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Association of protein intake with bone mineral density and bone mineral content among elderly women: The OSTPRE fracture prevention study

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The journal of nutrition, health & aging

Abstract

Abstract

It has been hypothesized that high protein intakes are associated with lower bone mineral content (BMC). Previous studies yield conflicting results and thus far no studies have undertaken the interaction of body mass index (BMI) and physical activity with protein intakes in relation to BMC and bone mineral density (BMD).

Objective

To evaluate the associations of dietary total protein (TP), animal protein (AP) and plant protein (PP) intakes with BMC and BMD and their changes. We tested also the interactions of protein intake with, obesity (BMI ≤30 vs. >30 kg/m2) and physical activity level (passive vs. active).

Design/ Setting

Prospective cohort study (Osteoporosis Risk-Factor and Fracture-Prevention Study).

Participants/measures

At the baseline, 554 women aged 65-72 years filled out a 3-day food record and a questionnaire covering data on lifestyle, physical activity, diseases, and medications. Intervention group received calcium 1000 mg/d and cholecalciferol 800 IU for 3 years. Control group received neither supplementation nor placebo. Bone density was measured at baseline and year 3, using dual energy x-ray absorptiometry. Multivariable regression analyses were conducted to examine the associations between protein intake and BMD and BMC.

Results

In cross-sectional analyses energy-adjusted TP (P≤0·029) and AP (P≤0·045) but not PP (g/d) were negatively associated with femoral neck (FN) BMD and BMC. Women with TP≥1·2 g/kg/body weight (BW) (Ptrend≤0·009) had lower FN, lumbar spine (LS) and total BMD and BMC. In follow-up analysis, TP (g/kg/BW) was inversely associated with LS BMD and LS BMC. The detrimental associations were stronger in women with BMI<30 kg/m2. In active women, TP (g/kg/BW) was positively associated with LS BMD and FN BMC changes.

Conclusions

This study suggests detrimental associations between protein intake and bone health. However, these negative associations maybe counteracted by BMI>30 kg/m2 and physical activity.

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References

  1. Simonen O. Osteoporosis: a big challenge to public health. Calcif.Tissue Int. 1986.5: 295-296.

  2. Nguyen ND, Pongchaiyakul C, Center JR, Eisman JA, Nguyen TV. Identification of High-Risk Individuals for Hip Fracture: A 14-Year Prospective Study. J Bone Miner Res 2005,11: 1921-1928.

  3. Tang M, O’Connor L, Campbell W. Diet-induced weight loss: the effect of dietary protein on bone. J Acad Nutr Diet 2014,1: 72-85.

  4. Mangano KM, Walsh SJ, Kenny AM, Insogna KL, Kerstetter JE. Dietary acid load is associated with lower bone mineral density in men with low intake of dietary calcium. J.Bone Miner.Res. 2014;2: 500–506.

    Article  Google Scholar 

  5. Emaus N, Wilsgaard T, Ahmed LA. Impacts of Body Mass Index, Physical Activity, and Smoking on Femoral Bone Loss: The Tromsø Study. J Bone Miner Res 2014;9: 2080–2089.

    Article  Google Scholar 

  6. Darling AL, Millward DJ, Torgerson DJ, Hewitt CE, Lanham-New SA. Dietary protein and bone health: a systematic review and meta-analysis. Am.J.Clin.Nutr. 2009;6: 1674–1692.

    Article  Google Scholar 

  7. Mangano KM, Sahni S, Kerstetter JE. Dietary protein is beneficial to bone health under conditions of adequate calcium intake: an update on clinical research. Curr. Opin.Clin.Nutr.Metab.Care 2014;1: 69–74.

    Google Scholar 

  8. Thorpe MP, Evans EM. Dietary protein and bone health: harmonizing conflicting theories. Nutr.Rev. 2011;4: 215–230.

    Article  Google Scholar 

  9. Ricci E, Cipriani S, Chiaffarino F, Malvezzi M, Parazzini F. Soy isoflavones and bone mineral density in perimenopausal and postmenopausal Western women: a systematic review and meta-analysis of randomized controlled trials. J.Womens Health.(Larchmt) 2010;9: 1609–1617.

