Advertisement

Diet-Induced Weight Loss: The Effect of Dietary Protein on Bone

Published:October 30, 2013DOI:https://doi.org/10.1016/j.jand.2013.08.021

      Abstract

      High-protein (>30% of energy from protein or >1.2 g/kg/day) and moderately high-protein (22% to 29% of energy from protein or 1.0 to 1.2 g/kg/day) diets are popular for weight loss, but the effect of dietary protein on bone during weight loss is not well understood. Protein may help preserve bone mass during weight loss by stimulating insulin-like growth factor 1, a potent bone anabolism stimulator, and increasing intestinal calcium absorption. Protein-induced acidity is considered to have minimal effect on bone resorption in adults with normal kidney function. Both the quantity and predominant source of protein influence changes in bone with diet-induced weight loss. Higher-protein, high-dairy diets may help attenuate bone loss during weight loss.

      Keywords

      To read this article in full you will need to make a payment

      Purchase one-time access:

      Academic & Personal: 24 hour online accessCorporate R&D Professionals: 24 hour online access
      One-time access price info
      • For academic or personal research use, select 'Academic and Personal'
      • For corporate R&D use, select 'Corporate R&D Professionals'

      Subscribe:

      Subscribe to Journal of the Academy of Nutrition and Dietetics
      Already a print subscriber? Claim online access
      Already an online subscriber? Sign in
      Institutional Access: Sign in to ScienceDirect

