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Distribution of daily protein intake across meals and lower extremity functioning in community-dwelling Spanish older adults: a prospective cohort study

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Abstract

Purpose

Total dietary protein intake has been associated with better physical function in older adults. However, it is unclear whether an even mealtime distribution of protein intake also has an impact on physical functioning. The aim of this study was to examine the prospective association between distribution of daily protein intake across meals and the risk of impaired lower extremity function (ILEF).

Methods

We used information of 2975 individuals ≥ 60 years from the Seniors-ENRICA cohort. Habitual dietary protein intake was assessed in 2008–2010 with a validated diet history. For each participant, dietary protein intake across meals was determined using the coefficient of variation (CV) of the distribution. Study participants were followed up until 2017 to identify incident ILEF, assessed with the short physical performance battery (SPPB).

Results

Over a median follow-up of 6.3 years, we identified 521 participants with ILEF (SPPB ≤ 6). After adjusting for potential confounders including total protein intake/kg/day, a higher CV (less even distribution) of protein intake did not show an association with the risk of ILEF [hazard ratios (HR) and 95% confidence intervals (CI) for second and third vs. the first tertile: 1.08 (0.87–1.34), and 1.06 (0.85–1.32), respectively; p trend = 0.60]. When assessing each component of the SPPB, a higher CV of protein intake was associated with higher risk of impaired standing balance (HR for tertile 3 vs. tertile 1: 1.26 (1.03–1.54); p trend = 0.02).

Conclusion

The mealtime distribution of protein intake was not associated with ILEF. The possibility of a detrimental effect of uneven distribution of protein on standing balance needs to be further investigated.

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References

  1. United Nations, Department of Economic and Social Affairs PD (2017) World Population Ageing 2017—Highlights (ST/ESA/SER.A/397). https://www.un.org/en/development/desa/population/publications/pdf/ageing/WPA2017_Highlights.pdf. Accessed 23 May 2019

  2. World Health Organization (2017) Global strategy and action plan on ageing and health. WHO, Geneva. https://www.who.int/ageing/global-strategy/en/. Accessed 23 May 2019

  3. World Health Organization (2015) World report on ageing and health. WHO, Geneva. https://www.who.int/ageing/events/world-report-2015-launch/en/. Accessed 23 May 2019

  4. Cesari M, Penninx BW, Pahor M, Lauretani F, Corsi AM, Rhys-Williams G, Guralnik JM, Ferrucci L (2004) Inflammatory markers and physical performance in older persons: the InCHIANTI study. J Gerontol A Biol Sci Med Sci 59:242–248. https://doi.org/10.1093/gerona/59.3.M242

    Article  PubMed  Google Scholar 

  5. Semba RD, Ferrucci L, Sun K, Walston J, Varadhan R, Guralnik JM, Fried LP (2007) Oxidative stress and severe walking disability among older women. Am J Med 120:1084–1089. https://doi.org/10.1016/j.amjmed.2007.07.028

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  6. Guallar-Castillón P, Sagardui-Villamor J, Banegas JR, Graciani A, Fornés NS, López García E, Rodríguez-Artalejo F (2007) Waist circumference as a predictor of disability among older adults. Obesity 15:233–244. https://doi.org/10.1038/oby.2007.532

    Article  PubMed  Google Scholar 

  7. Sinclair A, Dunning T, Rodriguez-Mañas L (2015) Diabetes in older people: new insights and remaining challenges. Lancet Diabetes Endocrinol 3:275–285. https://doi.org/10.1016/S2213-8587(14)70176-7

    Article  PubMed  Google Scholar 

  8. Stefanick ML, Brunner RL, Leng X, Limacher MC, Bird CE, Garcia DO, Hogan PE, LaMonte MJ, Mackey RH, Johnson KC et al (2016) The relationship of cardiovascular disease to physical functioning in women surviving to age 80 and above in the women’s health initiative. J Gerontol A Biol Sci Med Sci 71:S42–S53. https://doi.org/10.1093/gerona/glv087

    Article  PubMed  PubMed Central  Google Scholar 

  9. Struijk EA, Banegas JR, Rodríguez-Artalejo F, Lopez-Garcia E (2018) Consumption of meat in relation to physical functioning in the seniors-ENRICA cohort. BMC Med 16:50. https://doi.org/10.1186/s12916-018-1036-4

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  10. Struijk EA, Lana A, Guallar-Castillón P, Rodríguez-Artalejo F, Lopez-Garcia E (2018) Intake of B vitamins and impairment in physical function in older adults. Clin Nutr 37:1271–1278. https://doi.org/10.1016/j.clnu.2017.05.016

