works
DIETARY RISK FACTORS FOR AGE-RELATED BONE LOSS AND FRACTURES
PARFITT, A. M. (1983) · The Lancet · doi:10.1016/s0140-6736(83)91226-6 · Cited by 106 · see citing works
Chu, J.-Y., Margen, S., & Costa, F. (1975) · American Journal of Clinical Nutrition · doi:10.1093/ajcn/28.9.1028 · Cited by 91 · see citing works
Nevitt, M. C. (1994) · Rheumatic Disease Clinics of North America · doi:10.1016/s0889-857x(21)00348-3 · Cited by 88 · see citing works
Protein-induced hypercalciuria.
Linkswiler, H., Zemel, M. B., Hegsted, M., & Schuette, S. A. (1981) · PubMed · Cited by 88 · see citing works
Nutrition in the elderly : the Boston nutritional status survey
Hartz, S. C., Russell, R. M., & Rosenberg, I. H. (1992) · Medical Entomology and Zoology · Cited by 77 · see citing works
Bone mineral content in postmenopausal women: comparison of omnivores and vegetarians
Hunt, I. F., Murphy, N. J., Henderson, C. T., Clark, V. A., Jacobs, R. M., JOHNSTON, P. K., & Coulson, A. H. (1989) · American Journal of Clinical Nutrition · doi:10.1093/ajcn/50.3.517 · Cited by 68 · see citing works
Kiel, D. P., Cali, C., Mercier, C. A., Dawson‐Hughes, B., Hannan, M. T., & Anderson, J. J. (1995) · Journal of Bone and Mineral Research · doi:10.1002/jbmr.5650100719 · Cited by 61 · see citing works
Self-citationCalcium metabolism in postmenopausal and osteoporotic women consuming two levels of dietary protein
Lutz, J., & Linkswiler, H. (1981) · American Journal of Clinical Nutrition · doi:10.1093/ajcn/34.10.2178 · Cited by 56 · see citing works
Serum protein concentrations and bone mineral content in aging normal men
ORWOLL, E. S., Weigel, R. M., Oviatt, S. K., Meier, D. E., & McClung, M. R. (1987) · American Journal of Clinical Nutrition · doi:10.1093/ajcn/46.4.614 · Cited by 35 · see citing works
Dietary Factors Influencing Calcium and Bone Metabolism: Introduction
Massey, L. K. (1993) · Journal of Nutrition · doi:10.1093/jn/123.9.1609 · Cited by 7 · see citing works
Flagged first, then by citations
1 of the 59 references couldn’t be matched to a known paper.
Cited by
Sorted by citations
Bauer, J., Biolo, G., Cederholm, T., Cesari, M., Cruz-Jentoft, A. J., Morley, J. E., Phillips, S., Sieber, C., Stehle, P., Teta, D., et al. (2013) · Journal of the American Medical Directors Association · doi:10.1016/j.jamda.2013.05.021 · Cited by 2,553 · see citing works
Position of the American Dietetic Association: Vegetarian Diets
Craig, W. J., & Mangels, A. R. (2009) · Journal of the American Dietetic Association · doi:10.1016/j.jada.2009.05.027 · Cited by 1,039 · see citing works
Scientific Opinion on Dietary Reference Values for protein
EFSA Panel on Dietetic Products, N. A. A. (. (2012) · EFSA Journal · doi:10.2903/j.efsa.2012.2557 · Cited by 739 · see citing works
Plant Proteins: Assessing Their Nutritional Quality and Effects on Health and Physical Function
Hertzler, S. R., Lieblein-Boff, J. C., Weiler, M., & Allgeier, C. (2020) · Nutrients · doi:10.3390/nu12123704 · Cited by 594 · see citing works
Hoffman, J. R., & Falvo, M. J. (2004) · Europe PMC (PubMed Central) · Cited by 519 · see citing works
Nutrition in Bone Health Revisited: A Story Beyond Calcium
Ilich, J. Z., & Kerstetter, J. E. (2000) · Journal of the American College of Nutrition · doi:10.1080/07315724.2000.10718070 · Cited by 510 · see citing works
Noakes, M., Keogh, J. B., Foster, P. R., & Clifton, P. M. (2005) · The American Journal of Clinical Nutrition · doi:10.1093/ajcn/81.6.1298 · Cited by 483 · see citing works
New, S. A., Robins, S. P., Campbell, M., Martin, J. C., Garton, M. J., Bolton-Smith, C., Grubb, D. A., Lee, S. J., & Reid, D. M. (2000) · American Journal of Clinical Nutrition · doi:10.1093/ajcn/71.1.142 · Cited by 482 · see citing works
Peacock, M., Turner, C. H., Econs, M. J., & Foroud, T. (2002) · Endocrine Reviews · doi:10.1210/edrv.23.3.0464 · Cited by 461 · see citing works
Farnsworth, E., Luscombe, N. D., Noakes, M., Wittert, G., Argyiou, E., & Clifton, P. M. (2003) · The American Journal of Clinical Nutrition · doi:10.1093/ajcn/78.1.31 · Cited by 438 · see citing works
