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Associations between Macronutrients Intake and Bone Mineral Density: A Longitudinal Analysis of the Health Workers Cohort Study Participants

  • Original Research
  • Published:
The journal of nutrition, health & aging

Abstract

Objective

This study aimed to evaluate the association between macronutrient intake and bone mineral density (BMD) using non-substitution and substitution statistical approaches.

Design

Longitudinal analysis.

Settings and Participants

1,317 adults in the Health Worker Cohort Study in Mexico.

Measurements

These participants were assessed at baseline (2004–2006) and follow-up (2010–2012). Dietary intakes were assessed using validated food frequency questionnaires. BMD at the different sites was performed by dual-energy X-ray absorptiometry (DXA). Hybrid-mixed effects regression models were performed to evaluate the associations of interest.

Results

Cross-sectional associations were found between fiber intake and higher total hip and femoral neck BMD in women and longitudinal associations with loss of femoral neck BMD in men. An increase in 5% energy intake from carbohydrate was associated with a BMD loss at several site in women and total hip and femoral neck in men. In both sexes, an increase in 5% energy intake of animal protein or fat was associated with a site-specific BMD gain after six years. Substitution analysis showed that the energy intake replacement from fat or carbohydrate by protein had an increase in BMD at different sites in women; while in men, it was only significant when replacing carbohydrate. Substitution of protein or fat by carbohydrates was associated with lower BMD in women, and only protein replacement by carbohydrates in men.

Conclusion

Our findings suggest that carbohydrate intake was associated with loss of BMD, while animal protein and fat intake was associated with gain of BMD among the Mexican population. Macronutrient substitutions resulted in significant associations; however, additional studies are needed to confirm these findings.

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References

  1. Yong E-L, Logan S. Menopausal osteoporosis: screening, prevention and treatment. Singapore Med J 2021;62:159–166.

    Article  PubMed  PubMed Central  Google Scholar 

  2. Minkin MJ. Menopause: Hormones, Lifestyle, and Optimizing Aging. Obstet Gynecol Clin North Am 2019;46:501–514.

    Article  PubMed  Google Scholar 

  3. Albergaria B-H, Chalem M, Clark P, Messina OD, Pereira RMR, Vidal LF. Consensus statement: osteoporosis prevention and treatment in Latin America-current structure and future directions. Arch Osteoporos 2018;13:90.

    Article  PubMed  PubMed Central  Google Scholar 

  4. Carlos F, Clark P, Galindo-Suárez RM, Chico-Barba LG. Health care costs of osteopenia, osteoporosis, and fragility fractures in Mexico. Arch Osteoporos 2013;8:125.

    Article  PubMed  Google Scholar 

  5. Muñoz-Garach A, García-Fontana B, Muñoz-Torres M. Nutrients and Dietary Patterns Related to Osteoporosis. Nutrients 2020;12. doi:https://doi.org/10.3390/nu12071986.

  6. Levis S, Lagari VS. The role of diet in osteoporosis prevention and management. Curr Osteoporos Rep 2012;. doi:https://doi.org/10.1007/s11914-012-0119-y.

  7. Lorincz C, Manske SL, Zernicke R. Bone health: part 1, nutrition. Sports Health 2009;1:253–260.

    Article  PubMed  PubMed Central  Google Scholar 

  8. Gao S, Qian X, Huang S, Deng W, Li Z, Hu Y. Association between macronutrients intake distribution and bone mineral density. Clin Nutr 2022;41:1689–1696.

    Article  CAS  PubMed  Google Scholar 

  9. Steell L, Sillars A, Welsh P, Iliodromiti S, Wong SC, Pell JP, Sattar N, Gill JMR, Celis-Morales CA, Gray SR. Associations of dietary protein intake with bone mineral density: An observational study in 70,215 UK Biobank participants. Bone 2019;120:38–43.

    Article  CAS  PubMed  Google Scholar 

  10. Dai Z, Jafarzadeh SR, Niu J, Felson DT, Jacques PF, Li S, Zhang Y. Body Mass Index Mediates the Association between Dietary Fiber and Symptomatic Knee Osteoarthritis in the Osteoarthritis Initiative and the Framingham Osteoarthritis Study. J Nutr 2018;148:1961–1967.

    Article  PubMed  PubMed Central  Google Scholar 

  11. Massey LK. Dietary animal and plant protein and human bone health: a whole foods approach. J Nutr 2003;133:862S–865S.