      References

        • Flegal K.M.
        • Carroll M.D.
        • Ogden C.L.
        • Curtin L.R.
        Prevalence and trends in obesity among US adults, 1999-2008.
        JAMA. 2010; 303: 235-241
        • Church T.
        Exercise in obesity, metabolic syndrome, and diabetes.
        Prog Cardiovasc Dis. 2011; 53: 412-418
        • Villareal D.T.
        • Apovian C.M.
        • Kushner R.F.
        • Klein S.
        Obesity in older adults: Technical review and position statement of the American Society for Nutrition and NAASO, The Obesity Society.
        Obes Res. 2005; 13: 1849-1863
        • Reid I.R.
        Relationships among body mass, its components, and bone.
        Bone. 2002; 31: 547-555
        • Jensen L.B.
        • Quaade F.
        • Sorensen O.H.
        Bone loss accompanying voluntary weight loss in obese humans.
        J Bone Miner Res. 1994; 9: 459-463
        • Pritchard J.E.
        • Nowson C.A.
        • Wark J.D.
        Bone loss accompanying diet-induced or exercise-induced weight loss: A randomised controlled study.
        Int J Obes Relat Metab Disord. 1996; 20: 513-520
        • Johnston C.S.
        • Tjonn S.L.
        • Swan P.D.
        High-protein, low-fat diets are effective for weight loss and favorably alter biomarkers in healthy adults.
        J Nutr. 2004; 134: 586-591
        • Westerterp-Plantenga M.S.
        • Rolland V.
        • Wilson S.A.
        • Westerterp K.R.
        Satiety related to 24 h diet-induced thermogenesis during high protein/carbohydrate vs high fat diets measured in a respiration chamber.
        Eur J Clin Nutr. 1999; 53: 495-502
        • Layman D.K.
        • Boileau R.A.
        • Erickson D.J.
        • et al.
        A reduced ratio of dietary carbohydrate to protein improves body composition and blood lipid profiles during weight loss in adult women.
        J Nutr. 2003; 133: 411-417
        • Leidy H.J.
        • Carnell N.S.
        • Mattes R.D.
        • Campbell W.W.
        Higher protein intake preserves lean mass and satiety with weight loss in pre-obese and obese women.
        Obesity (Silver Spring). 2007; 15: 421-429
        • Farnsworth E.
        • Luscombe N.D.
        • Noakes M.
        • Wittert G.
        • Argyiou E.
        • Clifton P.M.
        Effect of a high-protein, energy-restricted diet on body composition, glycemic control, and lipid concentrations in overweight and obese hyperinsulinemic men and women.
        Am J Clin Nutr. 2003; 78: 31-39
        • Heaney R.P.
        Dairy and bone health.
        J Am Coll Nutr. 2009; 28: 82S-90S
        • Conigrave A.D.
        • Brown E.M.
        • Rizzoli R.
        Dietary protein and bone health: Roles of amino acid-sensing receptors in the control of calcium metabolism and bone homeostasis.
        Annu Rev Nutr. 2008; 28: 131-155
        • Lutz J.
        Calcium balance and acid-base status of women as affected by increased protein intake and by sodium bicarbonate ingestion.
        Am J Clin Nutr. 1984; 39: 281-288
        • Sebastian A.
        • Morris Jr., R.C.
        Improved mineral balance and skeletal metabolism in postmenopausal women treated with potassium bicarbonate.
        N Engl J Med. 1994; 331: 279
        • Kerstetter J.E.
        • Allen L.H.
        Dietary protein increases urinary calcium.
        J Nutr. 1990; 120: 134-136
        • Kerstetter J.E.
        • O'Brien K.O.
        • Insogna K.L.
        Dietary protein affects intestinal calcium absorption.
        Am J Clin Nutr. 1998; 68: 859-865
        • Schurch M.A.
        • Rizzoli R.
        • Slosman D.
        • Vadas L.
        • Vergnaud P.
        • Bonjour J.P.
        Protein supplements increase serum insulin-like growth factor-I levels and attenuate proximal femur bone loss in patients with recent hip fracture. A randomized, double-blind, placebo-controlled trial.
        Ann Intern Med. 1998; 128: 801-809
        • Heaney R.P.
        • McCarron D.A.
        • Dawson-Hughes B.
        • et al.
        Dietary changes favorably affect bone remodeling in older adults.
        J Am Diet Assoc. 1999; 99: 1228-1233
        • Dawson-Hughes B.
        • Harris S.S.
        • Rasmussen H.
        • Song L.
        • Dallal G.E.
        Effect of dietary protein supplements on calcium excretion in healthy older men and women.
        J Clin Endocrinol Metab. 2004; 89: 1169-1173
        • Geinoz G.
        • Rapin C.H.
        • Rizzoli R.
        • et al.
        Relationship between bone mineral density and dietary intakes in the elderly.
        Osteoporos Int. 1993; 3: 242-248
        • Hannan M.T.
        • Tucker K.L.
        • Dawson-Hughes B.
        • Cupples L.A.
        • Felson D.T.
        • Kiel D.P.
        Effect of dietary protein on bone loss in elderly men and women: The Framingham Osteoporosis Study.
        J Bone Miner Res. 2000; 15: 2504-2512
        • Delmi M.
        • Rapin C.H.
        • Bengoa J.M.
        • Delmas P.D.
        • Vasey H.
        • Bonjour J.P.
        Dietary supplementation in elderly patients with fractured neck of the femur.
        Lancet. 1990; 335: 1013-1016
        • Darling A.L.
        • Millward D.J.
        • Torgerson D.J.
        • Hewitt C.E.
        • Lanham-New S.A.
        Dietary protein and bone health: A systematic review and meta-analysis.
        Am J Clin Nutr. 2009; 90: 1674-1692
        • Guadalupe-Grau A.
        • Fuentes T.
        • Guerra B.
        • Calbet J.A.
        Exercise and bone mass in adults.
        Sports Med. 2009; 39: 439-468
      1. Methodology: What is the Academy of Nutrition and Dietetics (formerly American Dietetic Association) Evidence Analysis Process? http://andevidencelibrary.com/category.cfm?cid=7&cat=0&CFID=15457634&CFTOKEN=c98e770554b4023b-0CCF5547-2219-1F3D-44FECC71A3FFE975&jsessionid=58309f801e4869431070113d142a53e5a653. Accessed September 16, 2013.

