Older adults have delayed amino acid absorption after a high protein mixed breakfast meal

Abstract

Objectives

To measure the postprandial plasma amino acid appearance in younger and older adults following a high protein mixed meal.

Design

Cross-sectional study.

Setting

Clinical research setting.

Participants

Healthy men and women aged 60-75 (n=15) years, and young controls aged 20-25 years (n=15) matched for body mass index and insulin sensitivity based on the homeostatic model assessment of insulin resistance.

Intervention

High protein mixed meal of complete food products.

Measurements

Circulating amino acid concentrations were determined hourly before and for 5 hours after meal ingestion.

Results

There was no difference between cohorts in postprandial appearance of non-essential amino acids, or area under the curve of any individual amino acid or amino acid class. However, older adults had higher baseline concentrations of aspartic acid, glutamic acid, glycine, ornithine, threonine and tyrosine and lower baseline concentrations of hydroxyproline, isoleucine, leucine, methionine and valine compared to younger adults. Younger adults showed peak essential (EAA) and branched-chain amino acid (BCAA) concentrations at 1 hour post meal while older adults’ peak EAA and BCAA concentration was at 3 hours. Similarly, peak total amino acid concentrations were at 3 hours in older adults.

Conclusion

Older adults digested and absorbed the protein within a mixed meal more slowly than younger adults. Delayed absorption of AA following a mixed meal of complete food products may suppress or delay protein synthesis in senescent muscle.

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

References

  1. 1.

    Koopman R, van Loon LJC. Aging, exercise, and muscle protein metabolism, 2009.

    Google Scholar 

  2. 2.

    Paddon-Jones D, Rasmussen BB. Dietary protein recommendations and the prevention of sarcopenia. Curr Opin Clin Nutr Metab Care 2009;12(1):86–90.

    PubMed Central  CAS  Article  PubMed  Google Scholar 

  3. 3.

    Paddon-Jones D, Leidy H. Dietary protein and muscle in older persons. Curr Opin Clin Nutr Metab Care 2014;17(1):5–11.

    PubMed Central  CAS  Article  PubMed  Google Scholar 

  4. 4.

    Volpi E, Campbell WW, Dwyer JT, Johnson MA, Jensen GL, Morley JE, Wolfe RR. Is the optimal level of protein intake for older adults greater than the recommended dietary allowance? Journals of Gerontology — Series A Biological Sciences and Medical Sciences 2013;68(6):677–681.

    CAS  Article  Google Scholar 

  5. 5.

    Dangin M, Boirie Y, Garcia-Rodenas C, Gachon P, Fauquant J, Callier P, Ballèvre O, Beaufrère B. The digestion rate of protein is an independent regulating factor of postprandial protein retention. Am J Physiol Endocrinol Metab 2011;280(2):E340–E348.

    Google Scholar 

  6. 6.

    Bohé J, Low A, Wolfe RR, Rennie MJ. Human Muscle Protein Synthesis is Modulated by Extracellular, Not Intramuscular Amino Acid Availability: A Dose-Response Study. J Physiol 2003;552(1):315–324.

    PubMed Central  Article  PubMed  Google Scholar 

  7. 7.

    Cuthbertson D, Smith K, Babraj J, Leese G, Waddell T, Atherton P, Wackerhage H, Taylor PM, Rennie MJ. Anabolic signaling deficits underlie amino acid resistance of wasting, aging muscle. FASEB journal: official publication of the Federation of American Societies for Experimental Biology 2005;19(3):422–424.

    CAS  Google Scholar 

  8. 8.

    Rémond D, Machebeuf M, Yven C, Buffière C, Mioche L, Mosoni L, Mirand PP. Postprandial whole-body protein metabolism after a meat meal is influenced by chewing efficiency in elderly subjects. Am J Clin Nutr 2007;85(5):1286–1292.

    PubMed  Google Scholar 

  9. 9.

    Feldman M, Cryer B, McArthur KE, Huet BA, Lee E. Effects of aging and gastritis on gastric acid and pepsin secretion in humans: A prospective study. Gastroenterology 1996;110(4):1043–1052.

    CAS  Article  PubMed  Google Scholar 

  10. 10.

    Shimamoto C, Hirata I, Hiraike Y, Takeuchi N, Nomura T, Katsu Ki. Evaluation of Gastric Motor Activity in the Elderly by Electrogastrography and the C-Acetate Breath Test. Gerontology 2002;48(6):381–386.

    Article  PubMed  Google Scholar 

  11. 11.

    Brogna A, Ferrara R, Bucceri AM, Lanteri E, Catalano F. Influence of aging on gastrointestinal transit time. An ultrasonographic and radiologic study. Invest Radiol 1999;34(5):357–359.

    CAS  Article  PubMed  Google Scholar 

  12. 12.

