The effects of endurance physical exercise with fat-free milk intake as a therapy for metabolic syndrome and/or sarcopenia

Main Article Content

Tetsuo Yamada Masaki Okada Masami Matsuzaki Akira Tanaka

Abstract

Background: Nutrition and exercise are important factors for addressing metabolic syndrome and sarcopenia as they are related to insulin secretion. Proteins, particularly branched-chain amino acids (BCAAs), have insulinotropic effects, while exercise reduces insulin secretion. It is thus important to investigate the effects of protein intake and exercise alone and in combination to determine suitable dietary and exercise therapies for treating metabolic syndrome and sarcopenia.


Methods: Eight healthy young adult female volunteers participated in a crossover trial consisting of two 5-day experiments. Days 1 and 2 comprised a body-weight-maintained adjustment period during which the participants consumed control diets (energy, 2,010 kcal; protein, 51.9 g). Days 3 to 5 comprised the treatment period during which the participants consumed experimental diets (energy, 2,010 kcal; protein 82.3 g) containing 402 kcal of fat-free milk, and either performed only normal daily activities (non-Ex) or performed normal daily activities and exercised on a bicycle with an ergometer at a target intensity of about 50% of the maximal oxygen intake, expending 402 kcal of additional energy (Ex). Total urine samples were collected during the daytime (6:45 to 18:45) and nighttime (18:45 to 6:45 the next morning). Fasting blood samples were collected early in the morning before and after the treatment period.


Results: Plasma valine, leucine, and BCAA levels were significantly elevated after both the non-Ex and Ex periods. Serum insulin levels were significantly elevated only after the non-Ex period. Urinary C-peptide immunoreactivity excretion levels increased significantly during the non-Ex period, but they decreased significantly during the Ex period. After the Ex period, the serum triglyceride and remnant lipoprotein-cholesterol (RLP-C) levels were significantly decreased. Homeostatic model assessment for insulin resistance (HOMA-IR) and atherosclerosis index (AI) values were slightly, yet significantly, increased after the non-Ex period, but were unchanged after the Ex period. The degree of change (Δ) in the RLP-C level significantly and positively correlated with the Δ HOMA-IR and Δ AI.


Conclusions: Exercise attenuated the insulinotropic effects of protein intake and had beneficial effects on glucose and lipid metabolism. Thus, protein intake in conjunction with exercise is recommended for preventing and/or improving metabolic syndrome and sarcopenia.

Article Details

How to Cite
YAMADA, Tetsuo et al. The effects of endurance physical exercise with fat-free milk intake as a therapy for metabolic syndrome and/or sarcopenia. Medical Research Archives, [S.l.], v. 12, n. 3, mar. 2024. ISSN 2375-1924. Available at: <https://esmed.org/MRA/mra/article/view/5158>. Date accessed: 13 apr. 2024. doi: https://doi.org/10.18103/mra.v12i3.5158.
Section
Research Articles

References

1. Castro-Barquero S, Ruiz-León AM, Sierra-Pérez M, Estruch R, Casas R. Dietary strategies for metabolic syndrome: A comprehensive review. Nutrients. Sep 29, 2020;12(10):2983. doi:10.3390/NU12102983

2. Holloszy JO. A forty-year memoir of research on the regulation of glucose transport into muscle. Am J Physiol Endocrinol Metab. 2003; 284(3):E453-E467. doi:10.1152/AJPENDO.00463.2002

3. Rodahl K, Miller HI, Issekutz B Jr. Plasma free fatty acids in exercise. J Appl Physiol. 1964; 19:489-492. doi:10.1152/JAPPL.1964.19.3.489

4. Carlson LA, Mossfeldt F. Acute effects of prolonged, heavy exercise on the concentration of plasma lipids and lipoproteins in man. Acta Physiol Scand. 1964;62(1-2):51-59. doi:10.1111/J.1748-1716.1964.TB03951.X

5. Papadopoulou SK, Papadimitriou K, Voulgaridou G, et al. Exercise and nutrition impact on osteoporosis and sarcopenia-The incidence of osteosarcopenia: A Narrative Review. Nutrients. Dec 16, 2021;13(12):4499. doi:10.3390/NU13124499

6. Mang ZA, Ducharme JB, Mermier C, Kravitz L, De Castro Magalhaes F, Amorim F. Aerobic adaptations to resistance training: The role of time under tension. Int J Sports Med. 2022; 43(10):829-839. doi:10.1055/A-1664-8701

7. Ganong WF. Review of medical physiology, 9th ed., Lange Medical Publications, Los Altos, 1979

8. Millward DJ, Bowtell JL, Pacy P, Rennie MJ. Physical activity, protein metabolism and protein requirements. Proc Nutr Soc. 1994;53 (1):223-240. doi:10.1079/PNS19940024

9. MacLean DA, Graham TE, Saltin B. Branched-chain amino acids augment ammonia metabolism while attenuating protein breakdown during exercise. Am J Physiol. 1994;267(6 Pt 1): E1010-E1022.
doi:10.1152/AJPENDO.1994.267.6.E1010

