Skip to main content
Log in

Evenness of dietary protein distribution is associated with higher muscle mass but not muscle strength or protein turnover in healthy adults: a systematic review

  • Original Contribution
  • Published:
European Journal of Nutrition Aims and scope Submit manuscript

Abstract

Purpose

Age-related decrease in muscle mass is, among several other factors, caused by suboptimal dietary protein intake. The protein intake of the general population has a skewed distribution towards the evening meal. However, it is hypothesised that an intake of protein with an even meal distribution leads to a more frequently maximised protein synthesis. This review investigates whether an even protein distribution is associated with preservation or gain in muscle mass, muscle strength, and protein turnover.

Methods

Seven databases: PubMed, Web of Science, Google Scholar, CINAHL, Cochrane Database of Systematic Reviews, Cochrane Central Register of Controlled Trials, and Embase were searched. Studies included had a healthy population between 20 and 85 years of age, with a BMI between 18.5 and 30.0, investigated even vs. skewed protein distribution, and measured skeletal muscle relevant outcomes. Case studies and systematic reviews were excluded. Studies were appraised using the AXIS scale for observational studies and the PEDro scale for the remaining studies.

Results

Fifteen studies met the eligibility criteria and were included. Three out of seven studies showed an association between even protein distribution and higher muscle mass. Two out of seven studies showed an association between greater muscle strength and an even protein distribution. Only one out of six studies found a positive association between protein synthesis and an even protein distribution.

Conclusion

Evidence indicated an association between muscle mass and an even protein intake. However, the evidence is currently insufficient to conclude whether an even protein intake is positively associated with muscle strength or protein turnover.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1

From: Moher D, Liberati A, Tetzlaff J, Altman DG, The PRISMA Group (2009). Preferred Reporting Items for Systematic Reviews and Meta-Analyses: The PRISMA Statement. PLoS Med 6(7): e1000097. doi: 10.1371/journal.pmed1000097. For more information, visit https://www.prisma-statement.org

Similar content being viewed by others

Availability of data and materials

Not applicable.

Code availability

Not applicable.

Abbreviations

AA:

Amino acids

AXIS:

Appraisal of cross-sectional studies

BW:

Body weight

CA:

Comparative study

CD:

Cohort study design

CI:

Confidence interval

CS:

Cross-sectional study

CT:

Clinical trial

CV:

Coefficient of variance

DXA:

Dual-energy X-ray absorptiometry

EAA:

Essential amino acids

FFM:

Fat free mass

FSR:

Fractional synthesis rate

IQR:

Interquartile range

MPB:

Muscle protein breakdown

MPS:

Muscle protein synthesis

PEDro:

Physiotherapy evidence database

RCT:

Randomised-controlled trial

RDA:

Recommended daily allowance

RM:

Repetition maximum

SEM:

Standard error of the mean

References

  1. Janssen I, Heymsfield SB, Wang ZM, Ross R (2000) Skeletal muscle mass and distribution in 468 men and women aged 18–88 yr. J Appl Physiol 89:81–88. https://doi.org/10.1152/jappl.2000.89.1.81

    Article  CAS  PubMed  Google Scholar 

  2. Cruz-Jentoft AJ, Baeyens JP, Bauer JM 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 

  3. Metter EJ, Talbot LA, Schrager M, Conwit R (2002) Skeletal muscle strength as a predictor of all-cause mortality in healthy men. J Gerontol A Biol Sci Med Sci 57:B359–B365. https://doi.org/10.1093/gerona/57.10.b359

    Article  PubMed  Google Scholar 

  4. Janssen I, Heymsfield SB, Ross R (2002) Low relative skeletal muscle mass (sarcopenia) in older persons is associated with functional impairment and physical disability. J Am Geriatr Soc 50:889–896. https://doi.org/10.1046/j.1532-5415.2002.50216.x

    Article  PubMed  Google Scholar 

  5. Christensen K, Doblhammer G, Rau R, Vaupel JW (2009) Ageing populations: the challenges ahead. Lancet (London, England) 374:1196–1208. https://doi.org/10.1016/S0140-6736(09)61460-4

    Article  Google Scholar 

  6. Klintefelt A (2018) Befolkningsfremskrivninger 2018–2060, Statistics Denmark

  7. Janssen I, Shepard DS, Katzmarzyk PT, Roubenoff R (2004) The healthcare costs of sarcopenia in the United States. J Am Geriatr Soc 52:80–85. https://doi.org/10.1111/j.1532-5415.2004.52014.x

