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The association between meat consumption and muscle strength index in young adults: the mediating role of total protein intake and lean mass percentage

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Abstract

Purpose

The aim of this study was to analyse the associations between the consumption of different types of meat and the muscle strength index (MSI) and to examine whether this relationship is mediated by total protein intake (TPI) and lean mass percentage (LM%) in young adults.

Methods

We conducted a cross-sectional study with first-year university students from Castilla-La Mancha, Spain. Different types of meat consumption (total, red, processed, and white and fish) were separately evaluated using a Food-Frequency Questionnaire. MSI was determined from the handgrip and standing long jump tests. ANCOVA models were used to test the mean differences in MSI by categories of meat consumption. Serial multiple mediation models were used to explore the mediating role of TPI and LM% in the relationship between meat consumption and MSI. All analyses were adjusted for age, sex, and socioeconomic level, identified through a directed acyclic graph. Additional analyses were performed with a small subsample including alcohol intake, tobacco smoking, physical activity, cardiorespiratory fitness, and total energy intake as covariates in the multiple mediation models.

Results

A total of 230 students (mean age 21.1 ± 2.1 years, 66.5% women) were included in the analysis. Young adults with higher meat consumption (total, red, and white and fish) had higher MSI adjusted means than their peers with lower meat consumption (p < 0.05). These associations did not remain after controlling for TPI and LM%. In adjusted mediation analyses, a significant indirect effect was observed through TPI and LM% in the associations between each of the types of meat consumption and MSI. In the additional analyses, a greater effect of white and fish meat consumption on muscle strength through mediation of TPI and LM% was reported compared to red or processed meat consumption, and no significant effects were observed between processed meat consumption and MSI.

Conclusion

Higher consumption of total, red, and white and fish meat was associated with increased MSI in young adults. TPI and LM% mediated this relationship.

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Availability of data and materials

The datasets generated and analysed in this study are available from the corresponding author on reasonable request.

References

  1. Godfray HCJ, Aveyard P, Garnett T, Hall JW, Key TJ, Lorimer J et al (2018) Meat consumption, health, and the environment. Science 361(6399):eaam5324. https://doi.org/10.1126/science.aam5324

    Article  CAS  PubMed  Google Scholar 

  2. Ministerio de Agricultura Pesca y Alimentación (2020) Informe del consumo de alimentación en España 2019. https://www.mapa.gob.es/en/alimentacion/temas/consumo-tendencias/informe2019_v2_tcm38-540250.pdf. Accesed 22 Dec 2021

  3. Wu G, Fanzo J, Miller DD, Pingali P, Post M, Steiner JL et al (2014) Production and supply of high-quality food protein for human consumption: sustainability, challenges, and innovations. Ann N Y Acad Sci 1321(1):1–19. https://doi.org/10.1111/NYAS.12500

    Article  CAS  PubMed  Google Scholar 

  4. González N, Marquès M, Nadal M, Domingo JL (2020) Meat consumption: which are the current global risks? A review of recent (2010–2020) evidences. Food Res Int 137:109341. https://doi.org/10.1016/J.FOODRES.2020.109341

    Article  PubMed  PubMed Central  Google Scholar 

  5. Wu G (2016) Dietary protein intake and human health. Food Funct 7(3):1251–1265. https://doi.org/10.1039/c5fo01530h

    Article  CAS  PubMed  Google Scholar 

  6. Harris C, Buyken A, Von Berg A, Berdel D, Lehmann I, Hoffmann B et al (2016) Prospective associations of meat consumption during childhood with measures of body composition during adolescence: results from the GINIplus and LISAplus birth cohorts. Nutr J 15(1):1–10. https://doi.org/10.1186/s12937-016-0222-5

    Article  CAS  Google Scholar 

  7. García-Hermoso A, Cavero-Redondo I, Ramírez-Vélez R, Ruiz JR, Ortega FB, Lee DC et al (2018) Muscular strength as a predictor of all-cause mortality in an apparently healthy population: a systematic review and meta-analysis of data from approximately 2 million men and women. Arch Phys Med Rehabil 99(10):2100-2113.e5. https://doi.org/10.1016/J.APMR.2018.01.008

    Article  PubMed  Google Scholar 

  8. Lynch GS, Koopman R (2018) Dietary meat and protection against sarcopenia. Meat Sci 144:180–185. https://doi.org/10.1016/J.MEATSCI.2018.06.023

    Article  PubMed  Google Scholar 

  9. Moon K, Krems C, Heuer T, Hoffmann I (2021) Association between body mass index and macronutrients differs along the body mass index range of German adults: results from the German National Nutrition Survey II. J Nutr Sci 10:1–8. https://doi.org/10.1017/JNS.2020.60