        • Ricci T.A.
        • Chowdhury H.A.
        • Heymsfield S.B.
        • Stahl T.
        • Pierson Jr., R.N.
        • Shapses S.A.
        Calcium supplementation suppresses bone turnover during weight reduction in postmenopausal women.
        J Bone Miner Res. 1998; 13: 1045-1050
        • Reid I.R.
        • Ames R.W.
        • Evans M.C.
        • Gamble G.D.
        • Sharpe S.J.
        Effect of calcium supplementation on bone loss in postmenopausal women.
        N Engl J Med. 1993; 328: 460-464
        • Campbell W.W.
        • Tang M.
        Protein intake, weight loss, and bone mineral density in postmenopausal women.
        J Gerontol A Biol Sci Med Sci. 2010; 65: 1115-1122
        • Bowen J.
        • Noakes M.
        • Clifton P.M.
        A high dairy protein, high-calcium diet minimizes bone turnover in overweight adults during weight loss.
        J Nutr. 2004; 134: 568-573
        • Skov A.R.
        • Haulrik N.
        • Toubro S.
        • Molgaard C.
        • Astrup A.
        Effect of protein intake on bone mineralization during weight loss: A 6-month trial.
        Obes Res. 2002; 10: 432-438
        • Thorpe M.P.
        • Jacobson E.H.
        • Layman D.K.
        • He X.
        • Kris-Etherton P.M.
        • Evans E.M.
        A diet high in protein, dairy, and calcium attenuates bone loss over twelve months of weight loss and maintenance relative to a conventional high-carbohydrate diet in adults.
        J Nutr. 2008; 138: 1096-1100
        • Sukumar D.
        • Ambia-Sobhan H.
        • Zurfluh R.
        • et al.
        Areal and volumetric bone mineral density and geometry at two levels of protein intake during caloric restriction: A randomized, controlled trial.
        J Bone Miner Res. 2011; 26: 1339-1348
        • Li Z.
        • Treyzon L.
        • Chen S.
        • Yan E.
        • Thames G.
        • Carpenter C.L.
        Protein-enriched meal replacements do not adversely affect liver, kidney or bone density: An outpatient randomized controlled trial.
        Nutr J. 2010; 9: 72
        • Noakes M.
        • Keogh J.B.
        • Foster P.R.
        • Clifton P.M.
        Effect of an energy-restricted, high-protein, low-fat diet relative to a conventional high-carbohydrate, low-fat diet on weight loss, body composition, nutritional status, and markers of cardiovascular health in obese women.
        Am J Clin Nutr. 2005; 81: 1298-1306
        • Josse A.R.
        • Atkinson S.A.
        • Tarnopolsky M.A.
        • Phillips S.M.
        Diets higher in dairy foods and dietary protein support bone health during diet- and exercise-induced weight loss in overweight and obese premenopausal women.
        J Clin Endocrinol Metab. 2012; 97: 251-260
        • Barzel U.S.
        • Massey L.K.
        Excess dietary protein can adversely affect bone.
        J Nutr. 1998; 128: 1051-1053
        • Patience J.F.
        A review of the role of acid-base balance in amino acid nutrition.
        J Anim Sci. 1990; 68: 398-408
        • Sellmeyer D.E.
        • Stone K.L.
        • Sebastian A.
        • Cummings S.R.
        A high ratio of dietary animal to vegetable protein increases the rate of bone loss and the risk of fracture in postmenopausal women. Study of Osteoporotic Fractures Research Group.
        Am J Clin Nutr. 2001; 73: 118-122
        • Feskanich D.
        • Willett W.C.
        • Stampfer M.J.
        • Colditz G.A.
        Protein consumption and bone fractures in women.
        Am J Epidemiol. 1996; 143: 472-479
        • Bonjour J.P.
        Dietary protein: An essential nutrient for bone health.
        J Am Coll Nutr. 2005; 24: 526S-536S
        • Whiting S.J.
        • Anderson D.J.
        • Weeks S.J.