    Article  CAS  PubMed  Google Scholar 

  11. Struijk EA, Guallar-Castillón P, Rodríguez-Artalejo F, López-García E (2018) Mediterranean dietary patterns and impaired physical function in older adults. J Gerontol A Biol Sci Med Sci 73:333–339. https://doi.org/10.1093/gerona/glw208

    Article  PubMed  Google Scholar 

  12. Arias-Fernández L, Machado-Fragua MD, Graciani A, Guallar-Castillón P, Banegas JR, Rodríguez-Artalejo F, Lana A, Lopez-Garcia E (2019) Prospective association between nut consumption and physical function in older men and women. J Gerontol A Biol Sci Med Sci 74:1091–1097. https://doi.org/10.1093/gerona/gly17

    Article  PubMed  Google Scholar 

  13. Farsijani S, Morais JA, Payette H, Gaudreau P, Shatenstein B, Gray-Donald K, Chevalier S (2016) Relation between mealtime distribution of protein intake and lean mass loss in free-living older adults of the NuAge study. Am J Clin Nutr 104:694–703. https://doi.org/10.3945/ajcn.116.130716

    Article  CAS  PubMed  Google Scholar 

  14. Gregorio L, Brindisi J, Kleppinger A, Sullivan R, Mangano KM, Bihuniak JD, Kenny AM, Kerstetter JE, Insogna KL (2014) Adequate dietary protein is associated with better physical performance among post-menopausal women 60–90 years. J Nutr Health Aging 18:155–160. https://doi.org/10.1007/s12603-013-0391-2

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  15. McLean RR, Mangano KM, Hannan MT, Kiel DP, Sahni S (2016) Dietary protein intake is protective against loss of grip strength among older adults in the Framingham Offspring Cohort. J Gerontol A Biol Sci Med Sci 71:356–361. https://doi.org/10.1093/gerona/glv184

    Article  CAS  PubMed  Google Scholar 

  16. Chernoff R (2004) Protein and older adults. J Am Coll Nutr 23:627S–630S. https://doi.org/10.1080/07315724.2004.10719434

    Article  CAS  PubMed  Google Scholar 

  17. Houston DK, Nicklas BJ, Ding J, Harris TB, Tylavsky FA, Newman AB, Lee JS, Sahyoun NR, Visser M, Kritchevsky SB (2008) Dietary protein intake is associated with lean mass change in older, community-dwelling adults: the Health, Aging, and Body Composition (Health ABC) Study. Am J Clin Nutr 87:150–155. https://doi.org/10.1093/ajcn/87.1.150

    Article  CAS  PubMed  Google Scholar 

  18. Gaffney-Stomberg E, Insogna KL, Rodriguez NR, Kerstetter JE (2009) Increasing dietary protein requirements in elderly people for optimal muscle and bone health. J Am Geriatr Soc 57:1073–1079. https://doi.org/10.1111/j.1532-5415.2009.02285.x

    Article  PubMed  Google Scholar 

  19. Coelho-Júnior HJ, Rodrigues B, Uchida M, Marzetti E (2018) Low protein intake is associated with frailty in older adults: a systematic review and meta-analysis of observational studies. Nutrients 10:1334. https://doi.org/10.3390/nu10091334

    Article  PubMed Central  Google Scholar 

  20. Coelho-Júnior HJ, Milano-Teixeira L, Rodrigues B, Bacurau R, Marzetti E, Uchida M (2018) Relative protein intake and physical function in older adults: a systematic review and meta-analysis of observational studies. Nutrients 10:1330. https://doi.org/10.3390/nu10091330

    Article  CAS  PubMed Central  Google Scholar 

  21. Farsijani S, Payette H, Morais JA, Shatenstein B, Gaudreau P, Chevalier S (2017) Even mealtime distribution of protein intake is associated with greater muscle strength, but not with 3-y physical function decline, in free-living older adults: the Quebec longitudinal study on Nutrition as a Determinant of Successful Aging (NuAge study). Am J Clin Nutr 106:113–124. https://doi.org/10.3945/ajcn.116.146555

    Article  CAS  PubMed  Google Scholar 

  22. Symons TB, Sheffield-Moore M, Wolfe RR, Paddon-Jones D (2009) Moderating the portion size of a protein-rich meal improves anabolic efficiency in young and elderly. J Am Diet Assoc 109:1582–1586. https://doi.org/10.1016/j.jada.2009.06.369