    Article  CAS  PubMed  Google Scholar 

  12. Kelly OJ, Gilman JC, Kim Y, Ilich JZ. Long-chain polyunsaturated fatty acids may mutually benefit both obesity and osteoporosis. Nutr Res 2013;33:521–533.

    Article  CAS  PubMed  Google Scholar 

  13. Cunha JS, Ferreira VM, Maquigussa E, Naves MA, Boim MA. Effects of high glucose and high insulin concentrations on osteoblast function in vitro. Cell Tissue Res 2014;358:249–256.

    Article  CAS  PubMed  Google Scholar 

  14. Sanguineti R, Puddu A, Mach F, Montecucco F, Viviani GL. Advanced glycation end products play adverse proinflammatory activities in osteoporosis. Mediators Inflamm 2014:975872.

  15. Miranda C, Giner M, Montoya MJ, Vázquez MA, Miranda MJ, Pérez-Cano R. Influence of high glucose and advanced glycation end-products (ages) levels in human osteoblast-like cells gene expression. BMC Musculoskelet Disord 2016;17:377.

    Article  PubMed  PubMed Central  Google Scholar 

  16. García-Gavilán JF, Bulló M, Camacho-Barcia L, Rosique-Esteban N, Hernández-Alonso P, Basora J, Martínez-González MA, Estruch R, Fitó M, Salas-Salvadó J. Higher dietary glycemic index and glycemic load values increase the risk of osteoporotic fracture in the PREvención con DIeta MEDiterránea (PREDIMED)-Reus trial. Am J Clin Nutr 2018;107:1035–1042.

    Article  PubMed  Google Scholar 

  17. Nouri M, Mahmoodi M, Shateri Z, Ghadiri M, Rajabzadeh-Dehkordi M, Vali M, Gargari BP. How do carbohydrate quality indices influence on bone mass density in postmenopausal women? A case-control study. BMC Womens Health 2023;23:42.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  18. Campbell WW, Tang M. Protein intake, weight loss, and bone mineral density in postmenopausal women. J Gerontol A Biol Sci Med Sci 2010;65:1115–1122.

    Article  PubMed  Google Scholar 

  19. Isanejad M, Sirola J, Mursu J, Kröger H, Tuppurainen M, Erkkilä AT. Association of Protein Intake with Bone Mineral Density and Bone Mineral Content among Elderly Women: The OSTPRE Fracture Prevention Study. J Nutr Health Aging 2017;21:622–630.

    Article  CAS  PubMed  Google Scholar 

  20. Rosato V, Temple NJ, La Vecchia C, Castellan G, Tavani A, Guercio V. Mediterranean diet and cardiovascular disease: a systematic review and meta-analysis of observational studies. Eur J Nutr 2019;58:173–191.

    Article  CAS  PubMed  Google Scholar 

  21. Schwingshackl L, Missbach B, König J, Hoffmann G. Adherence to a Mediterranean diet and risk of diabetes: a systematic review and meta-analysis. Public Health Nutr 2015;18:1292–1299.

    Article  PubMed  Google Scholar 

  22. Schwingshackl L, Hoffmann G. Adherence to Mediterranean diet and risk of cancer: an updated systematic review and meta-analysis of observational studies. Cancer Med 2015;4:1933–1947.

    Article  PubMed  PubMed Central  Google Scholar 

  23. Andreo-López MC, Contreras-Bolívar V, García-Fontana B, García-Fontana C, Muñoz-Torres M. The Influence of the Mediterranean Dietary Pattern on Osteoporosis and Sarcopenia. Nutrients 2023;15. doi:https://doi.org/10.3390/nu15143224.

  24. Bere E, Brug J. Towards health-promoting and environmentally friendly regional diets - a Nordic example. Public Health Nutr 2009;12:91–96.

    Article  PubMed  Google Scholar 

  25. Valerino-Perea S, Lara-Castor L, Armstrong MEG, Papadaki A. Definition of the Traditional Mexican Diet and Its Role in Health: A Systematic Review. Nutrients 2019;11. doi:https://doi.org/10.3390/nu11112803.

  26. Groenendijk I, Grootswagers P, Santoro A, Franceschi C, Bazzocchi A, Meunier N, Caille A, Malpuech-Brugere C, Bialecka-Debek A, Pietruszka B, Fairweather-Tait S, Jennings A, de Groot LCPGM. Protein intake and bone mineral density: Cross-sectional relationship and longitudinal effects in older adults. J Cachexia Sarcopenia Muscle 2023;14:116–125.