    Article  Google Scholar 

  10. Mangano KM, Sahni S, Kiel DP, Tucker KL, Dufour AB, Hannan MT (2017) Dietary protein is associated with musculoskeletal health independently of dietary pattern: the Framingham third generation study. Am J Clin Nutr 105(3):714–722. https://doi.org/10.3945/ajcn.116.136762

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  11. Travison T, Araujo A, Esche G, Beck T, McKinlay J (2008) Lean mass and not fat mass is associated with male proximal femur strength. J Bone Miner Res 23(2):189–198. https://doi.org/10.1359/JBMR.071016

    Article  PubMed  Google Scholar 

  12. Tomé D, Benoit S, Azzout-Marniche D (2021) Protein metabolism and related body function: mechanistic approaches and health consequences. Proc Nutr Soc 80(2):243–251. https://doi.org/10.1017/S0029665120007880

    Article  CAS  PubMed  Google Scholar 

  13. Johnson N, Kotarsky C, Hackney K, Trautman K, Dicks N, Byun W et al (2021) Measures derived from panoramic ultrasonography and animal-based protein intake are related to muscular performance in middle-aged adults. J Clin Med 10(5):988. https://doi.org/10.3390/JCM10050988

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  14. Bradlee ML, Mustafa J, Singer MR, Moore LL (2018) High-protein foods and physical activity protect against age-related muscle loss and functional decline. J Gerontol A Biol Sci Med Sci 73(1):88–94. https://doi.org/10.1093/gerona/glx070

    Article  CAS  Google Scholar 

  15. Valenzuela P, Mata F, Morales J, Castillo-García A, Lucia A (2019) Does beef protein supplementation improve body composition and exercise performance? A systematic review and meta-analysis of randomized controlled trials. Nutrients. https://doi.org/10.3390/NU11061429

    Article  PubMed  PubMed Central  Google Scholar 

  16. McGregor RA, Cameron-Smith D, Poppitt SD (2014) It is not just muscle mass: a review of muscle quality, composition and metabolism during ageing as determinants of muscle function and mobility in later life. Longev Health 3(1):1–8. https://doi.org/10.1186/2046-2395-3-9

    Article  Google Scholar 

  17. Celis-Morales CA, Petermann F, Steell L, Anderson J, Welsh P, Mackay DF et al (2018) Associations of dietary protein intake with fat-free mass and grip strength: a cross-sectional study in 146,816 UK biobank participants. Am J Epidemiol 187(11):2405–2414. https://doi.org/10.1093/aje/kwy134

    Article  PubMed  Google Scholar 

  18. Morgan PT, Harris DO, Marshall RN, Quinlan JI, Edwards SJ, Allen SL et al (2021) Protein source and quality for skeletal muscle anabolism in young and older adults: a systematic review and meta-analysis. J Nutr. https://doi.org/10.1093/jn/nxab055

    Article  PubMed  PubMed Central  Google Scholar 

  19. Gutiérrez-Fisac JL, Guallar-Castillón P, León-Muñoz LM, Graciani A, Banegas JR, Rodríguez-Artalejo F (2012) Prevalence of general and abdominal obesity in the adult population of Spain, 2008–2010: the ENRICA study. Obes Rev 13(4):388–392. https://doi.org/10.1111/J.1467-789X.2011.00964.X

    Article  PubMed  Google Scholar 

  20. Lee H, Cashin AG, Lamb SE, Hopewell S, Vansteelandt S, VanderWeele TJ et al (2021) A guideline for reporting mediation analyses of randomized trials and observational studies: the AGReMA statement. JAMA 326(11):1045–1056. https://doi.org/10.1001/JAMA.2021.14075

    Article  PubMed  PubMed Central  Google Scholar 

  21. Fernández-Ballart JD, Piñol JL, Zazpe I, Corella D, Carrasco P, Toledo E et al (2010) Relative validity of a semi-quantitative food-frequency questionnaire in an elderly Mediterranean population of Spain. Br J Nutr 103(12):1808–1816. https://doi.org/10.1017/S0007114509993837

    Article  CAS  PubMed  Google Scholar 

  22. Moreiras O, Carbajal A, Cabrera L, Cuadrado C (2018) Tablas de composición de alimentos. Guía de practices, 19th edn. Piramide, Madrid

    Google Scholar 

  23. Léger LA, Mercier D, Gadoury C, Lambert J (1988) The multistage 20 metre shuttle run test for aerobic fitness. J Sports Sci 6(2):93–101. https://doi.org/10.1080/02640418808729800

    Article  PubMed  Google Scholar 

  24. da Silva ICM, van Hees VT, Ramires VV, Knuth AG, Bielemann RM, Ekelund U et al (2014) Physical activity levels in three Brazilian birth cohorts as assessed with raw triaxial wrist accelerometry. Int J Epidemiol 43(6):1959–1968. https://doi.org/10.1093/IJE/DYU203