    Grassi M, Petraccia L, Mennuni G, Fontana M, Scarno A, Sabetta S, Fraioli A. Changes, functional disorders, and diseases in the gastrointestinal tract of elderly. Nutr Hosp 2011;26(4):659–668.

    CAS  PubMed  Google Scholar 

  13. 13.

    Fereday A, Gibson NR, Cox M, Pacy PJ, Millward DJ. Protein requirements and ageing: Metabolic demand and efficiency of utilization. Br J Nutr 1997;77(5):685–702.

    CAS  Article  PubMed  Google Scholar 

  14. 14.

    Koopman R, Walrand S, Beelen M, Gijsen AP, Kies AK, Boirie Y, Saris WHM, Van Loon LJC. Dietary protein digestion and absorption rates and the subsequent postprandial muscle protein synthetic response do not differ between young and elderly men. J Nutr 2009;139(9):1707–1713.

    CAS  Article  PubMed  Google Scholar 

  15. 15.

    Boirie Y, Gachon P, Beaufrère B. Splanchnic and whole-body leucine kinetics in young and elderly men. Am J Clin Nutr 1997;65(2):489–495.

    CAS  PubMed  Google Scholar 

  16. 16.

    Jourdan M, Deutz N, Cynober L, Aussel C (2011) Features, causes and consequences of splanchnic sequestration of amino acid in old rats. PLoS One 2011;6(11):e27002.

    CAS  Article  Google Scholar 

  17. 17.

    Volpi E, Mittendorfer B, Wolf SE, Wolfe RR. Oral amino acids stimulate muscle protein anabolism in the elderly despite higher first-pass splanchnic extraction. Am J Phisiol Endocrinol Metab 1999;277(40):E513–E520.

    CAS  Google Scholar 

  18. 18.

    Rutten EPA, Engelen MPKJ, Castro CLN, Wouters EFM, Schols AMWJ, Deutz NEP. Decreased whole-body and splanchnic glutamate metabolism in healthy elderly men and patients with chronic obstructive pulmonary disease in the postabsorptive state and in response to feeding. J Nutr 2005;135(9):2166–2170.

    CAS  PubMed  Google Scholar 

  19. 19.

    Ten Have GA, Engelen MP, Luiking YC, Deutz NE. Absorption kinetics of amino acids, peptides, and intact proteins. Int J Sport Nutr Exerc Metab 2007;17(Suppl):S23–36.

    CAS  PubMed  Google Scholar 

  20. 20.

    Dangin M, Boirie Y, Guillet C, Beaufrere B. Influence of the protein digestion rate on protein turnover in young and elderly subjects. J Nutr 2002;132(Suppl):3228S–3233S.

    CAS  PubMed  Google Scholar 

  21. 21.

    Boirie Y, Dangin M, Gachon P, Vasson MP, Maubois JL, Beaufrère B. Slow and fast dietary proteins differently modulate postprandial protein accretion. Proc Natl Acad Sci U S A 1997;94(26):14930–14935.

    PubMed Central  CAS  Article  PubMed  Google Scholar 

  22. 22.

    Arnal M-A, Mosoni L, Boirie Y, Houlier M-L, Morin L, Verdier E, Ritz P, Antoine J-M, Prugnaud J, Beaufrère B, Mirand PP. Protein pulse feeding improves protein retention in elderly women. Am J Clin Nutr 1999;69(6):1202–1208.

    CAS  PubMed  Google Scholar 

  23. 23.

    Tang JE, Moore DR, Kujbida GW, Tarnopolsky MA, Phillips SM. 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 2009;107(3):987–992.

    CAS  Article  PubMed  Google Scholar 

  24. 24.

    Pennings B, Boirie Y, Senden JM, Gijsen AP, Kuipers H, van Loon LJ. Whey protein stimulates postprandial muscle protein accretion more effectively than do casein and casein hydrolysate in older men. The American journal of clinical nutrition 2011;93(5):997–1005.

    CAS  Article  PubMed  Google Scholar 

  25. 25.

    Areta JL, Burke LM, Ross ML, Camera DM, West DW, Broad EM, Jeacocke NA, Moore DR, Stellingwerff T, Phillips SM, Hawley JA, Coffey VG. Timing and distribution of protein ingestion during prolonged recovery from resistance exercise alters myofibrillar protein synthesis. The Journal of physiology 2013;591(Pt 9):2319–2331.

    PubMed Central  CAS  Article  PubMed  Google Scholar 

  26. 26.

    Mamerow MM, Mettler JA, English KL, Casperson SL, Arentson-Lantz E, Sheffield-Moore M, Layman DK, Paddon-Jones D. Dietary protein distribution positively influences 24-h muscle protein synthesis in healthy adults. The Journal of nutrition 2014;144(6):876–880.

    PubMed Central  CAS  Article  PubMed  Google Scholar 

  27. 27.