    Article  Google Scholar 

  10. Jasien J, Daimon CM, Maudsley S, Shapiro BK, Martin B. Aging and bone health in individuals with developmental disabilities. Int.J.Endocrinol. 2012; 469235.

  11. Gregorio L, Brindisi J, Kleppinger A, Sullivan R, Mangano KM, Bihuniak JD, Kenny AM, Kerstetter JE, Insogna KL. Adequate dietary protein is associated with better physical performance among post-menopausal women 60-90 years. J.Nutr.Health Aging 2014;2: 155–160.

    Article  Google Scholar 

  12. Calvez J, Poupin N, Chesneau C, Lassale C, Tome D. Protein intake, calcium balance and health consequences. Eur.J.Clin.Nutr. 2012;3: 281–295.

    Article  Google Scholar 

  13. Sahni S, Cupples L, Mclean R, Tucker K, Broe K, Kiel D, Hannan M. Protective Effect of High Protein and Calcium Intake on the Risk of Hip Fracture in the Framingham Offspring Cohort. 2010;12: 2770–2775.

  14. Kerstetter JE, Allen LH. Dietary protein increases urinary calcium. J.Nutr. 1990;1: 134–136.

    Google Scholar 

  15. Salamat MR, Salamat AH, Abedi I, Janghorbani M. Relationship between Weight, Body Mass Index, and Bone Mineral Density in Men Referred for Dual-Energy X-Ray Absorptiometry Scan in Isfahan, Iran. J.Osteoporos 2013; 205963.

  16. Ho-Pham L, Nguyen UDT, Nguyen TV. Association Between Lean Mass, Fat Mass, and Bone Mineral Density: A Meta-analysis. 2014;1: 30–38.

  17. Polidoulis I, Beyene J, Cheung AM. The effect of exercise on pQCT parameters of bone structure and strength in postmenopausal women—a systematic review and meta-analysis of randomized controlled trials. Osteoporos.Int. 2012;1: 39–51.

    Article  Google Scholar 

  18. Holm L, Olesen JL, Matsumoto K, Doi T, Mizuno M, Alsted TJ, Mackey AL, Schwarz P, Kjaer M. Protein-containing nutrient supplementation following strength training enhances the effect on muscle mass, strength, and bone formation in postmenopausal women. J.Appl.Physiol 2008;1985;1: 274–281.

  19. Daly R, Duckham R, Gianoudis J. Evidence for an Interaction Between Exercise and Nutrition for Improving Bone and Muscle Health. Curr Osteoporos Rep 2014;2: 219–226.

    Article  Google Scholar 

  20. Karkkainen M, Tuppurainen M, Salovaara K, Sandini L, Rikkonen T, Sirola J, Honkanen R, Jurvelin J, Alhava E, Kroger H. Effect of calcium and vitamin D supplementation on bone mineral density in women aged 65-71 years: a 3-year randomized population-based trial (OSTPRE-FPS). Osteoporos.Int. 2010;12: 2047–2055.

    Article  Google Scholar 

  21. Miyabara Y, Holmes D, Camp J, Miller VM, Kearns AE. Comparison of calibrated and uncalibrated bone mineral density by CT to DEXA in menopausal women. Climacteric 2012;4: 374–381.

    Article  Google Scholar 

  22. Erkkila AT, Jarvinen R, Karvonen H, Keronen L, Tuppurainen MT. Study (OSTPRE-FPS). Public Health Nutr. 2012;4: 635–639.

    Article  Google Scholar 

  23. Department of Health. Dietary Reference Values for Food Energy and Nutrients for the United Kingdom. London, 1991.

  24. Goldberg GR, Black AE, Jebb SA, Cole TJ, Murgatroyd PR, Coward WA, Prentice AM. Critical evaluation of energy intake data using fundamental principles of energy physiology: 1. Derivation of cut-off limits to identify under-recording. Eur.J.Clin. Nutr. 1991;12: 569–581.