10. Kimball SR. The role of nutrition in stimulating muscle protein accretion at the molecular level. Biochem Soc Trans. 2007;35 (Pt 5):1298-1301. doi:10.1042/BST0351298

11. Berger S, Vongaraya N. Insulin response to ingested protein in diabetes. Diabetes. 1966; 15(5):303-306. doi:10.2337/DIAB.15.5.303

12. Holt SH, Miller JC, Petocz P. An insulin index of foods: the insulin demand generated by 1000-kJ portions of common foods. Am J Clin Nutr. 1997;66(5):1264-1276. doi:10.1093/AJCN/66.5.1264

13. Nuttall FQ, Gannon MC. Metabolic response of people with type 2 diabetes to a high protein diet. Nutr Metab (Lond). Sep 13, 2004;1:6. doi:10.1186/1743-7075-1-6

14. Richter EA, Sylow L, Hargreaves M. Interactions between insulin and exercise. Biochem J. 2021;478(21):3827-3846. doi:10.1042/BCJ20210185

15. Rennie MJ, Edwards RH, Krywawych S, et al. Effect of exercise on protein turnover in man. Clin Sci (Lond). 1981;61(5):627-639. doi:10.1042/CS0610627

16. Rennie MJ, Edwards RH, Davies CT, et al. Protein and amino acid turnover during and after exercise. Biochem Soc Trans. 1980;8(5): 499-501. doi:10.1042/BST0080499

17. Faul F, Erdfelder E, Lang AG, Buchner A. G*Power 3: a flexible statistical power analysis program for the social, behavioral, and biomedical sciences. Behav Res Methods. 2007;39(2):175-191. doi:10.3758/BF03193146

18. FAul F, Erdfelder E, Buchner A, Lang AG. Statistical power analyses using G*Power 3.1: tests for correlation and regression analyses. Behav Res Methods. 2009;41(4):1149-1160. doi:10.3758/BRM.41.4.1149

19. Yamada T, Kurasawa S, Matsuzaki M, Tanaka A. Remnant lipoprotein metabolism is improved more when body weight is reduced by exercise than by dietary restriction. Clin Chim Acta. 2008;388(1-2):28-32. doi:10.1016/J.CCA.2007.09.022

20. Ministry of Health and Welfare, Japan. Dietary Reference Intakes for Japanese, 2015, DAI-ICHI Shuppan Publishing, Tokyo, 2014

21. Report of the Subdivision on Resources, The Council for Science and Technology, Ministry of Education, Culture, Sports, Science and Technology, Japan. Standard Tables of Food Composition in Japan, 2015 (Seventh Revised Edition), Official Gazette Co-operation of Japan, Tokyo, 2015

22. Millward DJ, Davies CT, Halliday D, Wolman SL, Matthews D, Rennie M. Effect of exercise on protein metabolism in humans as explored with stable isotopes. Fed Proc. 1982;41(10):2686-2691.

23. Kraemer WJ, Ratamess NA, Nindl BC. Recovery responses of testosterone, growth hormone, and IGF-1 after resistance exercise. J Appl Physiol. 2017;122(3):549-558. doi:10.1152/JAPPLPHYSIOL.00599.2016

24. Janssen JAMJL. Impact of physical Exercise on endocrine aging. Front Horm Res. 2016;47:68-81. doi:10.1159/000445158

25. Schakman O, Kalista S, Barbé C, Loumaye A, Thissen JP. Glucocorticoid-induced skeletal muscle atrophy. Int J Biochem Cell Biol. 2013;45(10):2163-2172. doi:10.1016/J.BIOCEL.2013.05.036

26. Adamo ML, Farrar RP. Resistance training, and IGF involvement in the maintenance of muscle mass during the aging process. Ageing Res Rev. 2006;5(3):310-331. doi:10.1016/J.ARR.2006.05.001

27. Weltman A, Wideman L, Weltman JY, Veldhuis JD. Neuroendocrine control of GH release during acute aerobic exercise. J Endocrinol Invest. 2003;26(9):843-850. doi:10.1007/BF03345234

28. Kraemer WJ, Ratamess NA, Hymer WC, Nindl BC, Fragala MS. Growth hormone(s), testosterone, insulin-like growth factors, and cortisol: Roles and integration for cellular development and growth with exercise. Front Endocrinol (Lausanne). Feb 25, 2020;11:33. doi:10.3389/FENDO.2020.00033

29. Young VR, Munro HN. Ntau-methylhistidine (3-methylhistidine) and muscle protein turnover: an overview. Fed Proc. 1978;37(9):2291-2300.