The Role of Nutrients in Bone Health, from A to Z
Palacios, C. S. (2006) · Critical Reviews in Food Science and Nutrition · doi:10.1080/10408390500466174 · Cited by 426 · see citing works
Hu, T., Mills, K. T., Yao, L., Demanelis, K., Eloustaz, M., Yancy, W. S., Kelly, T. N., He, J., & Bazzano, L. A. (2012) · American Journal of Epidemiology · doi:10.1093/aje/kws264 · Cited by 417 · see citing works
Ettinger, B. B., Harris, S. T., Kendler, D. L., Kessel, B., McClung, M. R., Gorodeski, G. I., Rothert, M. L., Henderson, V. W., Richardson, M. K., Freedman, R. R., et al. (2006) · Cited by 403 · see citing works
Reddy, S. T., Wang, C.-Y., Sakhaee, K., Brinkley, L., & Pak, C. Y. C. (2002) · American Journal of Kidney Diseases · doi:10.1053/ajkd.2002.34504 · Cited by 391 · see citing works
Management of osteoporosis in postmenopausal women
(2010) · Menopause The Journal of The North American Menopause Society · doi:10.1097/gme.0b013e3181c617e6 · Cited by 382 · see citing works
Diet, nutrition and the prevention of osteoporosis
Prentice, A. (2004) · Public Health Nutrition · doi:10.1079/phn2003590 · Cited by 339 · see citing works
Dawson-Hughes, B. F., & Harris, S. S. (2002) · American Journal of Clinical Nutrition · doi:10.1093/ajcn/75.4.773 · Cited by 325 · see citing works
Self-citationDietary protein and bone health: a systematic review and meta-analysis
Darling, A. L., Millward, D. J., Torgerson, D. J., Hewitt, C. E., & Lanham-New, S. A. (2009) · The American Journal of Clinical Nutrition · doi:10.3945/ajcn.2009.27799 · Cited by 310 · 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
Frailty and sarcopenia: definitions and outcome parameters
Cooper, C. C., Dere, W. H., Evans, W. J., Kanis, J. A., Rizzoli, R., Sayer, A. A., Sieber, C. C., Kaufman, J., van Kan, G. A., Boonen, S., et al. (2012) · Osteoporosis International · doi:10.1007/s00198-012-1913-1 · Cited by 302 · see citing works
Eisenstein, J., Roberts, S. B., Dallal, G. E., & Saltzman, E. J. (2002) · Nutrition Reviews · doi:10.1301/00296640260184264 · Cited by 295 · see citing works
The Impact of Dietary Protein on Calcium Absorption and Kinetic Measures of Bone Turnover in Women
Kerstetter, J. E., O'Brien, K. O., Caseria, D. M., Wall, D. E., & Insogna, K. L. (2005) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jc.2004-0179 · Cited by 290 · see citing works
Dietary Protein: An Essential Nutrient For Bone Health
Bonjour, J. (2005) · Journal of the American College of Nutrition · doi:10.1080/07315724.2005.10719501 · Cited by 295 · see citing works
Bone mineral density and dietary patterns in older adults: the Framingham Osteoporosis Study,,
Tucker, K. L., Chen, H., Hannan, M. T., Cupples, L. A., Wilson, P. W. F., Felson, D. T., & Kiel, D. P. (2002) · American Journal of Clinical Nutrition · doi:10.1093/ajcn/76.1.245 · Cited by 279 · see citing works
Self-citationShams‐White, M., Chung, M. C., Du, M., Fu, Z., Insogna, K. L., Karlsen, M. C., LeBoff, M. S., Shapses, S. A., Sackey, J. D., Wallace, T. C., et al. (2017) · American Journal of Clinical Nutrition · doi:10.3945/ajcn.116.145110 · Cited by 264 · see citing works
Amount and type of protein influences bone health
Heaney, R. P., & Layman, D. K. (2008) · American Journal of Clinical Nutrition · doi:10.1093/ajcn/87.5.1567s · Cited by 259 · see citing works
Lanou, A. J., Berkow, S. E., & Barnard, N. D. (2005) · PEDIATRICS · doi:10.1542/peds.2004-0548 · Cited by 257 · see citing works
The DASH Diet and Sodium Reduction Improve Markers of Bone Turnover and Calcium Metabolism in Adults
Lin, P., Ginty, F., Appel, L. J., Aickin, M. G., Bohannon, A., Garnero, P., Barclay, D., & Svetkey, L. P. (2003) · Journal of Nutrition · doi:10.1093/jn/133.10.3130 · Cited by 255 · see citing works
Rizzoli, R., Stevenson, J. C., Bauer, J. M., van Loon, L. J. C., Walrand, S., Kanis, J. A., Cooper, C., Brandi, M.-L., Diez-Perez, A., & Reginster, J.-Y. (2014) · Maturitas · doi:10.1016/j.maturitas.2014.07.005 · Cited by 291 · see citing works
Dietary Acid Load: A Novel Nutritional Target in Chronic Kidney Disease?
