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Daily and per-meal animal and plant protein intake in relation to muscle mass in healthy older adults without functional limitations: an enable study

  • Anne Gingrich
  • Alexandra Spiegel
  • Julia E. Gradl
  • Thomas Skurk
  • Hans Hauner
  • Cornel C. Sieber
  • Dorothee Volkert
  • Eva Kiesswetter
Original Article
  • 16 Downloads

Abstract

Objective

Animal protein sources are considered to be of higher quality than plant protein sources in terms of stimulating muscle metabolism. Our objective was to investigate whether protein intake from animal and plant sources on a daily and per-meal basis differs between healthy older adults with normal and with low muscle mass.

Methods

In this cross-sectional study including 100 healthy, community-dwelling adults (51 women) aged 75–85 years without functional limitations dietary intake was assessed using 7-day food records. Protein intake was classified by six animal and six plant protein sources. Skeletal muscle index (SMI) was determined based on bioelectrical impedance analysis and categorized into ‘normal’ or ‘low’ (men ≤ 8.50, women ≤ 5.75 kg/m2). The absolute animal and plant protein intake and their proportion of total protein intake were compared between these groups using Mann–Whitney U test.

Results

Daily protein intake was 0.96 ± 0.27 g/kg body weight (BW), 61 ± 10% hereof were from animal origin with no difference between men and women. SMI was low in 39% of men and 35% of women. No differences in absolute daily animal and plant protein intake between participants with normal vs. low SMI were observed. The proportion of animal protein was not different on neither a daily nor a per-meal basis between those with normal and those with low SMI. Women with low SMI consumed less animal protein (in g) for breakfast (4.8 ± 4.1 g vs. 8.5 ± 6.9 g, p = 0.031) and fewer meals per day with at least 50% animal protein (2.2 ± 0.9 vs. 2.7 ± 1.0, p = 0.046) compared to those with normal SMI.

Conclusion

On a daily basis, the absolute and relative animal protein intake does not differ between healthy older adults without functional limitations with normal vs. low SMI. However, our results indicate that in women animal protein intake on a per-meal basis might be of relevance for the maintenance of muscle mass.

Keywords

Protein intake Food source Protein distribution Muscle mass Aging 

Notes

Acknowledgements

We thank Dr. Lynne Stecher for her statistical advice and Julius Hannink for his technical support in data preparation.

Author contributions

DV, HH, TS, CCS, EK and AG conceived and designed the experiments. AG and AT performed the experiments. AG analyzed the data. JEG analyzed the 7-day food records and supported the data analysis. AG, EK and DV interpreted the data. AG wrote the paper and EK and DV revised it critically. All authors have read and approved the final version of the article. The present work was performed in fulfillment of the requirements for obtaining the degree Dr. rer. biol. hum (Doctoral Degree in Human Biology).

Funding

This work was funded by a grant of the German Ministry for Education and Research (BMBF) 01EA1409C. The German Ministry for Education and Research (BMBF) had no role in design, methods, subject recruitment, data collections, analysis and preparation of paper. The preparation of this paper was supported by the enable Cluster and is catalogued by the enable Steering Committee as enable 012 (http://enable-cluster.de). We acknowledge support by Deutsche Forschungsgemeinschaft and Friedrich-Alexander-Universität Erlangen-Nürnberg (FAU) within the funding programme Open Access Publishing.

Compliance with ethical standards

Conflict of interest

All authors declare that they have no conflicts of interest.

Ethics approval

All procedures were approved by the ethics committee of the Friedrich-Alexander-Universitat Erlangen-Nurnberg (number: 291_15 B).

Statement of human and animal rights

All procedures performed in studies involving human participants were in accordance with the ethical standards of the institutional and/or national research committee and with the 1964 Helsinki declaration and its later amendments or comparable ethical standards.

Informed consent

Written informed consent was obtained from all participants prior to the assessments.

Supplementary material

40520_2018_1081_MOESM1_ESM.pdf (457 kb)
Supplementary material 1 (PDF 457 KB)