30. Yamada T, Matsuzaki M, Tanaka A. Increase in insulin secretion and decrease in muscle degradation by fat-free milk intake are attenuated by physical exercise. Clin Chim Acta. 2018;484:21-25.
doi:10.1016/J.CCA.2018.05.017

31. Nagasawa T, Hirano J, Yoshizawa F, Nishizawa N. Myofibrillar protein catabolism is rapidly suppressed following protein feeding. Biosci Biotechnol Biochem. 1998;62(10):1932-1937. doi:10.1271/BBB.62.1932

32. Dohm GL, Williams RT, Kasperek GJ, Van Rij AM. Increased excretion of urea and N tau -methylhistidine by rats and humans after a bout of exercise. J Appl Physiol Respir Environ Exerc Physiol. 1982;52(1):27-33. doi:10.1152/JAPPL.1982.52.1.27

33. Viru A. Mobilisation of structural proteins during exercise. Sports Med. 1987;4(2):95-128. doi:10.2165/00007256-198704020-00003

34. Galbo H, Tobin L, Van Loon LJC. Responses to acute exercise in type 2 diabetes, with an emphasis on metabolism and interaction with oral hypoglycemic agents and food intake. Appl Physiol Nutr Metab. 2007;32(3):567-575. doi:10.1139/H07-029

35. Sonoda R, Tanaka K, Kikuchi T, et al. C-peptide level in fasting plasma and pooled urine predicts HbA1c after hospitalization in patients with type 2 diabetes mellitus. PLoS One. Feb 5, 2016;11(2):e0147303.
doi:10.1371/JOURNAL.PONE.0147303

36. Lithell H, Orlander J, Schéle R, Sjödin B, Karlsson J. Changes in lipoprotein-lipase activity and lipid stores in human skeletal muscle with prolonged heavy exercise. Acta Physiol Scand. 1979;107(3):257-261. doi:10.1111/J.1748-1716.1979.TB06471.X

37. Jakicic JM, Otto AD. Physical activity considerations for the treatment and prevention of obesity. Am J Clin Nutr. 2005; 82(1 Suppl): 226S-229S. doi:10.1093/AJCN/82.1.226S

38. Gill JM, Hardman AE. Postprandial lipemia: effects of exercise and restriction of energy intake compared. Am J Clin Nutr. 2000;71(2): 465-471. doi:10.1093/AJCN/71.2.465

39. McNamara JR, Shah PK, Nakajima K, et al. Remnant-like particle (RLP) cholesterol is an independent cardiovascular disease risk factor in women: results from the Framingham Heart Study. Atherosclerosis. 2001;154(1):229-236. doi:10.1016/S0021-9150(00)00484-6

40. Ai M, Tanaka A, Ogita K, et al. Relationship between hyperinsulinemia and remnant lipoprotein concentrations in patients with impaired glucose tolerance. J Clin Endocrinol Metab. 2000;85(10):3557-3560.
doi:10.1210/JCEM.85.10.6894

41. Gill JMR, Al-Mamari A, Ferrell WR, et al. Effects of a moderate exercise session on postprandial lipoproteins, apolipoproteins and lipoprotein remnants in middle-aged men. Atherosclerosis. 2006;185(1):87-96. doi:10.1016/J.ATHEROSCLEROSIS.2005.06.009

42. Koutsari C, Karpe F, Humphreys SM, Frayn KN, Hardman AE. Exercise prevents the accumulation of triglyceride-rich lipoproteins and their remnants seen when changing to a high-carbohydrate diet. Arterioscler Thromb Vasc Biol. 2001;21(9):1520-1525. doi:10.1161/HQ0901.095553

43. She P, Reid TM, Bronson SK, et al. Disruption of BCATm in mice leads to increased energy expenditure associated with the activation of a futile protein turnover cycle. Cell Metab. 2007;6(3):181-194. doi:10.1016/J.CMET.2007.08.003

44. Kadota Y, Kazama S, Bajotto G, Kitaura Y, Shimomura Y. Clofibrate-induced reduction of plasma branched-chain amino acid concentrations impairs glucose tolerance in rats. JPEN J Parenter Enteral Nutr. 2012;36(3): 337-343. doi:10.1177/0148607111414578

45. Newgard CB, An J, Bain JR, et al. A branched-chain amino acid-related metabolic signature that differentiates obese and lean humans and contributes to insulin resistance. Cell Metab. 2009;9(4):311-326.
doi:10.1016/J.CMET.2009.02.002

46. Rietman A, Schwarz J, Tomé D, Kok FJ, Mensink M. High dietary protein intake, reducing or eliciting insulin resistance? Eur J Clin Nutr. 2014;68(9):973-979. doi:10.1038/EJCN.2014.123

47. Lynch CJ, Adams SH. Branched-chain amino acids in metabolic signalling and insulin resistance. Nat Rev Endocrinol. 2014;10(12): 723-736. doi:10.1038/NRENDO.2014.171

48. Piatti PM, Monti F, Fermo I, et al. Hypocaloric high-protein diet improves glucose oxidation and spares lean body mass: comparison to hypocaloric high-carbohydrate diet. Metabolism. 1994;43(12):1481-1487. doi:10.1016/0026-0495(94)90005-1

49. Layman DK, Baum JI. Dietary protein impact on glycemic control during weight loss. J Nutr. 2004;134(4):968S-973S. doi:10.1093/JN/134.4.968S

50. Metges CC, Barth CA. Metabolic consequences of a high dietary-protein intake in adulthood: assessment of the available evidence. J Nutr. 2000;130(4):886-889. doi:10.1093/JN/130.4.886