Scialla, J. J., & Anderson, C. A. M. (2013) · Advances in Chronic Kidney Disease · doi:10.1053/j.ackd.2012.11.001 · Cited by 253 · see citing works
Brinkworth, G. D., Noakes, M., Keogh, J. B., Luscombe, N. D., Wittert, G. A., & Clifton, P. M. (2004) · International Journal of Obesity · doi:10.1038/sj.ijo.0802617 · Cited by 245 · see citing works
Clinical Evidence and Mechanisms of High-Protein Diet-Induced Weight Loss
Moon, J., & Koh, G. (2020) · Journal of Obesity & Metabolic Syndrome · doi:10.7570/jomes20028 · Cited by 233 · see citing works
Update on Osteoporosis Screening and Management
Anam, A. K., & Insogna, K. L. (2021) · Medical Clinics of North America · doi:10.1016/j.mcna.2021.05.016 · Cited by 238 · see citing works
Dietary protein, calcium metabolism, and skeletal homeostasis revisited
Kerstetter, J. E., O'Brien, K. O., & Insogna, K. L. (2003) · American Journal of Clinical Nutrition · doi:10.1093/ajcn/78.3.584s · Cited by 218 · see citing works
Low Plasma Vitamin B12 Is Associated With Lower BMD: The Framingham Osteoporosis Study
Tucker, K. L., Hannan, M. T., Qiao, N., Jacques, P. F., Selhub, J., Cupples, L. A., & Kiel, D. P. (2005) · Journal of Bone and Mineral Research · doi:10.1359/jbmr.041018 · Cited by 215 · see citing works
Self-citationLow Protein Intake: The Impact on Calcium and Bone Homeostasis in Humans
Kerstetter, J. E., O'Brien, K. O., & Insogna, K. L. (2003) · The Journal of Nutrition · doi:10.1093/jn/133.3.855s · Cited by 212 · see citing works
Maurer, M., Riesen, W., Muser, J. M., Hulter, H. N., & Krapf, R. (2003) · American Journal of Physiology-Renal Physiology · doi:10.1152/ajprenal.00212.2002 · Cited by 211 · see citing works
Lupsa, B. C., & Insogna, K. L. (2015) · Endocrinology and Metabolism Clinics of North America · doi:10.1016/j.ecl.2015.05.002 · Cited by 206 · see citing works
Park, Y., Choi, J.-E., & Hwang, H.-S. (2018) · The American Journal of Clinical Nutrition · doi:10.1093/ajcn/nqy214 · Cited by 193 · see citing works
Heaney, R. P. (2009) · Journal of the American College of Nutrition · doi:10.1080/07315724.2009.10719808 · Cited by 190 · see citing works
Macdonald, H. M., New, S. A., Fraser, W. D., Campbell, M., & Reid, D. M. (2005) · American Journal of Clinical Nutrition · doi:10.1093/ajcn/81.4.923 · Cited by 186 · see citing works
Management of osteoporosis in postmenopausal women
(2006) · Menopause The Journal of The North American Menopause Society · doi:10.1097/01.gme.0000222475.93345.b3 · Cited by 184 · see citing works
Heaney, R. P., & Weaver, C. M. (2003) · Endocrinology and Metabolism Clinics of North America · doi:10.1016/s0889-8529(02)00063-4 · Cited by 181 · see citing works
Jehle, S., Zanetti, A., Muser, J., Hulter, H. N., & Krapf, R. (2006) · Journal of the American Society of Nephrology · doi:10.1681/asn.2006030233 · Cited by 172 · see citing works
Red meat in the diet: an update
Wyness, L., Weichselbaum, E., O’Connor, Á., Williams, E. B., Benelam, B., Riley, H., & Stanner, S. A. (2011) · Nutrition Bulletin · doi:10.1111/j.1467-3010.2010.01871.x · Cited by 164 · see citing works
Ilich, J. Z., Brownbill, R. A., & Tamborini, L. (2003) · European Journal of Clinical Nutrition · doi:10.1038/sj.ejcn.1601577 · Cited by 161 · see citing works