References

  1. 1.
    Marzetti E, Calvani R, Tosato M et al (2017) Sarcopenia: an overview. Aging Clin Exp Res 29:11–17.  https://doi.org/10.1007/s40520-016-0704-5 CrossRefPubMedGoogle Scholar
  2. 2.
    Janssen I, Baumgartner RN, Ross R et al (2004) Skeletal muscle cutpoints associated with elevated physical disability risk in older men and women. Am J Epidemiol 159:413–421CrossRefPubMedGoogle Scholar
  3. 3.
    Paddon-Jones D, Short KR, Campbell WW et al (2008) Role of dietary protein in the sarcopenia of aging. Am J Clin Nutr 87:1562s–1566sCrossRefPubMedGoogle Scholar
  4. 4.
    Cruz-Jentoft AJ, Kiesswetter E, Drey M et al (2017) Nutrition, frailty, and sarcopenia. Aging Clin Exp Res 29:43–48.  https://doi.org/10.1007/s40520-016-0709-0 CrossRefPubMedGoogle Scholar
  5. 5.
    Breen L, Phillips SM (2011) Skeletal muscle protein metabolism in the elderly: interventions to counteract the ‘anabolic resistance’ of ageing. Nutr Metab (Lond) 8:68.  https://doi.org/10.1186/1743-7075-8-68 CrossRefGoogle Scholar
  6. 6.
    Murphy CH, Oikawa SY, Phillips SM (2016) Dietary protein to maintain muscle mass in aging: a case for per-meal protein recommendations. J Frailty Aging 5:49–58.  https://doi.org/10.14283/jfa.2016.80 CrossRefPubMedGoogle Scholar
  7. 7.
    Gorissen SHM, Witard OC (2017) Characterising the muscle anabolic potential of dairy, meat and plant-based protein sources in older adults. Proc Nutr Soc.  https://doi.org/10.1017/s002966511700194x CrossRefPubMedGoogle Scholar
  8. 8.
    Wilkinson SB, Tarnopolsky MA, Macdonald MJ et al (2007) Consumption of fluid skim milk promotes greater muscle protein accretion after resistance exercise than does consumption of an isonitrogenous and isoenergetic soy-protein beverage. Am J Clin Nutr 85:1031–1040CrossRefPubMedGoogle Scholar
  9. 9.
    Tang JE, Moore DR, Kujbida GW et al (2009) Ingestion of whey hydrolysate, casein, or soy protein isolate: effects on mixed muscle protein synthesis at rest and following resistance exercise in young men. J Appl Physiol (1985) 107:987–992.  https://doi.org/10.1152/japplphysiol.00076.2009 CrossRefGoogle Scholar
  10. 10.
    Yang Y, Churchward-Venne TA, Burd NA et al (2012) Myofibrillar protein synthesis following ingestion of soy protein isolate at rest and after resistance exercise in elderly men. Nutr Metab (Lond) 9:57.  https://doi.org/10.1186/1743-7075-9-57 CrossRefPubMedCentralGoogle Scholar
  11. 11.
    Phillips SM (2012) Nutrient-rich meat proteins in offsetting age-related muscle loss. Meat Sci 92:174–178.  https://doi.org/10.1016/j.meatsci.2012.04.027 CrossRefPubMedGoogle Scholar
  12. 12.
    Aubertin-Leheudre M, Adlercreutz H (2009) Relationship between animal protein intake and muscle mass index in healthy women. Br J Nutr 102:1803–1810.  https://doi.org/10.1017/s0007114509991310 CrossRefPubMedGoogle Scholar
  13. 13.
    Lord C, Chaput JP, Aubertin-Leheudre M et al (2007) Dietary animal protein intake: association with muscle mass index in older women. J Nutr Health Aging 11:383–387PubMedGoogle Scholar
  14. 14.
    Sahni S, Mangano KM, Hannan MT et al (2015) Higher protein intake is associated with higher lean mass and quadriceps muscle strength in adult men and women. J Nutr 145:1569–1575.  https://doi.org/10.3945/jn.114.204925 CrossRefPubMedPubMedCentralGoogle Scholar
  15. 15.
    Folstein MF, Robins LN, Helzer JE (1983) The mini-mental state examination. Arch Gen Psychiatry 40:812CrossRefPubMedGoogle Scholar
  16. 16.
    Freiberger E, de Vreede P, Schoene D et al (2012) Performance-based physical function in older community-dwelling persons: a systematic review of instruments. Age Ageing 41:712–721.  https://doi.org/10.1093/ageing/afs099 CrossRefPubMedGoogle Scholar
  17. 17.
    Guralnik JM, Simonsick EM, Ferrucci L et al (1994) A short physical performance battery assessing lower extremity function: association with self-reported disability and prediction of mortality and nursing home admission. J Gerontol 49:M85–M94CrossRefPubMedPubMedCentralGoogle Scholar
  18. 18.
    Guralnik JM, Ferrucci L, Pieper CF et al (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–M231CrossRefPubMedPubMedCentralGoogle Scholar
  19. 19.
    D’Ath P, Katona P, Mullan E et al (1994) Screening, detection and management of depression in elderly primary care attenders. I: the acceptability and performance of the 15 item Geriatric Depression Scale (GDS15) and the development of short versions. Fam Pract 11:260–266CrossRefPubMedGoogle Scholar