        Calciuric effects of protein and potassium bicarbonate but not of sodium chloride or phosphate can be detected acutely in adult women and men.
        Am J Clin Nutr. 1997; 65: 1465-1472
        • Frassetto L.A.
        • Morris Jr., R.C.
        • Sebastian A.
        Effect of age on blood acid-base composition in adult humans: Role of age-related renal functional decline.
        Am J Physiol. 1996; 271: F1114-F1122
        • Roughead Z.K.
        • Hunt J.R.
        • Johnson L.K.
        • Badger T.M.
        • Lykken G.I.
        Controlled substitution of soy protein for meat protein: Effects on calcium retention, bone, and cardiovascular health indices in postmenopausal women.
        J Clin Endocrinol Metab. 2005; 90: 181-189
        • Kenny A.M.
        • Mangano K.M.
        • Abourizk R.H.
        • et al.
        Soy proteins and isoflavones affect bone mineral density in older women: A randomized controlled trial.
        Am J Clin Nutr. 2009; 90: 234-242
        • Massey L.K.
        Dietary animal and plant protein and human bone health: A whole foods approach.
        J Nutr. 2003; 133: 862S-865S
        • New S.A.
        Intake of fruit and vegetables: Implications for bone health.
        Proc Nutr Soc. 2003; 62: 889-899
        • Heaney R.P.
        Calcium, dairy products and osteoporosis.
        J Am Coll Nutr. 2000; 19: 83S-99S
        • Howard J.E.
        Calcium metabolism, bones and calcium homeostasis; a review of certain current concepts.
        J Clin Endocrinol Metab. 1957; 17: 1105-1123
        • Hasling C.
        • Charles P.
        • Jensen F.T.
        • Mosekilde L.
        Calcium metabolism in postmenopausal osteoporosis: The influence of dietary calcium and net absorbed calcium.
        J Bone Miner Res. 1990; 5: 939-946
        • Horowitz M.
        • Need A.G.
        • Morris H.A.
        • Wishart J.
        • Nordin B.E.
        Biochemical effects of calcium supplementation in postmenopausal osteoporosis.
        Eur J Clin Nutr. 1988; 42: 775-778
        • Riggs B.L.
        • O'Fallon W.M.
        • Muhs J.
        • O'Connor M.K.
        • Kumar R.
        • Melton 3rd, L.J.
        Long-term effects of calcium supplementation on serum parathyroid hormone level, bone turnover, and bone loss in elderly women.
        J Bone Miner Res. 1998; 13: 168-174
        • Andon M.B.
        • Smith K.T.
        • Bracker M.
        • Sartoris D.
        • Saltman P.
        • Strause L.
        Spinal bone density and calcium intake in healthy postmenopausal women.
        Am J Clin Nutr. 1991; 54: 927-929
        • Cumming R.G.
        • Cummings S.R.
        • Nevitt M.C.
        • et al.
        Calcium intake and fracture risk: Results from the study of osteoporotic fractures.
        Am J Epidemiol. 1997; 145: 926-934
        • Heaney R.P.
        Calcium in the prevention and treatment of osteoporosis.
        J Intern Med. 1992; 231: 169-180
        • Kerstetter J.E.
        • O'Brien K.O.
        • Insogna K.L.
        Dietary protein, calcium metabolism, and skeletal homeostasis revisited.
        Am J Clin Nutr. 2003; 78: 584S-592S
        • Kerstetter J.E.
        • O'Brien K.O.
        • Insogna K.L.
        Low protein intake: The impact on calcium and bone homeostasis in humans.
        J Nutr. 2003; 133: 855S-861S
        • Kerstetter J.E.
        • O'Brien K.O.
        • Insogna K.L.
        Dietary protein affects intestinal calcium absorption.
        Am J Clin Nutr. 1998; 68: 859-865
        • Kerstetter J.E.
        • O'Brien K.O.
        • Caseria D.M.
        • Wall D.E.
        • Insogna K.L.
        The impact of dietary protein on calcium absorption and kinetic measures of bone turnover in women.
        J Clin Endocrinol Metab. 2005; 90: 26-31