    Google Scholar 

  25. Black AE. Critical evaluation of energy intake using the Goldberg cut-off for energy intake:basal metabolic rate. A practical guide to its calculation, use and limitations. Int.J.Obes.Relat.Metab.Disord. 2000;9: 1119–1130.

    Article  Google Scholar 

  26. Isanejad M, Mursu J, Sirola J, Kroger H, Rikkonen T, Tuppurainen M, Erkkila AT. Dietary protein intake is associated with better physical function and muscle strength among elderly women. Br.J.Nutr. 2016;7: 1281–1291.

    Article  Google Scholar 

  27. Willett WC, Howe GR, Kushi LH. Adjustment for total energy intake in epidemiologic studies. Am.J.Clin.Nutr. 1997;4 Suppl: 1220S-1228S; discussion 1229S-1231S.

  28. Institute of Medicine of the National Academy of Sciences. Dietary Reference Intakes for Energy, Carbohydrate, Fiber, Fat, Fatty Acids, Cholesterol, Protein, and Amino Acids (Macronutrients), 2005.

  29. Bauer J, Biolo G, Cederholm T, Cesari M, Cruz-Jentoft AJ, Morley JE, Phillips S, Sieber C, Stehle P, Teta D, Visvanathan R, Volpi E, Boirie Y. Evidence-based recommendations for optimal dietary protein intake in older people: a position paper from the PROT-AGE Study Group. J.Am.Med.Dir.Assoc. 2013;8: 542–559.

    Article  Google Scholar 

  30. Nordic Nutrition Recommendations. Integrating nutrition and physical activity, 2012.

  31. Mason CH, Perreault WD. Collinearity, Power, and Interpretation of Multiple Regression Analysis. J.Market.Res. 1991;3: 268–280.

    Article  Google Scholar 

  32. Spiegelman D. Approaches to uncertainty in exposure assessment in environmental epidemiology. Annu.Rev.Public Health: 2010;149–163.

    Google Scholar 

  33. World Health Organization. Obesity: preventing and managing the global epidemic, 2000.

  34. Sahni S, Broe KE, Tucker KL, McLean RR, Kiel DP, Cupples LA, Hannan MT. Association of total protein intake with bone mineral density and bone loss in men and women from the Framingham Offspring Study. Public Health Nutr. 2014;11: 2570–2576.

    Article  Google Scholar 

  35. Ilich JZ, Brownbill RA, Tamborini L. Bone and nutrition in elderly women: protein, energy, and calcium as main determinants of bone mineral density. Eur.J.Clin.Nutr. 2003;4: 554–565.

    Article  Google Scholar 

  36. Beasley JM, LaCroix AZ, Larson JC, Huang Y, Neuhouser ML, Tinker LF, Jackson R, Snetselaar L, Johnson KC, Eaton CB, Prentice RL. Biomarker-calibrated protein intake and bone health in the Women’s Health Initiative clinical trials and observational study. Am.J.Clin.Nutr. 2014;4: 934–940.

    Article  Google Scholar 

  37. Darling AL, Hart KH, Lanham-New SA. Increased dietary protein is strongly associated with reduced bone mineral density and bone mineral content at the femoral neck and lumbar spine in UK dwelling South Asian and Caucasian postmenopausal women. Proc.Nutr.Soc. 2011; (OCE4), E123.

    Google Scholar 

  38. Cao JJ, Johnson LK, Hunt JR. 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;3: 391–397.

    Article  Google Scholar 

  39. Thorpe MP, Jacobson EH, Layman DK, He X, Kris-Etherton PM, Evans EM. 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;6: 1096–1100.

    Google Scholar 

  40. Sellmeyer D, Stone K, Sebastian A, Cummings S. A high ratio of dietary animal to vegetable protein increases the rate of bone loss and the risk of fracture in postmenopausal women. Am J Clin Nutr 2001;1: 118–122.