    Article  PubMed  Google Scholar 

  8. Houston DK, Nicklas BJ, Ding J et al (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 

  9. FAO expert Consultation (2013) Dietary protein quality evaluation in human nutrition. Food and Agriculrure Organization of the United Nations, Rome

    Google Scholar 

  10. Campbell WW, Trappe TA, Wolfe RR, Evans WJ (2001) The recommended dietary allowance for protein may not be adequate for older people to maintain skeletal muscle. J Gerontol A Biol Sci Med Sci 56:M373–M380. https://doi.org/10.1093/gerona/56.6.m373

    Article  CAS  PubMed  Google Scholar 

  11. Bauer J, Biolo G, Cederholm T 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 

  12. Rand WM, Pellett PL, Young VR (2003) Meta-analysis of nitrogen balance studies for estimating protein requirements in healthy adults. Am J Clin Nutr 77:109–127. https://doi.org/10.1093/ajcn/77.1.109

    Article  CAS  PubMed  Google Scholar 

  13. Trumbo P, Schlicker S, Yates AA et al (2002) Dietary reference intakes for energy, carbohydrate, fiber, fat, fatty acids, cholesterol, protein and amino acids. J Am Diet Assoc 102:1621–1630. https://doi.org/10.1016/S0002-8223(02)90346-9

    Article  PubMed  Google Scholar 

  14. Wall BT, Gorissen SH, Pennings B et al (2015) Aging is accompanied by a blunted muscle protein synthetic response to protein ingestion. PLoS ONE 10:e0140903. https://doi.org/10.1371/journal.pone.0140903

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  15. Katsanos CS, Kobayashi H, Sheffield-Moore M et al (2005) Aging is associated with diminished accretion of muscle proteins after the ingestion of a small bolus of essential amino acids. Am J Clin Nutr 82:1065–1073. https://doi.org/10.1093/ajcn/82.5.1065

    Article  CAS  PubMed  Google Scholar 

  16. Moore DR, Churchward-Venne TA, Witard O et al (2015) Protein ingestion to stimulate myofibrillar protein synthesis requires greater relative protein intakes in healthy older versus younger men. J Gerontol A Biol Sci Med Sci 70:57–62. https://doi.org/10.1093/gerona/glu103

    Article  CAS  PubMed  Google Scholar 

  17. Wolfe RR (2012) The role of dietary protein in optimizing muscle mass, function and health outcomes in older individuals. Br J Nutr 108(Suppl):S88-93. https://doi.org/10.1017/S0007114512002590

    Article  CAS  PubMed  Google Scholar 

  18. Wolfe RR, Miller SL, Miller KB (2008) Optimal protein intake in the elderly. Clin Nutr 27:675–684. https://doi.org/10.1016/j.clnu.2008.06.008

    Article  CAS  PubMed  Google Scholar 

  19. Katsanos CS, Kobayashi H, Sheffield-Moore M et al (2006) A high proportion of leucine is required for optimal stimulation of the rate of muscle protein synthesis by essential amino acids in the elderly. Am J Physiol Endocrinol Metab 291:E381–E387. https://doi.org/10.1152/ajpendo.00488.2005

    Article  CAS  PubMed  Google Scholar 

  20. Nordic Council of Ministers NC of M (2008) Nordic nutrition recommendations 2012. Nord Nutr Recomm 2012(5):1–3. https://doi.org/10.6027/Nord2014-002

    Article  Google Scholar 

  21. Rousset S, Patureau Mirand P, Brandolini M et al (2003) Daily protein intakes and eating patterns in young and elderly French. Br J Nutr 90:1107–1115. https://doi.org/10.1079/bjn20031004

    Article  CAS  PubMed  Google Scholar 

  22. Fulgoni VL (2008) Current protein intake in America: analysis of the National Health and Nutrition Examination Survey, 2003–2004. Am J Clin Nutr 87:1554S-1557S. https://doi.org/10.1093/ajcn/87.5.1554S

    Article  CAS  PubMed  Google Scholar 

  23. 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 

  24. U.S. Department of Agriculture ARS (2018) Energy intakes: percentages of energy from protein, carbohydrate, fat, and alcohol, by gender and age, what we eat in America. NHANES 2015–2016

  25. Tieland M, Borgonjen-Van den Berg KJ, Van Loon LJC, de Groot LCPGM (2015) Dietary protein intake in dutch elderly people: a focus on protein sources. Nutrients 7:9697–9706. https://doi.org/10.3390/nu7125496

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  26. Norton LE, Wilson GJ, Moulton CJ, Layman DK (2017) Meal distribution of dietary protein and leucine influences long-term muscle mass and body composition in adult rats. J Nutr 147:195–201. https://doi.org/10.3945/jn.116.231779