    Soop M, Nehra V, Henderson GC, Boirie Y, Ford GC, Nair KS. Coingestion of whey protein and casein in a mixed meal: demonstration of a more sustained anabolic effect of casein. Am J Physiol Endocrinol Metab 2012;303(1):E152–E162.

    PubMed Central  CAS  Article  PubMed  Google Scholar 

  28. 28.

    Pennings B, Groen BBL, Van Dijk JW, De Lange A, Kiskini A, Kuklinski M, Senden JMG, Van Loon LJC. Minced beef is more rapidly digested and absorbed than beef steak, resulting in greater postprandial protein retention in older men. Am J Clin Nutr 2013;98(1):121–128.

    CAS  Article  PubMed  Google Scholar 

  29. 29.

    Gorissen SHM, Burd NA, Hamer HM, Gijsen AP, Groen BB, van Loon LJC. Carbohydrate Coingestion Delays Dietary Protein Digestion and Absorption but Does Not Modulate Postprandial Muscle Protein Accretion. J Clin Endocrinol Metab 2014;99(6):2250–2258.

    CAS  Article  PubMed  Google Scholar 

  30. 30.

    Singh J, Dartois A, Kaur L. Starch digestibility in food matrix: a review. Trends Food Sci Technol 2010;21(4):168–180.

    CAS  Article  Google Scholar 

  31. 31.

    Gallier S, Singh H. The physical and chemical structure of lipids in relation to digestion and absorption. Lipid Technology 2012;24(12):271–273.

    CAS  Article  Google Scholar 

  32. 32.

    Matthews D, Hosker J, Rudenski A, Naylor B, Treacher D, Turner R. Homeostasis model assessment: insulin resistance and B-cell function from fasting plasma glucose and insulin concentrations in man. Diabetologia 1985;28(7):412–419.

    CAS  Article  PubMed  Google Scholar 

  33. 33.

    Condino AM, Aquilani R, Pasini E, Iadarola P, Viglio S, Verri M, D’Agostino L, Boschi F. Plasma kinetic of ingested essential amino acids in healthy elderly people. Aging Clin Exp Res 2013;25(6):711–714.

    Article  PubMed  Google Scholar 

  34. 34.

    Katsanos CS, Kobayashi H, Sheffield-Moore M, Aarsland A, Wolfe RR. Aging is associated with diminished accretion of muscle proteins after the ingestion of a small bolus of essential amino acids. Am J Clin Nutr 2005;82(5):1065–1073.

    CAS  PubMed  Google Scholar 

  35. 35.

    Volpi E, Kobayashi H, Sheffield-Moore M, Mittendorfer B, Wolfe RR. Essential amino acids are primarily responsible for the amino acid stimulation of muscle protein anabolism in healthy elderly adults. Am J Clin Nutr 2003;78(2):250–258.

    PubMed Central  CAS  PubMed  Google Scholar 

  36. 36.

    Koopman R, Crombach N, Gijsen AP, Walrand S, Fauquant J, Kies AK, Lemosquet S, Saris WHM, Boirie Y, van Loon LJC. Ingestion of a protein hydrolysate is accompanied by an accelerated in vivo digestion and absorption rate when compared with its intact protein. Am J Clin Nutr 2009;90(1):106–115.

    CAS  Article  PubMed  Google Scholar 

  37. 37.

    Pennings B, Boirie Y, Senden JMG, Gijsen AP, Kuipers H, van Loon LJC. Whey protein stimulates postprandial muscle protein accretion more effectively than do casein and casein hydrolysate in older men. Am J Clin Nutr 2011;93(5):997–1005.

    CAS  Article  PubMed  Google Scholar 

  38. 38.

    Luiking Y, Deutz NEP, Memelink RG, Verlaan S, Wolfe RR. Postprandial muscle protein synthesis is higher after a high whey protein, leucine-enriched supplement than after a dairy-like product in healthy older people: a randomized controlled trial. Nutr J 2014;13(9):E1–14.

    Google Scholar 

  39. 39.

    Børsheim E, Cree MG, Tipton KD, Elliott TA, Aarsland A, Wolfe RR. Effect of carbohydrate intake on net muscle protein synthesis during recovery from resistance exercise. 2004;96(674–678.

    Google Scholar 

  40. 40.

    Dangin M, Guillet C, Garcia-Rodenas C, Gachon P, Bouteloup-Demange C, Reiffers-Magnani K, Fauquant J, Ballèvre O, Beaufrère B. The rate of protein digestion affects protein gain differently during aging in humans. J Physiol 2003;549(2):635–644.

    PubMed Central  CAS  Article  PubMed  Google Scholar 

  41. 41.