        • Roughead Z.K.
        • Johnson L.K.
        • Lykken G.I.
        • Hunt J.R.
        Controlled high meat diets do not affect calcium retention or indices of bone status in healthy postmenopausal women.
        J Nutr. 2003; 133: 1020-1026
        • Hunt J.R.
        • Johnson L.K.
        • Fariba Roughead Z.K.
        Dietary protein and calcium interact to influence calcium retention: a controlled feeding study.
        Am J Clin Nutr. 2009; 89: 1357-1365
        • Cao J.J.
        • Johnson L.K.
        • Hunt J.R.
        A diet high in meat protein and potential renal acid load increases fractional calcium absorption and urinary calcium excretion without affecting markers of bone resorption or formation in postmenopausal women.
        J Nutr. 2011; 141: 391-397
        • Dawson-Hughes B.
        Interaction of dietary calcium and protein in bone health in humans.
        J Nutr. 2003; 133: 852S-854S
        • Langdahl B.L.
        • Kassem M.
        • Moller M.K.
        • Eriksen E.F.
        The effects of IGF-I and IGF-II on proliferation and differentiation of human osteoblasts and interactions with growth hormone.
        Eur J Clin Invest. 1998; 28: 176-183
        • Palmer G.
        • Bonjour J.P.
        • Caverzasio J.
        Stimulation of inorganic phosphate transport by insulin-like growth factor I and vanadate in opossum kidney cells is mediated by distinct protein tyrosine phosphorylation processes.
        Endocrinology. 1996; 137: 4699-4705
        • Giustina A.
        • Mazziotti G.
        • Canalis E.
        Growth hormone, insulin-like growth factors, and the skeleton.
        Endocr Rev. 2008; 29: 535-559
        • Arjmandi B.H.
        • Khalil D.A.
        • Smith B.J.
        • et al.
        Soy protein has a greater effect on bone in postmenopausal women not on hormone replacement therapy, as evidenced by reducing bone resorption and urinary calcium excretion.
        J Clin Endocrinol Metab. 2003; 88: 1048-1054
        • Langlois J.A.
        • Rosen C.J.
        • Visser M.
        • et al.
        Association between insulin-like growth factor I and bone mineral density in older women and men: The Framingham Heart Study.
        J Clin Endocrinol Metab. 1998; 83: 4257-4262
        • Rizzoli R.
        • Bianchi M.L.
        • Garabedian M.
        • McKay H.A.
        • Moreno L.A.
        Maximizing bone mineral mass gain during growth for the prevention of fractures in the adolescents and the elderly.
        Bone. 2010; 46: 294-305
        • Chevalley T.
        • Rizzoli R.
        • Manen D.
        • Caverzasio J.
        • Bonjour J.P.
        Arginine increases insulin-like growth factor-1 production and collagen synthesis in osteoblast-like cells.
        Bone. 1998; 23: 103-109
        • Cadogan J.
        • Eastell R.
        • Jones N.
        • Barker M.E.
        Milk intake and bone mineral acquisition in adolescent girls: Randomised, controlled intervention trial.
        BMJ. 1997; 315: 1255-1260
        • Budek A.Z.
        • Hoppe C.
        • Michaelsen K.F.
        • Bugel S.
        • Molgaard C.
        Associations of total, dairy, and meat protein with markers for bone turnover in healthy, prepubertal boys.
        J Nutr. 2007; 137: 930-934
        • Larsson S.C.
        • Wolk K.
        • Brismar K.
        • Wolk A.
        Association of diet with serum insulin-like growth factor I in middle-aged and elderly men.
        Am J Clin Nutr. 2005; 81: 1163-1167
        • Bonjour J.P.
        • Schurch M.A.
        • Chevalley T.
        • Ammann P.
        • Rizzoli R.
        Protein intake, IGF-1 and osteoporosis.
        Osteoporos Int. 1997; 7: S36-S42
      2. Nutrition and Your Health: Dietary Guidelines for Americans, 2005. 6th ed. US Government Printing Office, Washington, DC2005