    Article  CAS  PubMed  Google Scholar 

  27. Hudson JL, Iii REB, Campbell WW (2020) Protein distribution and muscle-related outcomes: does the evidence support the concept? Nutrients 12:1–22. https://doi.org/10.3390/nu12051441

    Article  CAS  Google Scholar 

  28. Liberati A, Altman DG, Tetzlaff J et al (2009) The PRISMA statement for reporting systematic reviews and meta-analyses of studies that evaluate healthcare interventions: explanation and elaboration. BMJ 339:b2700. https://doi.org/10.1136/bmj.b2700

    Article  PubMed  PubMed Central  Google Scholar 

  29. Guillet C, Delcourt I, Rance M et al (2009) Changes in basal and insulin and amino acid response of whole body and skeletal muscle proteins in obese men. J Clin Endocrinol Metab 94:3044–3050. https://doi.org/10.1210/jc.2008-2216

    Article  CAS  PubMed  Google Scholar 

  30. Soares MJ, Piers LS, Shetty PS et al (1994) Whole body protein turnover in chronically undernourished individuals. Clin Sci (Lond) 86:441–446. https://doi.org/10.1042/cs0860441

    Article  CAS  Google Scholar 

  31. Furber M, Anton-Solanas A, Koppe E et al (2017) A 7-day high protein hypocaloric diet promotes cellular metabolic adaptations and attenuates lean mass loss in healthy males. Clin Nutr Exp 14:13–25. https://doi.org/10.1016/j.yclnex.2017.05.002

    Article  Google Scholar 

  32. Agergaard J, Trøstrup J, Uth J et al (2015) Does vitamin-D intake during resistance training improve the skeletal muscle hypertrophic and strength response in young and elderly men?—a randomized controlled trial. Nutr Metab (Lond) 12:32. https://doi.org/10.1186/s12986-015-0029-y

    Article  CAS  Google Scholar 

  33. Weinheimer EM, Sands LP, Campbell WW (2010) A systematic review of the separate and combined effects of energy restriction and exercise on fat-free mass in middle-aged and older adults: implications for sarcopenic obesity. Nutr Rev 68:375–388. https://doi.org/10.1111/j.1753-4887.2010.00298.x

    Article  PubMed  Google Scholar 

  34. Hector AJ, McGlory C, Damas F et al (2018) Pronounced energy restriction with elevated protein intake results in no change in proteolysis and reductions in skeletal muscle protein synthesis that are mitigated by resistance exercise. FASEB J 32:265–275. https://doi.org/10.1096/fj.201700158RR

    Article  CAS  PubMed  Google Scholar 

  35. (1999) PEDro scale (English). In: Physiother. Evid. Database. https://www.pedro.org.au/english/downloads/pedro-scale/. Accessed 28 Aug 2019

  36. Downes MJ, Brennan ML, Williams HC, Dean RS (2016) Development of a critical appraisal tool to assess the quality of cross-sectional studies (AXIS). BMJ Open 6:e011458. https://doi.org/10.1136/bmjopen-2016-011458

    Article  PubMed  PubMed Central  Google Scholar 

  37. Mamerow MM, Mettler JA, English KL et al (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 

  38. Yasuda J, Asako M, Arimitsu T, Fujita S (2019) Association of protein intake in three meals with muscle mass in healthy young subjects: a cross-sectional study. Nutrients 11:612. https://doi.org/10.3390/nu11030612

    Article  CAS  PubMed Central  Google Scholar 

  39. Arnal MA, Mosoni L, Boirie Y et al (2000) Protein feeding pattern does not affect protein retention in young women. J Nutr 130:1700–1704. https://doi.org/10.1093/jn/130.7.1700

    Article  CAS  PubMed  Google Scholar 

  40. Gingrich A, Spiegel A, Kob R et al (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. https://doi.org/10.3390/nu9121358

    Article  PubMed  PubMed Central  Google Scholar 

  41. Loenneke JP, Loprinzi PD, Murphy CH, Phillips SM (2016) Per meal dose and frequency of protein consumption is associated with lean mass and muscle performance. Clin Nutr 35:1506–1511. https://doi.org/10.1016/j.clnu.2016.04.002

    Article  PubMed  Google Scholar 

  42. Kim I-Y, Schutzler S, Schrader AM et al (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 

  43. Farsijani S, Morais JA, Payette H et al (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 

  44. Valenzuela RER, Ponce JA, Morales-Figueroa GG et al (2013) Insufficient amounts and inadequate distribution of dietary protein intake in apparently healthy older adults in a developing country: implications for dietary strategies to prevent sarcopenia. Clin Interv Aging 8:1143–1148. https://doi.org/10.2147/CIA.S49810