Arjmandi, B. H., Lucas, E. A., Khalil, D. A., Devareddy, L., Smith, B. J., McDonald, J., Arquitt, A. B., Payton, M. E., & Mason, C. (2005) · Nutrition Journal · doi:10.1186/1475-2891-4-8 · Cited by 153 · see citing works
Osteoporosis prevention and nutrition
Tucker, K. L. (2009) · Current Osteoporosis Reports · doi:10.1007/s11914-009-0020-5 · Cited by 151 · see citing works
Self-citationFarina, E. K., Kiel, D. P., Roubenoff, R., Schaefer, E. J., Cupples, L. A., & Tucker, K. L. (2011) · American Journal of Clinical Nutrition · doi:10.3945/ajcn.110.005926 · Cited by 148 · see citing works
Self-citationDietary Protein Intake and Risk of Osteoporotic Hip Fracture in Elderly Residents of Utah
Wengreen, H. J., Munger, R. G., West, N. A., Cutler, D. R., Corcoran, C. D., Zhang, J., & Sassano, N. E. (2004) · Journal of Bone and Mineral Research · doi:10.1359/jbmr.040208 · Cited by 147 · see citing works
Roughead, Z. K., Johnson, L. K., Hunt, J. R., & LYKKEN, G. I. (2003) · Journal of Nutrition · doi:10.1093/jn/133.4.1020 · Cited by 147 · see citing works
Dietary Animal and Plant Protein and Human Bone Health: A Whole Foods Approach
Massey (2003) · Journal of Nutrition · doi:10.1093/jn/133.3.862s · Cited by 145 · see citing works
Pinheiro, M. M., Schuch, N. J., Genaro, P. D. S., Ciconelli, R. M., Ferraz, M. B., & Martini, L. A. (2009) · Nutrition Journal · doi:10.1186/1475-2891-8-6 · Cited by 144 · see citing works
Effect of vegetarian diets on bone mineral density: a Bayesian meta-analysis
Ho-Pham, L. T., Nguyen, N. D., & Nguyen, T. V. (2009) · American Journal of Clinical Nutrition · doi:10.3945/ajcn.2009.27521 · Cited by 142 · see citing works
Dietary Protein and Bone Health
Rizzoli, R., & Bonjour, J. (2004) · Journal of Bone and Mineral Research · doi:10.1359/jbmr.040204 · Cited by 141 · see citing works
Clinical and Histological Evaluation of Postextraction Platelet-rich Fibrin Socket Filling
Hauser, F., Gaydarov, N., Badoud, I., Vazquez, L., Bernard, J., & Ammann, P. (2013) · Implant Dentistry · doi:10.1097/id.0b013e3182906eb3 · Cited by 139 · see citing works
Melton, L. J., Crowson, C. S., O’Fallon, W. M., Wahner, H. W., & Riggs, B. L. (2003) · Journal of Bone and Mineral Research · doi:10.1359/jbmr.2003.18.2.312 · Cited by 138 · see citing works
Sánchez-Sánchez, M. L., García-Vigara, A., Hidalgo-Mora, J. J., García-Pérez, M.-Á., Tarín, J., & Cano, A. (2020) · Maturitas · doi:10.1016/j.maturitas.2020.03.008 · Cited by 137 · see citing works
Sukumar, D., Ambia‐Sobhan, H., Zurfluh, R., Schlussel, Y., Stahl, T. J., Gordon, C. L., & Shapses, S. A. (2010) · Journal of Bone and Mineral Research · doi:10.1002/jbmr.318 · Cited by 136 · see citing works
Defining meal requirements for protein to optimize metabolic roles of amino acids
Layman, D., Anthony, T., Rasmussen, B., Adams, S., Lynch, C., Brinkworth, G., & Davis, T. (2015) · American Journal of Clinical Nutrition · doi:10.3945/ajcn.114.084053 · Cited by 141 · see citing works
Non-pharmacological management of osteoporosis: a consensus of the Belgian Bone Club
Body, J., Bergmann, P., Boonen, S., Boutsen, Y., Bruyère, O., Devogelaer, J.-P., Goemaere, S., Hollevoet, N., Kaufman, J., Milisen, K., et al. (2011) · Osteoporosis International · doi:10.1007/s00198-011-1545-x · Cited by 136 · see citing works
Dietary patterns, bone resorption and bone mineral density in early post-menopausal Scottish women