    Article  PubMed  Google Scholar 

  27. Lee T, Suh HS. Associations between Dietary Fiber Intake and Bone Mineral Density in Adult Korean Population: Analysis of National Health and Nutrition Examination Survey in 2011. J bone Metab 2019;26:151–160.

    Article  PubMed  PubMed Central  Google Scholar 

  28. Aburto TC, Batis C, Pedroza-Tobías A, Pedraza LS, Ramírez-Silva I, Rivera JA. Dietary intake of the Mexican population: comparing food group contribution to recommendations, 2012–2016. Salud Publica Mex 2022;64:267–279.

    Article  PubMed  Google Scholar 

  29. Rivera-Paredez B, Quezada-Sánchez AD, Denova-Gutiérrez E, Torres-Ibarra L, Flores YN, Salmerón J, Velázquez-Cruz R. Diet Modulates the Effects of Genetic Variants on the Vitamin D Metabolic Pathway and Bone Mineral Density in Mexican Postmenopausal Women. J Nutr 2021;151:1726–1735.

    Article  PubMed  PubMed Central  Google Scholar 

  30. Denova-Gutiérrez E, Flores YN, Gallegos-Carrillo K, et al. Health workers cohort study: methods and study design. Salud Publica Mex 2016;58:708–716.

    Article  PubMed  Google Scholar 

  31. Hernández-Avila M, Romieu I, Parra S. Validity and reproducibility of a food frequency questionnaire to assess dietary intake of women living in Mexico City. Salud Publica Mex 1998;39:133–140.

    Article  Google Scholar 

  32. Hernández-Avila M, Resoles M PS. Sistema de evaluación de hábitos nutricionales y consumo de nutrimentos (SNUT), 2000.

  33. Davis SR, Lambrinoudaki I, Lumsden M, Mishra GD, Pal L, Rees M, Santoro N, Simoncini T. Menopause. Nat Rev Dis Prim 2015;1:15004.

    Article  PubMed  Google Scholar 

  34. Emaus N, Berntsen GKR, Joakimsen R, Fonnebø V. Longitudinal changes in forearm bone mineral density in women and men aged 45–84 years: the Tromso Study, a population-based study. Am J Epidemiol 2006;163:441–449.

    Article  CAS  PubMed  Google Scholar 

  35. Who WHO, 1998. Obesity. Preventing and managing the global epidemic. Available at: https://iris.paho.org/handle/10665.2/43000. Accessed March 5, 2020.

  36. Who WHO, 2010. Global recommendations on physical activity for health. Geneva World Heal Organ. doi:https://doi.org/10.1080/11026480410034349.

  37. Committee ADAPP. 2. Classification and Diagnosis of Diabetes: Standards of Medical Care in Diabetes—2022. Diabetes Care 2021;45:S17–S38.

    Google Scholar 

  38. Allison P. Fixed Effects Regression Models 2009. doi:https://doi.org/10.4135/9781412993869.

  39. Jacob C. Statistical Power Analysis for the Behavioral Sciences. 2nd editio. Routledge, 1988. doi: https://doi.org/10.4324/9780203771587.

  40. Groenendijk I, den Boeft L, van Loon LJC, de Groot LCPGM. High Versus low Dietary Protein Intake and Bone Health in Older Adults: a Systematic Review and Meta-Analysis. Comput Struct Biotechnol J 2019;17:1101–1112.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  41. Shams-White MM, Chung M, Du M, Fu Z, Insogna KL, Karlsen MC, LeBoff MS, Shapses SA, Sackey J, Wallace TC, Weaver CM. Dietary protein and bone health: A systematic review and meta-analysis from the National Osteoporosis Foundation. Am J Clin Nutr, 2017. doi:https://doi.org/10.3945/ajcn.116.145110.

  42. Hannan MT, Tucker KL, Dawson-Hughes B, Cupples LA, Felson DT, Kiel DP. Effect of dietary protein on bone loss in elderly men and women: The Framingham Osteoporosis Study. J Bone Miner Res, 2000. doi:https://doi.org/10.1359/jbmr.2000.15.12.2504.

  43. Weaver AA, Tooze JA, Cauley JA, Bauer DC, Tylavsky FA, Kritchevsky SB, Houston DK. Effect of Dietary Protein Intake on Bone Mineral Density and Fracture Incidence in Older Adults in the Health, Aging, and Body Composition Study. J Gerontol A Biol Sci Med Sci 2021;76:2213–2222.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  44. Sellmeyer DE, Stone KL, Sebastian A, Cummings SR. 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.