    Google Scholar 

  41. Hu T, Rianon NJ, Nettleton JA, Hyder JA, He J, Steffen LM, Jacobs DR, Criqui MH, Bazzano LA. Protein intake and lumbar bone density: the Multi-Ethnic Study of Atherosclerosis (MESA). Br.J.Nutr. 2014;8: 1384–1392.

    Article  Google Scholar 

  42. Thorpe M, Mojtahedi M, Chapman-Novakofski K, McAuley E, Evans E. A positive association of dietary protein with lumbar spine bone mineral density is suppressed by a negative association of protein sulfur. 2008;1: 80–85.

    Google Scholar 

  43. Langsetmo L, Barr SI, Berger C, Kreiger N, Rahme E, Adachi JD, Papaioannou A, Kaiser SM, Prior JC, Hanley DA, Kovacs CS, Josse RG, Goltzman D, CaMos Research Group. Associations of Protein Intake and Protein Source with Bone Mineral Density and Fracture Risk: A Population-Based Cohort Study. J.Nutr.Health Aging 2015;8: 861–868.

    Article  Google Scholar 

  44. Lim S, Joung H, Shin CS, Lee HK, Kim KS, Shin EK, Kim HY, Lim MK, Cho SI. Body composition changes with age have gender-specific impacts on bone mineral density. Bone 2004;3: 792–798.

    Article  Google Scholar 

  45. Migliaccio S, Greco EA, Fornari R, Donini LM, Lenzi A. Is obesity in women protective against osteoporosis? Diabetes Metab.Syndr.Obes. 2011;273–282.

    Google Scholar 

  46. Zhao L, Jiang H, Papasian CJ, Maulik D, Drees B, Hamilton J, Deng H. Correlation of Obesity and Osteoporosis: Effect of Fat Mass on the Determination of Osteoporosis. 2008;1: 17–29.

    Google Scholar 

  47. Yang S, Shen X. Association and relative importance of multiple obesity measures with bone mineral density: the National Health and Nutrition Examination Survey 2005-2006. Arch Osteoporos 2015;1: 219–015-0219-2. Epub 2015 May 9.

    Google Scholar 

  48. Luhrmann PM, Herbert BM, Gaster C, Neuhauser-Berthold M. Validation of a selfadministered 3-day estimated dietary record for use in the elderly. Eur.J.Nutr. 1999;5: 235–240.

    Google Scholar 

  49. Paddon-Jones D, Sheffield-Moore M, Katsanos CS, Zhang XJ, Wolfe RR. Differential stimulation of muscle protein synthesis in elderly humans following isocaloric ingestion of amino acids or whey protein. Exp.Gerontol. 2006;2: 215–219.

    Article  Google Scholar 

  50. Lord C, Chaput JP, Aubertin-Leheudre M, Labonte M, Dionne IJ. Dietary animal protein intake: association with muscle mass index in older women. J.Nutr.Health Aging 2007;5: 383–387.

    Google Scholar 

  51. Ho-Pham L, Nguyen ND, Lai TQ, Nguyen TV. Contributions of lean mass and fat mass to bone mineral density: a study in postmenopausal women. 2010;59–59.

    Google Scholar 

  52. Kurka J, Vezina J, Brown D, Schumacher J, Cullen R, Laurson K. Combined increases in muscle-strengthening activity frequency and protein intake reveal graded relationship with fat-free mass percentage in US adults, NHANES, 1999-2004.

    Google Scholar 

  53. van Loan MD, Johnson HL, Barbieri TF. Effect of weight loss on bone mineral content and bone mineral density in obese women. Am.J.Clin.Nutr. 1998;4: 734–738.

    Google Scholar 

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Correspondence to Masoud Isanejad.

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Isanejad, M., Sirola, J., Mursu, J. et al. Association of protein intake with bone mineral density and bone mineral content among elderly women: The OSTPRE fracture prevention study. J Nutr Health Aging 21, 622–630 (2017). https://doi.org/10.1007/s12603-016-0800-4

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