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  45. Arnal MA, Mosoni L, Boirie Y et al (1999) Protein pulse feeding improves protein retention in elderly women. Am J Clin Nutr 69:1202–1208. https://doi.org/10.1093/ajcn/69.6.1202

    Article  CAS  PubMed  Google Scholar 

  46. Farsijani S, Payette H, Morais JA et al (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 

  47. Mishra S, Goldman JD, Sahyoun NR, Moshfegh AJ (2018) Association between dietary protein intake and grip strength among adults aged 51 years and over: what we eat in America, National Health and Nutrition Examination Survey 2011–2014. PLoS ONE 13:e0191368. https://doi.org/10.1371/journal.pone.0191368

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  48. Bollwein J, Diekmann R, Kaiser MJ et al (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 

  49. Ten Haaf DSM, van Dongen EJI, Nuijten MAH et al (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 10:1–13. https://doi.org/10.3390/nu10040506

    Article  CAS  Google Scholar 

  50. Kim I-Y, Schutzler S, Schrader A et al (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 

  51. Arnal MA, Mosoni L, Boirie Y et al (2000) Protein turnover modifications induced by the protein feeding pattern still persist after the end of the diets. Am J Physiol Endocrinol Metab 278:E902–E909. https://doi.org/10.1152/ajpendo.2000.278.5.E902

    Article  CAS  PubMed  Google Scholar 

  52. Narici MV, Roi GS, Landoni L et al (1989) Changes in force, cross-sectional area and neural activation during strength training and detraining of the human quadriceps. Eur J Appl Physiol Occup Physiol 59:310–319. https://doi.org/10.1007/BF02388334

    Article  CAS  PubMed  Google Scholar 

  53. İlhan B, Bahat G, Erdoğan T et al (2019) Anorexia is independently associated with decreased muscle mass and strength in community dwelling older adults. J Nutr Health Aging 23:202–206. https://doi.org/10.1007/s12603-018-1119-0

    Article  PubMed  Google Scholar 

  54. Devries MC, Sithamparapillai A, Brimble KS et al (2018) Changes in kidney function do not differ between healthy adults consuming higher- compared with lower- or normal-protein diets: a systematic review and meta-analysis. J Nutr 148:1760–1775. https://doi.org/10.1093/jn/nxy197

    Article  PubMed  PubMed Central  Google Scholar 

  55. Boirie Y, Gachon P, Beaufrère B (1997) Splanchnic and whole-body leucine kinetics in young and elderly men. Am J Clin Nutr 65:489–495. https://doi.org/10.1093/ajcn/65.2.489

    Article  CAS  PubMed  Google Scholar 

  56. Bouillanne O, Curis E, Hamon-Vilcot B et al (2013) Impact of protein pulse feeding on lean mass in malnourished and at-risk hospitalized elderly patients: a randomized controlled trial. Clin Nutr 32:186–192. https://doi.org/10.1016/j.clnu.2012.08.015

    Article  CAS  PubMed  Google Scholar 

  57. Gasier HG, Fluckey JD, Previs SF (2010) The application of 2H2O to measure skeletal muscle protein synthesis. Nutr Metab (Lond) 7:31. https://doi.org/10.1186/1743-7075-7-31

    Article  CAS  Google Scholar 

Download references

Funding

The research is funded by Innovation Fund Denmark.

Author information

Authors and Affiliations

Authors

Contributions

The author contributions were as follows: SEJ and JA designed research; SEJ conducted research; SEJ and JA analysed data; SEJ wrote the paper. JA had primary responsibility for the final content. Both authors read and approved the final manuscript.

Corresponding author

Correspondence to Jakob Agergaard.

Ethics declarations

Conflict of interest

JA is funded by Danish Crown Ingredients A/S. Other than this, the authors declare no conflicts of interest.

Ethics approval

Not applicable, but the review is registered at PROSPERO International Prospective Register of Systematic Reviews with the ID NR: CRD42019127793.

Consent to participate

Not applicable.

Consent for publication

The authors give their consent for publication.

Supplementary Information

Below is the link to the electronic supplementary material.

Supplementary file1 (DOCX 245 KB)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Jespersen, S.E., Agergaard, J. Evenness of dietary protein distribution is associated with higher muscle mass but not muscle strength or protein turnover in healthy adults: a systematic review. Eur J Nutr 60, 3185–3202 (2021). https://doi.org/10.1007/s00394-021-02487-2

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00394-021-02487-2

Keywords

Navigation