    Article  CAS  PubMed  Google Scholar 

  45. Hu T, Rianon NJ, Nettleton JA, Hyder JA, He J, Steffen LM, Jacobs DRJ, Criqui MH, Bazzano LA. Protein intake and lumbar bone density: the Multi-Ethnic Study of Atherosclerosis (MESA). Br J Nutr 2014;112:1384–1392.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  46. Wallace TC, Frankenfeld CL. Dietary Protein Intake above the Current RDA and Bone Health: A Systematic Review and Meta-Analysis. J Am Coll Nutr 2017;36:481–496.

    Article  CAS  PubMed  Google Scholar 

  47. Promislow JHE, Goodman-Gruen D, Slymen DJ, Barrett-Connor E. Protein consumption and bone mineral density in the elderly: the Rancho Bernardo Study. Am J Epidemiol 2002;155:636–644.

    Article  PubMed  Google Scholar 

  48. 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. Associations of Protein Intake and Protein Source with Bone Mineral Density and Fracture Risk: A Population-Based Cohort Study. J Nutr Health Aging 2015;19:861–868.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  49. Beasley JM, Ichikawa LE, Ange BA, Spangler L, LaCroix AZ, Ott SM, Scholes D. Is protein intake associated with bone mineral density in young women? Am J Clin Nutr 2010;91:1311–1316.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  50. Itkonen ST, Päivärinta E, Pellinen T, Viitakangas H, Risteli J, Erkkola M, Lamberg-Allardt C, Pajari A-M. Partial Replacement of Animal Proteins with Plant Proteins for 12 Weeks Accelerates Bone Turnover Among Healthy Adults: A Randomized Clinical Trial. J Nutr 2021;151:11–19.

    Article  PubMed  Google Scholar 

  51. Bonjour J-P. Protein intake and bone health. Int J Vitam Nutr Res Int Zeitschrift fur Vitamin- und Ernahrungsforschung J Int Vitaminol Nutr 2011;81:134–142.

    Article  CAS  Google Scholar 

  52. Martiniakova M, Babikova M, Mondockova V, Blahova J, Kovacova V, Omelka R. The Role of Macronutrients, Micronutrients and Flavonoid Polyphenols in the Prevention and Treatment of Osteoporosis. Nutrients 2022;14. doi:https://doi.org/10.3390/nu14030523.

  53. 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;141:391–397.

    Article  CAS  PubMed  Google Scholar 

  54. Lim MT, Pan BJ, Toh DWK, Sutanto CN, Kim JE. Animal Protein versus Plant Protein in Supporting Lean Mass and Muscle Strength: A Systematic Review and Meta-Analysis of Randomized Controlled Trials. Nutrients 2021;13. doi:https://doi.org/10.3390/nu13020661.

  55. Ho-Pham LT, Nguyen UDT, Nguyen T V. Association between lean mass, fat mass, and bone mineral density: a meta-analysis. J Clin Endocrinol Metab 2014;99:30–38.

    Article  CAS  PubMed  Google Scholar 

  56. Reynolds A, Mann J, Cummings J, Winter N, Mete E, Te Morenga L. Carbohydrate quality and human health: a series of systematic reviews and meta-analyses. Lancet (London, England) 2019;393:434–445.

    Article  CAS  PubMed  Google Scholar 

  57. Denova-Gutiérrez E, Clark P, Tucker KL, Muñoz-Aguirre P, Salmerón J. Dietary patterns are associated with bone mineral density in an urban Mexican adult population. Osteoporos Int, 2016. doi:https://doi.org/10.1007/s00198-016-3633-4.

  58. Tucker KL, Chen H, Hannan MT, Adrienne Cupples L, Wilson PWF, Felson D, Kiel DP. Bone mineral density and dietary patterns in older adults: The Framingham Osteoporosis Study. Am J Clin Nutr, 2002.

  59. Han X, Feng Z, Chen Y, Zhu L, Li X, Wang X, Sun H, Li J. Effects of High-Fructose Corn Syrup on Bone Health and Gastrointestinal Microbiota in Growing Male Mice. Front Nutr 2022;9:829396.