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  23. Mamerow MM, Mettler JA, English KL, Casperson SL, Arentson-Lantz E, Sheffield-Moore M, Layman DK, Paddon-Jones D (2014) Dietary protein distribution positively influences 24-h muscle protein synthesis in healthy adults. J Nutr 144:876–880. https://doi.org/10.3945/jn.113.185280

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  24. Bollwein J, Diekmann R, Kaiser MJ, Bauer JM, Uter W, Sieber CC, Volkert D (2013) Distribution but not amount of protein intake is associated with frailty: a cross-sectional investigation in the region of Nürnberg. Nutr J 12:109. https://doi.org/10.1186/1475-2891-12-109

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  25. Ten Haaf DSM, Van Dongen EJI, Nuijten MAH, Eijsvogels TMH, De Groot LCPGM, Hopman MTE (2018) Protein intake and distribution in relation to physical functioning and quality of life in community-dwelling elderly people: acknowledging the role of physical activity. Nutrients 10:506. https://doi.org/10.3390/nu10040506

    Article  CAS  PubMed Central  Google Scholar 

  26. Rodríguez-Artalejo F, Graciani A, Guallar-Castillón P, León-Muñoz LM, Zuluaga MC, López-García E, Gutiérrez-Fisac JL, Taboada JM, Aguilera MT, Regidor E et al (2011) Justificación y métodos del estudio sobre nutrición y riesgo cardiovascular en España (ENRICA). Rev Española Cardiol 64:876–882. https://doi.org/10.1016/j.recesp.2011.05.019

    Article  Google Scholar 

  27. León-Muñoz LM, García-Esquinas E, López-García E, Banegas JR, Rodríguez-Artalejo F (2015) Major dietary patterns and risk of frailty in older adults: a prospective cohort study. BMC Med 13:11. https://doi.org/10.1186/s12916-014-0255-6

    Article  PubMed  PubMed Central  Google Scholar 

  28. Guallar-Castillón P, Sagardui-Villamor J, Balboa-Castillo T, Sala-Vila A, Ariza Astolfi MJ, Sarrión Pelous MD, León-Muñoz LM, Graciani A, Laclaustra M, Benito C et al (2014) Validity and reproducibility of a Spanish Dietary History. PLoS ONE 9:e86074. https://doi.org/10.1371/journal.pone.0086074

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  29. Schröder H, Fitó M, Estruch R, Martínez-González MA, Corella D, Salas-Salvadó J, Lamuela-Raventós R, Ros E, Salaverría I, Fiol M et al (2011) A short screener is valid for assessing mediterranean diet adherence among older spanish men and women. J Nutr 141:1140–1145. https://doi.org/10.3945/jn.110.135566

    Article  CAS  PubMed  Google Scholar 

  30. Willett W, Rockström J, Loken B, Springmann M, Lang T, Vermeulen S, Garnett T, Tilman D, DeClerck F, Wood A et al (2019) Food in the anthropocene: the EAT-Lancet Commission on healthy diets from sustainable food systems. Lancet 393:447–492. https://doi.org/10.1016/S0140-6736(18)31788-4

    Article  PubMed  Google Scholar 

  31. Guralnik JM, Ferrucci L, Pieper CF, Leveille SG, Markides KS, Ostir GV, Studenski S, Berkman LF, Wallace RB (2000) Lower extremity function and subsequent disability: consistency across studies, predictive models, and value of gait speed alone compared with the short physical performance battery. J Gerontol A Biol Sci Med Sci 55:M221–M231. https://doi.org/10.1093/gerona/55.4.M221

    Article  CAS  PubMed  Google Scholar 

  32. Cruz-Jentoft AJ, Baeyens JP, Bauer JM, Boirie Y, Cederholm T, Landi F, Martin FC, Michel JP, Rolland Y, Schneider SM et al (2010) Sarcopenia: European consensus on definition and diagnosis: Report of the European Working Group on Sarcopenia in Older People. Age Ageing 39:412–423. https://doi.org/10.1093/ageing/afq034

    Article  PubMed  PubMed Central  Google Scholar 

  33. Ortolá R, García-Esquinas E, López-García E, León-Muñoz LM, Banegas JR, Rodríguez-Artalejo F (2019) Alcohol consumption and all-cause mortality in older adults in Spain: an analysis accounting for the main methodological issues. Addiction 114:59–68. https://doi.org/10.1111/add.14402

    Article  PubMed  Google Scholar 

  34. Pols MA, Peeters PH, Ocké MC, Slimani N, Bueno-de-Mesquita HB, Collette HJ (1997) Estimation of reproducibility and relative validity of the questions included in the EPIC Physical Activity Questionnaire. Int J Epidemiol 26:S181–S189. https://doi.org/10.1093/ije/26.suppl_1.S181