        • Recker R.R.
        • Heaney R.P.
        The effect of milk supplements on calcium metabolism, bone metabolism and calcium balance.
        Am J Clin Nutr. 1985; 41: 254-263
        • Cheng S.
        • Lyytikainen A.
        • Kroger H.
        • et al.
        Effects of calcium, dairy product, and vitamin D supplementation on bone mass accrual and body composition in 10-12-y-old girls: A 2-y randomized trial.
        Am J Clin Nutr. 2005; 82: 1115-1126
        • Gueguen L.
        • Pointillart A.
        The bioavailability of dietary calcium.
        J Am Coll Nutr. 2000; 19: 119S-136S
        • Aoe S.
        • Koyama T.
        • Toba Y.
        • Itabashi A.
        • Takada Y.
        A controlled trial of the effect of milk basic protein (MBP) supplementation on bone metabolism in healthy menopausal women.
        Osteoporos Int. 2005; 16: 2123-2128
        • Uenishi K.
        • Ishida H.
        • Toba Y.
        • Aoe S.
        • Itabashi A.
        • Takada Y.
        Milk basic protein increases bone mineral density and improves bone metabolism in healthy young women.
        Osteoporos Int. 2007; 18: 385-390
        • Christiansen P.
        The skeleton in primary hyperparathyroidism: A review focusing on bone remodeling, structure, mass, and fracture.
        APMIS Suppl. 2001; 102: 1-52
        • Heaney R.P.
        The bone remodeling transient: Interpreting interventions involving bone-related nutrients.
        Nutr Rev. 2001; 59: 327-334
        • Elders P.J.
        • Lips P.
        • Netelenbos J.C.
        • et al.
        Long-term effect of calcium supplementation on bone loss in perimenopausal women.
        J Bone Miner Res. 1994; 9: 963-970
        • Heaney R.P.
        The bone-remodeling transient: implications for the interpretation of clinical studies of bone mass change.
        J Bone Miner Res. 1994; 9: 1515-1523
        • Wahner H.W.
        • Dunn W.L.
        • Brown M.L.
        • Morin R.L.
        • Riggs B.L.
        Comparison of dual-energy x-ray absorptiometry and dual photon absorptiometry for bone mineral measurements of the lumbar spine.
        Mayo Clin Proc. 1988; 63: 1075-1084
        • Prentice A.
        • Parsons T.J.
        • Cole T.J.
        Uncritical use of bone mineral density in absorptiometry may lead to size-related artifacts in the identification of bone mineral determinants.
        Am J Clin Nutr. 1994; 60: 837-842
        • Van Loan M.D.
        • Johnson H.L.
        • Barbieri T.F.
        Effect of weight loss on bone mineral content and bone mineral density in obese women.
        Am J Clin Nutr. 1998; 67: 734-738
        • Yoganandan N.
        • Pintar F.A.
        • Stemper B.D.
        • et al.
        Bone mineral density of human female cervical and lumbar spines from quantitative computed tomography.
        Spine (Phila Pa 1976). 2006; 31: 73-76
        • Villareal D.T.
        • Kotyk J.J.
        • Armamento-Villareal R.C.
        • et al.
        Reduced bone mineral density is not associated with significantly reduced bone quality in men and women practicing long-term calorie restriction with adequate nutrition.
        Aging Cell. 2011; 10: 96-102

      Biography

      M. Tang is a postdoctoral research associate, University of Colorado Denver; at the time of the study, she was a graduate student, Nutrition Science department, Purdue University, West Lafayette, IN.

      Biography

      L. E. O'Connor is a research technician, Department of Nutrition Science, Purdue University, West Lafayette, IN.

      Biography

      W. W. Campbell is a professor of nutrition science, Department of Nutrition Science, Purdue University, West Lafayette, IN.