    Hamer HM, Wall B, Kiskini A, de Lange A, Groen BB, Bakker JA, Gijsen AP, Verdijk LB, van Loon LJ. Carbohydrate co-ingestion with protein does not further augment post-prandial muscle protein accretion in older men. Nutr Metab (Lond) 2013;10(1):15.

    CAS  Article  Google Scholar 

  42. 42.

    Smith GI, P A, Villareal DT, Frimel TN, Rankin D, Rennie MJ, Mittendorfer B. Differences in muscle protein synthesis and anabolic signaling in the postabsorptive state and in response to food in 65–80 year old men and women. PLoS One 2008;3(3):e1875.

    PubMed Central  Article  PubMed  Google Scholar 

  43. 43.

    Churchward-Venne TA, Breen L, Di Donato DM, Hector AJ, Mitchell CJ, Moore DR, Stellingwerff T, Breuille D, Offord EA, Baker SK, Phillips SM. Leucine supplementation of a low-protein mixed macronutrient beverage enhances myofibrillar protein synthesis in young men: a double-blind, randomized trial. The American journal of clinical nutrition 2014;99(2):276–286.

    CAS  Article  PubMed  Google Scholar 

  44. 44.

    Rudman D, Mattson DE, Feller AG, Cotter R, Johnson RC. Fasting plasma amino acids in elderly men. Am J Clin Nutr 1989;49(3):559–566.

    CAS  PubMed  Google Scholar 

  45. 45.

    Polge A, Bancel E, Bellet H, Strubel D, Poirey S, Peray P, Carlet C, Magnan de Bornier B. Plasma amino acid concentrations in elderly patients with protein energy malnutrition. Age Ageing 1997;26(6):457–462.

    CAS  Article  PubMed  Google Scholar 

  46. 46.

    Caballero B, Gleason R, Wurtman R. Plasma amino acid concentrations in healthy elderly men and women. Am J Clin Nutr 1991;53(5):1249–1252.

    CAS  PubMed  Google Scholar 

  47. 47.

    Cuthbertson D, Smith K, Babraj J, Leese G, Waddell T, Atherton P, Wackerhage H, Taylor PM, Rennie MJ. Anabolic signaling deficits underlie amino acid resistance of wasting, aging muscle. FASEB J 2004;19(3):422–424.

    PubMed  Google Scholar 

  48. 48.

    Churchward-Venne TA, Burd NA, Mitchell CJ, West DWD, Philp A, Marcotte GR, Baker SK, Baar K, Phillips SM. Supplementation of a suboptimal protein dose with leucine or essential amino acids: effects on myofibrillar protein synthesis at rest and following resistance exercise in men. J Physiol 2012;590(11):2751–2765.

    PubMed Central  CAS  Article  PubMed  Google Scholar 

  49. 49.

    Breen L, Churchward-Venne TA. Leucine: a nutrient ‘trigger’ for muscle anabolism, but what more? J Physiol 2012;590(9):2065–2066.

    PubMed Central  CAS  Article  PubMed  Google Scholar 

  50. 50.

    Magne H, Savary-Auzeloux I, Migné C, Peyron M-A, Combaret L, Rémond D, Dardevet D. Contrarily to whey and high protein diets, dietary free leucine supplementation cannot reverse the lack of recovery of muscle mass after prolonged immobilization during ageing. J Physiol 2012;590(8):2035–2049.

    PubMed Central  CAS  Article  PubMed  Google Scholar 

  51. 51.

    Drummond MJ, Dreyer HC, Pennings B, Fry CS, Dhanani S, Dillon EL, Sheffield-Moore M, Volpi E, Rasmussen BB. Skeletal muscle protein anabolic response to resistance exercise and essential amino acids is delayed with aging. J Appl Physiol 2008;104(5):1452–1461.

    PubMed Central  CAS  Article  PubMed  Google Scholar 

  52. 52.

    Stoll B, Burrin DG. Measuring splanchnic amino acid metabolism in vivo using stable isotopic tracers. J Anim Sci 2006;84(E Suppl):E60–E72.

    PubMed  Google Scholar 

  53. 53.

    Staples AW, Burd N, West DWD, Currie KD, Atherton PJ, Moore DR, Rennie MJ, Macdonald MJ, Baker SK, Phillips SM. Carbohydrate does not augment exercise-induced protein accretion versus protein alone. Sci Sports Exerc 2011;43(7):1154–1161.

    CAS  Article  Google Scholar 

Download references

Author information

Affiliations

Authors

Corresponding author

Correspondence to Cameron Mitchell.

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

Milan, A.M., D’Souza, R.F., Pundir, S. et al. Older adults have delayed amino acid absorption after a high protein mixed breakfast meal. J Nutr Health Aging 19, 839–845 (2015). https://doi.org/10.1007/s12603-015-0500-5

Download citation

Keywords

  • Ageing
  • sarcopenia
  • protein digestion
  • mixed meal