    Article  PubMed  Google Scholar 

  35. Huerta JM, Chirlaque MD, Tormo MJ, Buckland G, Ardanaz E, Arriola L, Gavrila D, Salmerón D, Cirera L, Carpe B et al (2016) Work, household, and leisure-time physical activity and risk of mortality in the EPIC-Spain cohort. Prev Med 85:106–112. https://doi.org/10.1016/j.ypmed.2016.02.009

    Article  PubMed  Google Scholar 

  36. Graciani A, Banegas JR, Guallar-Castillón P, Domínguez-Rojas V, Rodríguez-Artalejo F (2006) Cognitive assessment of the non-demented elderly community dwellers in Spain. Dement Geriatr Cogn Disord 21:104–112. https://doi.org/10.1159/000090509

    Article  PubMed  Google Scholar 

  37. Morley JE, Malmstrom TK, Miller DK (2012) A simple frailty questionnaire (FRAIL) predicts outcomes in middle aged African Americans. J Nutr Health Aging 16:601–608

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  38. Gingrich A, Spiegel A, Kob R, Schoene D, Skurk T, Hauner H, Sieber CC, Volkert D, Kieswetter E (2017) Amount, distribution, and quality of protein intake are not associated with muscle mass, strength, and power in healthy older adults without functional limitations—an enable study. Nutrients 9:1358. https://doi.org/10.3390/nu9121358

    Article  CAS  PubMed Central  Google Scholar 

  39. Institute of Medicine (2005) Dietary Reference Intakes for energy, carbohydrate, fiber, fat, fatty acids, cholesterol, protein, and amino acids (macronutrients). Washington, DC: The National Academies Press. https://doi.org/10.17226/10490 Accessed 27 May 2019

  40. Bauer J, Biolo G, Cederholm T, Cesari M, Cruz-Jentoft AJ, Morley JE, Phillips S, Sieber C, Stehle P, Teta D et al (2013) 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 14:542–559. https://doi.org/10.1016/j.jamda.2013.05.021

    Article  PubMed  Google Scholar 

  41. Scott D, Blizzard L, Fell J, Giles G, Jones G (2010) Associations between dietary nutrient intake and muscle mass and strength in community-dwelling older adults: the Tasmanian older adult cohort study. J Am Geriatr Soc 58:2129–2134. https://doi.org/10.1111/j.1532-5415.2010.03147.x

    Article  PubMed  Google Scholar 

  42. Wallace TC, Frankenfeld CL (2017) Dietary protein intake above the current RDA and bone health: a systematic review and meta-analysis. J Am Coll Nutr 36:481–496. https://doi.org/10.1080/07315724.2017.1322924

    Article  CAS  PubMed  Google Scholar 

  43. Rizzoli R, Biver E, Bonjour JP, Coxam V, Goltzman D, Kanis JA, Lappe J, Rejnmark L, Sahni S, Weaver C et al (2018) Benefits and safety of dietary protein for bone health—an expert consensus paper endorsed by the European Society for Clinical and Economical Aspects of Osteopororosis, Osteoarthritis, and Musculoskeletal Diseases and by the International Osteoporosis Foundation. Osteoporos Int 29:1933–1948. https://doi.org/10.1007/s00198-018-4534-5

    Article  CAS  PubMed  Google Scholar 

  44. Promislow JHE, Goodman-Gruen D, Slymen DJ, Barrett-Connor E (2002) Protein consumption and bone mineral density in the elderly: the Rancho Bernardo Study. Am J Epidemiol 155:636–644. https://doi.org/10.1093/aje/155.7.636

    Article  PubMed  Google Scholar 

  45. Fielding RA, Vellas B, Evans WJ, Bhasin S, Morley JE, Newman AB, Abellan van Kan G, Andrieu S, Bauer J, Breuille D et al (2011) Sarcopenia: an undiagnosed condition in older adults. current consensus definition: prevalence, etiology, and consequences. International Working Group on Sarcopenia. J Am Med Dir Assoc 12:249–256. https://doi.org/10.1016/j.jamda.2011.01.003

    Article  PubMed  Google Scholar 

  46. Otsuka R, Tange C, Tomida M, Nishita Y, Kato Y, Yuki A, Ando F, Shimokata H, Arai H (2019) Dietary factors associated with the development of physical frailty in community-dwelling older adults. J Nutr Health Aging 23:89–95. https://doi.org/10.1007/s12603-018-1124-3