Hardcastle, A. C., Aucott, L. S., Fraser, W. D., Reid, D. M., & Macdonald, H. M. (2010) · European Journal of Clinical Nutrition · doi:10.1038/ejcn.2010.264 · Cited by 135 · see citing works
Holm, L., Olesen, J. L., Matsumoto, K., Doi, T., Mizuno, M., Alsted, T. J., Mackey, A. L., Schwarz, P., & Kjær, M. (2008) · Journal of Applied Physiology · doi:10.1152/japplphysiol.00935.2007 · Cited by 131 · see citing works
Changes in Bone Turnover in Young Women Consuming Different Levels of Dietary Protein1
Kerstetter, J. E., Mitnick, M., Gundberg, C. M., Caseria, D. M., Ellison, A. F., Carpenter, T. O., & Insogna, K. L. (1999) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jcem.84.3.5552 · Cited by 131 · see citing works
Sahni, S., Tucker, K. L., Kiel, D. P., Quach, L., Casey, V. A., & Hannan, M. T. (2013) · Archives of Osteoporosis · doi:10.1007/s11657-013-0119-2 · Cited by 129 · see citing works
Self-citationInteraction of Dietary Calcium and Protein in Bone Health in Humans
Dawson‐Hughes, B. (2003) · Journal of Nutrition · doi:10.1093/jn/133.3.852s · Cited by 128 · see citing works
Self-citationMeng, X., Zhu, K., Devine, A., Kerr, D. A., Binns, C. W., & Prince, R. L. (2009) · Journal of Bone and Mineral Research · doi:10.1359/jbmr.090513 · Cited by 123 · see citing works
Dietary Patterns and Fractures in Postmenopausal Women
Haring, B., Crandall, C. J., Wu, C., LeBlanc, E. S., Shikany, J. M., Carbone, L. D., Orchard, T., Thomas, F., Wactawski‐Wende, J., Li, W., et al. (2016) · JAMA Internal Medicine · doi:10.1001/jamainternmed.2016.0482 · Cited by 123 · see citing works
Dietary Protein Intake above the Current RDA and Bone Health: A Systematic Review and Meta-Analysis
Wallace, T. C., & Frankenfeld, C. L. (2017) · Journal of the American College of Nutrition · doi:10.1080/07315724.2017.1322924 · Cited by 123 · see citing works
Durosier, C., Biver, E., Merminod, F., van Rietbergen, B., Chevalley, T., Herrmann, F. R., Ferrari, S., & Rizzoli, R. (2017) · American Journal of Clinical Nutrition · doi:10.3945/ajcn.116.134676 · Cited by 122 · see citing works
The North American Menopause Society (2002) · Menopause The Journal of The North American Menopause Society · doi:10.1097/00042192-200203000-00003 · Cited by 121 · see citing works
Vegetarian diets and bone status
Tucker, K. L. (2014) · American Journal of Clinical Nutrition · doi:10.3945/ajcn.113.071621 · Cited by 118 · see citing works
Self-citationGroenendijk, I., den Boeft, L. M., van Loon, L. J. C., & de Groot, C. P. G. M. (2019) · Computational and Structural Biotechnology Journal · doi:10.1016/j.csbj.2019.07.005 · Cited by 116 · see citing works
Dietary Approaches for Bone Health: Lessons from the Framingham Osteoporosis Study
Sahni, S., Mangano, K. M., McLean, R. R., Hannan, M. T., & Kiel, D. P. (2015) · Current Osteoporosis Reports · doi:10.1007/s11914-015-0272-1 · Cited by 119 · see citing works
Self-citationNutrition: its role in bone health
Rizzoli, R. (2008) · Best Practice & Research Clinical Endocrinology & Metabolism · doi:10.1016/j.beem.2008.08.005 · Cited by 116 · see citing works
Makovey, J., Macara, M., Chen, J. S., Hayward, C., MARCH, L. M., Seibel, M. J., & Sambrook, P. N. (2012) · Bone · doi:10.1016/j.bone.2012.10.025 · Cited by 115 · see citing works