  20. 20.
    Cwikel J, Ritchie K (1989) Screening for depression among the elderly in Israel: an assessment of the Short Geriatric Depression Scale (S-GDS). Isr J Med Sci 25:131–137PubMedGoogle Scholar
  21. 21.
    Guigoz Y, Vellas B, Garry PJ (1996) Assessing the nutritional status of the elderly: The Mini Nutritional Assessment as part of the geriatric evaluation. Nutr Rev 54:S59–S65CrossRefPubMedGoogle Scholar
  22. 22.
    Roberts HC, Denison HJ, Martin HJ et al (2011) A review of the measurement of grip strength in clinical and epidemiological studies: towards a standardised approach. Age Ageing 40:423–429.  https://doi.org/10.1093/ageing/afr051 CrossRefPubMedGoogle Scholar
  23. 23.
    Alley DE, Shardell MD, Peters KW et al (2014) Grip strength cutpoints for the identification of clinically relevant weakness. J Gerontol A Biol Sci Med Sci 69:559–566.  https://doi.org/10.1093/gerona/glu011 CrossRefPubMedPubMedCentralGoogle Scholar
  24. 24.
    Branson RD, Johannigman JA (2004) The measurement of energy expenditure. Nutr Clin Pract 19:622–636.  https://doi.org/10.1177/0115426504019006622 CrossRefPubMedGoogle Scholar
  25. 25.
    Masse LC, Fuemmeler BF, Anderson CB, Matthews CE, Trost SG, Catellier DJ, Treuth M (2005) Accelerometer data reduction: a comparison of four reduction algorithms on select outcome variables. Med Sci Sports Exerc 37:S544–S554CrossRefPubMedGoogle Scholar
  26. 26.
    Janssen I, Heymsfield SB, Baumgartner RN et al (2000) Estimation of skeletal muscle mass by bioelectrical impedance analysis. J Appl Physiol (1985) 89:465–471CrossRefGoogle Scholar
  27. 27.
    Kyle UG, Genton L, Karsegard L et al (2001) Single prediction equation for bioelectrical impedance analysis in adults aged 20–94 years. Nutrition 17:248–253CrossRefPubMedGoogle Scholar
  28. 28.
    Dehne LI, Klemm C, Henseler G et al (1999) The German food code and nutrient data base (BLS II.2). Eur J Epidemiol 15:355–359CrossRefPubMedGoogle Scholar
  29. 29.
    Cardon-Thomas DK, Riviere T, Tieges Z et al (2017) Dietary protein in older adults: adequate daily intake but potential for improved distribution. Nutrients.  https://doi.org/10.3390/nu9030184 CrossRefPubMedPubMedCentralGoogle Scholar
  30. 30.
    Deutsche Gesellschaft für Ernährung (2017) Wie viel Protein brauchen wir? https://www.dge.de/wissenschaft/referenzwerte/protein/. Accessed 26 Jul 2018
  31. 31.
    Tieland M, Borgonjen-Van den Berg KJ, Van Loon LJ et al (2015) Dietary protein intake in Dutch elderly people: a focus on protein sources. Nutrients 7:9697–9706.  https://doi.org/10.3390/nu7125496 CrossRefPubMedPubMedCentralGoogle Scholar
  32. 32.
    Rousset S, Patureau Mirand P, Brandolini M et al (2003) Daily protein intakes and eating patterns in young and elderly French. Br J Nutr 90:1107–1115CrossRefPubMedGoogle Scholar
  33. 33.
    Pasiakos SM, Agarwal S, Lieberman HR et al (2015) Sources and amounts of animal, dairy, and plant protein intake of US Adults in 2007–2010. Nutrients 7:7058–7069.  https://doi.org/10.3390/nu7085322 CrossRefPubMedPubMedCentralGoogle Scholar
  34. 34.
    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 CrossRefPubMedGoogle Scholar
  35. 35.
    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 CrossRefPubMedPubMedCentralGoogle Scholar
  36. 36.
    Schaafsma G (2000) The protein digestibility-corrected amino acid score. J Nutr 130:1865s–1867sCrossRefPubMedGoogle Scholar
  37. 37.
    Song M, Fung TT, Hu FB, Willett WC, Longo VD, Chan AT, Giovannucci EL (2016) Association of animal and plant protein intake with all-cause and cause-specific mortality. JAMA Intern Med 176:1453–1463.  https://doi.org/10.1001/jamainternmed.2016.4182 CrossRefPubMedPubMedCentralGoogle Scholar

Copyright information

© Springer Nature Switzerland AG 2018

Authors and Affiliations

  • Anne Gingrich
    • 1
  • Alexandra Spiegel
    • 1
  • Julia E. Gradl
    • 1
  • Thomas Skurk
    • 2
  • Hans Hauner
    • 2
    • 3
  • Cornel C. Sieber
    • 1
    • 4
  • Dorothee Volkert
    • 1
  • Eva Kiesswetter
    • 1
  1. 1.Institute for Biomedicine of AgingFriedrich-Alexander-Universität Erlangen-NürnbergNurembergGermany
  2. 2.Chair of Nutritional MedicineTechnische Universität MünchenFreising, WeihenstephanGermany
  3. 3.Institute of Nutritional Medicine, Klinikum rechts der IsarTechnical University of MunichMunichGermany
  4. 4.Krankenhaus Barmherzige Brüder RegensburgRegensburgGermany

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