    Article  CAS  PubMed  Google Scholar 

  47. Sandoval-Insausti H, Pérez-Tasigchana RF, López-García E, García-Esquinas E, Rodríguez-Artalejo F, Guallar-Castillón P (2016) Macronutrients intake and incident frailty in older adults: a prospective cohort study. J Gerontol A Biol Sci Med Sci 71:1329–1334. https://doi.org/10.1093/gerona/glw033

    Article  CAS  PubMed  Google Scholar 

  48. Hruby A, Sahni S, Bolster D, Jacques PF (2018) Protein intake and functional integrity in aging: the Framingham heart study offspring. J Gerontol A Biol Sci Med Sci. https://doi.org/10.1093/gerona/gly201

    Article  PubMed Central  Google Scholar 

  49. Houston DK, Tooze JA, Garcia K, Visser M, Rubin S, Harris TB, Newman AB, Kritchevsky SB (2017) Protein intake and mobility limitation in community-dwelling older adults: the health ABC study. J Am Geriatr Soc 65:1705–1711. https://doi.org/10.1111/jgs.14856

    Article  PubMed  PubMed Central  Google Scholar 

  50. Paddon-Jones D, van Loon L (2012) Nutritional approaches to treating sarcopenia. In: Cruz‐Jentoft AJ, Morley JE (ed) Sarcopenia. Chichester, UK, pp 275–295

  51. Paddon-Jones D, Rasmussen BB (2009) Dietary protein recommendations and the prevention of sarcopenia. Curr Opin Clin Nutr Metab Care 12:86–90. https://doi.org/10.1097/MCO.0b013e32831cef8b

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  52. Lonnie M, Hooker E, Brunstrom JM, Corfe BM, Green MA, Watson AW, Williams EA, Stevenson EJ, Penson S, Johnstone AM (2018) Protein for life: review of optimal protein intake, sustainable dietary sources and the effect on appetite in ageing adults. Nutrients 10:360. https://doi.org/10.3390/nu10030360

    Article  CAS  PubMed Central  Google Scholar 

  53. Kim IY, Schutzler S, Schrader AM, Spencer HJ, Azhar G, Wolfe RR, Ferrando AA (2018) Protein intake distribution pattern does not affect anabolic response, lean body mass, muscle strength or function over 8 weeks in older adults: a randomized-controlled trial. Clin Nutr 37:488–493. https://doi.org/10.1016/j.clnu.2017.02.020

    Article  CAS  PubMed  Google Scholar 

  54. Kim IY, Schutzler S, Schrader A, Spencer H, Kortebein P, Deutz NEP, Wolfe RR, Ferrando AA (2015) Quantity of dietary protein intake, but not pattern of intake, affects net protein balance primarily through differences in protein synthesis in older adults. Am J Physiol Endocrinol Metab 308:E21–E28. https://doi.org/10.1152/ajpendo.00382.2014

    Article  CAS  PubMed  Google Scholar 

  55. Cardon-Thomas DK, Riviere T, Tieges Z, Greig CA (2017) Dietary protein in older adults: adequate daily intake but potential for improved distribution. Nutrients 9:184. https://doi.org/10.3390/nu9030184

    Article  CAS  PubMed Central  Google Scholar 

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Acknowledgements

This work was supported by Consejo Nacional de Ciencia y Tecnología de México (CONACyT 493867), FIS Grants 16/609 and 16/1512 (Instituto de Salud Carlos III, State Secretary of R+D+I, and FEDER/FSE), the ATHLOS project (EU H2020- Project ID: 635316) and the JPI HDHL (SALAMANDER project). The funding agencies had no role in the study design, data analysis, interpretation of results, writing of the report, and in the decision to submit the article for publication.

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The authors’ responsibilities were as follows: DBE-D, EAS, and EL-G created the study concept and design; DBE-D and FC analyzed data; DBE-D and EL-G drafted the manuscript; FR-A and EL-G obtained funding; EL-G supervised the manuscript. All authors have read and approved the manuscript as submitted and are prepared to take public responsibility for the work.

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Correspondence to Ellen A. Struijk or Esther Lopez-Garcia.

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Study participants gave their informed written consent. The Clinical Research Ethics Committee of ‘La Paz’ University Hospital in Madrid approved the study protocol.

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Estrada-DeLeón, D.B., Struijk, E.A., Caballero, F. et al. Distribution of daily protein intake across meals and lower extremity functioning in community-dwelling Spanish older adults: a prospective cohort study. Eur J Nutr 60, 665–675 (2021). https://doi.org/10.1007/s00394-020-02273-6

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