Nutritional aspects of bone health
Rizzoli, R. (2014) · Best Practice & Research Clinical Endocrinology & Metabolism · doi:10.1016/j.beem.2014.08.003 · Cited by 115 · see citing works
Sahni, S., Cupples, L. A., McLean, R. R., Tucker, K. L., Broe, K. E., Kiel, D. P., & Hannan, M. T. (2010) · Journal of Bone and Mineral Research · doi:10.1002/jbmr.194 · Cited by 112 · see citing works
Self-citationDay, N., Bingham, S. A., Khaw, K., Kaptoge, S., Welch, A. A., McTaggart, A., Mulligan, A. A., Dalzell, N., & REEVE, J. (2003) · Osteoporosis International · doi:10.1007/s00198-003-1391-6 · Cited by 112 · see citing works
Hengeveld, L. M., Boer, J., Gaudreau, P., Heymans, M., Jagger, C., Mendonça, N., Ocké, M., Presse, N., Sette, S., Simonsick, E., et al. (2020) · Journal of Cachexia, Sarcopenia and Muscle · doi:10.1002/jcsm.12580 · Cited by 96 · see citing works
Protein consumption is an important predictor of lower limb bone mass in elderly women
Devine, A., Dick, I. M., Islam, A. F., Dhaliwal, S. S., & Prince, R. L. (2005) · The American Journal of Clinical Nutrition · doi:10.1093/ajcn/81.6.1423 · Cited by 110 · see citing works
The Low-Carbohydrate Diet: Short-Term Metabolic Efficacy Versus Longer-Term Limitations
Barber, T. M., Hanson, P., Kabisch, S., Pfeiffer, A. F. H., & Weickert, M. O. (2021) · Nutrients · doi:10.3390/nu13041187 · Cited by 109 · see citing works
Nutrients, Endpoints, and the Problem of Proof
Heaney, R. P. (2008) · Journal of Nutrition · doi:10.1093/jn/138.9.1591 · Cited by 109 · see citing works
Jennings, A., MacGregor, A. J., Spector, T. D., & Cassidy, A. (2015) · Journal of Bone and Mineral Research · doi:10.1002/jbmr.2703 · Cited by 108 · see citing works
Nutrition and Aging in Developing Countries
Tucker, K. L., & Buranapin, S. (2001) · Journal of Nutrition · doi:10.1093/jn/131.9.2417s · Cited by 107 · see citing works
Self-citationZhu, K., & Prince, R. L. (2015) · Current Osteoporosis Reports · doi:10.1007/s11914-014-0248-6 · Cited by 106 · see citing works
Mangano, K. M., Sahni, S., Kiel, D. P., Tucker, K. L., Dufour, A. B., & Hannan, M. T. (2017) · American Journal of Clinical Nutrition · doi:10.3945/ajcn.116.136762 · Cited by 110 · see citing works
Self-citationConigrave, A. D., Brown, E. M., & Rizzoli, R. (2008) · Annual Review of Nutrition · doi:10.1146/annurev.nutr.28.061807.155328 · Cited by 104 · see citing works
Whiting, S. J., Boyle, J. L., Thompson, A. M., Mirwald, R. L., & Faulkner, R. A. (2002) · Journal of the American College of Nutrition · doi:10.1080/07315724.2002.10719242 · Cited by 102 · see citing works
Protein Intake and Bone Health
Bonjour, J.-P. (2011) · International Journal for Vitamin and Nutrition Research · doi:10.1024/0300-9831/a000063 · Cited by 102 · see citing works
Cao, J., Johnson, L. K., & Hunt, J. R. (2011) · Journal of Nutrition · doi:10.3945/jn.110.129361 · Cited by 101 · see citing works
Shams-White, M. M., Chung, M., Fu, Z., Insogna, K. L., Karlsen, M. C., LeBoff, M. S., Shapses, S. A., Sackey, J., Shi, J., Wallace, T. C., et al. (2018) · PLOS ONE · doi:10.1371/journal.pone.0192459 · Cited by 100 · see citing works
Exercise and nutritional approaches to prevent frail bones, falls and fractures: an update
Daly, R. M. (2017) · Climacteric · doi:10.1080/13697137.2017.1286890 · Cited by 99 · see citing works