    Article  PubMed  PubMed Central  Google Scholar 

  60. Quach D, Britton RA. Gut Microbiota and Bone Health. Adv Exp Med Biol 2017;1033:47–58.

    Article  CAS  PubMed  Google Scholar 

  61. Dai Z, Zhang Y, Lu N, Felson DT, Kiel DP, Sahni S. Association Between Dietary Fiber Intake and Bone Loss in the Framingham Offspring Study. J bone Miner Res Off J Am Soc Bone Miner Res 2018;33:241–249.

    Article  CAS  Google Scholar 

  62. Zhou T, Wang M, Ma H, Li X, Heianza Y, Qi L. Dietary Fiber, Genetic Variations of Gut Microbiota-derived Short-chain Fatty Acids, and Bone Health in UK Biobank. J Clin Endocrinol Metab 2021;106:201–210.

    Article  PubMed  Google Scholar 

  63. López-Olmedo N, Carriquiry AL, Rodríguez-Ramírez S, Ramírez-Silva I, Espinosa-Montero J, Hernández-Barrera L, Campirano F, Martínez-Tapia B, Rivera JA. Usual Intake of Added Sugars and Saturated Fats Is High while Dietary Fiber Is Low in the Mexican Population. J Nutr 2016;146:1856S–1865S.

    Article  PubMed  Google Scholar 

  64. Wang Y, Dellatore P, Douard V, Qin L, Watford M, Ferraris RP, Lin T, Shapses SA. High fat diet enriched with saturated, but not monounsaturated fatty acids adversely affects femur, and both diets increase calcium absorption in older female mice. Nutr Res 2016;36:742–750.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  65. Tolonen S, Juonala M, Fogelholm M, Pahkala K, Laaksonen M, Kähönen M, Sievänen H, Viikari J, Raitakari O. Dietary Saturated Fat and Bone Health in Young Adults: The Young Finns Cohort. Calcif Tissue Int 2022;111:419–429.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  66. Qiao J, Wu Y, Ren Y. The impact of a high fat diet on bones: potential mechanisms. Food Funct 2021;12:963–975.

    Article  CAS  PubMed  Google Scholar 

  67. El-Sayed E, Ibrahim K. Effect of the types of dietary fats and non-dietary oils on bone metabolism. Crit Rev Food Sci Nutr 2017;57:653–658.

    Article  CAS  PubMed  Google Scholar 

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Acknowledgments

We would like to sincerely thank the Health Workers Cohort Study team and the study subjects for their participation.

Funding

Funding statement: The Health Workers Cohort Study was supported by: Consejo Nacional de Ciencia y Tecnología (Grant numbers: 7876, 87783, 262233, 26267M, SALUD-2010-01-139796, SALUD-2011-01-161930, and CB-2013-01-221628).

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Authors and Affiliations

  1. Research Center in Policies, Population, and Health, School of Medicine, National Autonomous University of Mexico (UNAM), Mexico City, 04510, Mexico

    Berenice Rivera-Paredez, D. Rangel-Marín & J. Salmerón

  2. Genomics of Bone Metabolism Laboratory, National Institute of Genomic Medicine (INMEGEN), Mexico City, 14610, Mexico

    G. León-Reyes & Rafael Velázquez-Cruz

Authors
  1. Berenice Rivera-Paredez
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  2. G. León-Reyes
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  3. D. Rangel-Marín
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  4. J. Salmerón
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  5. Rafael Velázquez-Cruz
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Contributions

Author contributions: B.R.-P.: Conceptualization, Methodology, Data curation, Formal analysis, Writing- Original draft preparation. G.L.-R.: Conceptualization, Writing - Original Draft, Writing - Review & Editing. D.R.-M.: Writing - Review & Editing, J.S.: Writing-Reviewing and Editing. R.V.-C.: Conceptualization, Supervision, Writing- Reviewing and Editing. All authors gave their final approval and agreed to be accountable for all aspects of the work to ensure integrity and accuracy.

Corresponding authors

Correspondence to Berenice Rivera-Paredez or Rafael Velázquez-Cruz.

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Conflict of interest: Authors declare no conflict of interest.

Ethical statement and informed consent: All procedures were reviewed and approved by the Institutional Review Board of the IMSS (12CEI 09 006 14); all participants provided written informed consent.

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Rivera-Paredez, B., León-Reyes, G., Rangel-Marín, D. et al. Associations between Macronutrients Intake and Bone Mineral Density: A Longitudinal Analysis of the Health Workers Cohort Study Participants. J Nutr Health Aging 27, 1196–1205 (2023). https://doi.org/10.1007/s12603-023-2038-2

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  • DOI: https://doi.org/10.1007/s12603-023-2038-2

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