Protein intake, calcium balance and health consequences
Calvez, J., Poupin, N., Chesneau, C., Lassale, C. M., & Tomé, D. (2011) · European Journal of Clinical Nutrition · doi:10.1038/ejcn.2011.196 · Cited by 98 · see citing works
Zhu, K., Meng, X., Kerr, D. A., Devine, A., Solah, V. A., Binns, C. W., & Prince, R. L. (2011) · Journal of Bone and Mineral Research · doi:10.1002/jbmr.429 · Cited by 97 · see citing works
Bowen, J., Noakes, M., & Clifton, P. M. (2004) · Journal of Nutrition · doi:10.1093/jn/134.3.568 · Cited by 97 · see citing works
Health effects of protein intake in healthy elderly populations: a systematic literature review
Pedersen, A. N., & Cederholm, T. (2014) · Food & Nutrition Research · doi:10.3402/fnr.v58.23364 · Cited by 93 · see citing works
Effect of protein intake on bone and muscle mass in the elderly.
Genaro, P. D. S., & Martini, L. (2010) · Nutrition reviews · doi:10.1111/j.1753-4887.2010.00321.x · Cited by 89 · see citing works
Growing older with health and vitality: a nexus of physical activity, exercise and nutrition
Witard, O. C., McGlory, C., Hamilton, D. L., & Phillips, S. M. (2016) · Biogerontology · doi:10.1007/s10522-016-9637-9 · Cited by 91 · see citing works
Dargent‐Molina, P., Sabia, S., Touvier, M., Kesse‐Guyot, E., Bréart, G., Clavel‐Chapelon, F., & Boutron‐Ruault, M. (2008) · Journal of Bone and Mineral Research · doi:10.1359/jbmr.080712 · Cited by 91 · see citing works
- Authors
- Hannan, M. T., Tucker, K. L., Dawson-Hughes, B., Cupples, L. A., Felson, D. T., & Kiel, D. P.
- Affiliations
- Boston University (US)
- Tufts University (US)
- Jean Mayer United States Department of Agriculture Human Nutrition Research Center on Aging at Tufts University, Boston, Massachusetts, U.S.A.
- Harvard University (US)
- Corresponding author
- Hannan, Marian T.
- Venue
- Journal of Bone and Mineral Research
- Publisher
- Oxford University Press (OUP)
- Published
- 2000-12-01
- Volume
- 15
- Issue
- 12
- Pages
- 2504-2512
- ISSN
- 0884-0431 (ISSN-L)
- 1523-4681
- OpenAlex
- W2087658867
- Cited by
- 536
- References
- 59
- Citations by year
- 2026: 4 · 2025: 7 · 2024: 15 · 2023: 14 · 2022: 9 · 2021: 12 · 2020: 21 · 2019: 17 · 2018: 17 · 2017: 21 · 2016: 15 · 2015: 20 · 2014: 29 · 2013: 30 · 2012: 14
- FWCI
- 19.72
- Type
- journal article
- Language
- en
- Open access
- closed
- Licence
- academic.oup.com/journals/pages/open_access/funder_policies/chorus/standard_publication_model (vor)
- Locations
- Journal of Bone and Mineral Research (publishedVersion)
- PubMed (publishedVersion)
- Funders
- Arthritis Foundation
- National Institute of Arthritis and Musculoskeletal and Skin Diseases (AR-20613, R01 AR/AG 41398, P60AR020613)
- 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 › Public Health, Environmental and Occupational Health › Nutritional Studies and Diet
- Keywords
- dietary protein, bone loss, bone mineral density, older adults, animal protein, calcium balance, osteoporosis, sex differences, femoral bone, radial bone
- MeSH terms
- Adult, Dietary Proteins, Female, Femur, Humans, Longitudinal Studies, Male, Middle Aged, Osteoporosis, Surveys and Questionnaires, Radius, Spine, Time Factors, Absorptiometry, Photon, Bone Density, Osteoporosis, Postmenopausal
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