    Article  PubMed  PubMed Central  Google Scholar 

  25. Alexandrov NV, Eelderink C, Singh-Povel CM, Navis GJ, Bakker SJL, Corpeleijn E (2018) Dietary protein sources and muscle mass over the life course: the lifelines cohort study. Nutrients. https://doi.org/10.3390/nu10101471

    Article  PubMed  PubMed Central  Google Scholar 

  26. Textor J, van der Zander B, Gilthorpe MS, Liśkiewicz M, Ellison GT (2016) Robust causal inference using directed acyclic graphs: the R package dagitty. Int J Epidemiol 45(6):1887–1894. https://doi.org/10.1093/IJE/DYW341

    Article  PubMed  Google Scholar 

  27. Tennant PWG, Murray EJ, Arnold KF, Berrie L, Fox MP, Gadd SC et al (2021) Use of directed acyclic graphs (DAGs) to identify confounders in applied health research: review and recommendations. Int J Epidemiol 50(2):620–632. https://doi.org/10.1093/IJE/DYAA213

    Article  PubMed  Google Scholar 

  28. Hayes AF (2018) Introduction to mediation, moderation, and conditional process analysis: a regression-based approach, 2nd edn. The Guilford Press, New York

    Google Scholar 

  29. Symons TB, Schutzler SE, Cocke TL, Chinkes DL, Wolfe RR, Paddon-Jones D (2007) Aging does not impair the anabolic response to a protein-rich meal. Am J Clin Nutr 86(2):451–456. https://doi.org/10.1093/ajcn/86.2.451

    Article  CAS  PubMed  Google Scholar 

  30. Negro M, Vandoni M, Ottobrini S, Codrons E, Correale L, Buonocore D et al (2014) Protein supplementation with low fat meat after resistance training: effects on body composition and strength. Nutrients 6(8):3040–3049. https://doi.org/10.3390/NU6083040

    Article  PubMed  PubMed Central  Google Scholar 

  31. Sharp MH, Lowery RP, Shields KA, Lane JR, Gray JL, Partl JM et al (2018) The effects of beef, chicken, or whey protein after workout on body composition and muscle performance. J Strength Cond Res 32(8):2233–2242. https://doi.org/10.1519/JSC.0000000000001936

    Article  PubMed  Google Scholar 

  32. Assmann K, Joslowski G, Buyken A, Cheng G, Remer T, Kroke A et al (2013) Prospective association of protein intake during puberty with body composition in young adulthood. Obes. https://doi.org/10.1002/OBY.20516

    Article  Google Scholar 

  33. Burd NA, Gorissen SH, Van Vliet S, Snijders T, Van Loon LJC (2015) Differences in postprandial protein handling after beef compared with milk ingestion during postexercise recovery: a randomized controlled trial. Am J Clin Nutr 102(4):828–836. https://doi.org/10.3945/ajcn.114.103184

    Article  CAS  PubMed  Google Scholar 

  34. Guimarães B, Pimenta L, Massini D, Dos Santos D, Siqueira L, Simionato A et al (2018) Muscle strength and regional lean body mass influence on mineral bone health in young male adults. PLoS ONE. https://doi.org/10.1371/JOURNAL.PONE.0191769

    Article  PubMed  PubMed Central  Google Scholar 

  35. 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(3):356–361. https://doi.org/10.1093/gerona/glv184

    Article  CAS  PubMed  Google Scholar 

  36. Vaara JP, Vasankari T, Wyss T, Pihlainen K, Ojanen T, Raitanen J et al (2020) Device-based measures of sedentary time and physical activity are associated with physical fitness and body fat content. Front Sport Act Living. https://doi.org/10.3389/FSPOR.2020.587789

    Article  Google Scholar 

  37. Burd NA, McKenna CF, Salvador AF, Paulussen KJM, Moore DR (2019) Dietary protein quantity, quality, and exercise are key to healthy living: a muscle-centric perspective across the lifespan. Front Nutr 6:83. https://doi.org/10.3389/fnut.2019.00083

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  38. Nicklas TA, O’Neil CE, Zanovec M, Keast DR, Fulgoni VL (2012) Contribution of beef consumption to nutrient intake, diet quality, and food patterns in the diets of the US population. Meat Sci 90(1):152–158. https://doi.org/10.1016/J.MEATSCI.2011.06.021

    Article  PubMed  Google Scholar 

  39. Zagarins SE, Ronnenberg AG, Bertone-Johnson ER (2021) Established diet quality indices are not universally associated with body composition in young adult women. Public Health Nutr 24(9):2465–2472. https://doi.org/10.1017/S1368980021001440

    Article  PubMed  Google Scholar 

  40. Järvinen L, Lundin Petersdotter S, Chaillou T (2022) High-intensity resistance exercise is not as effective as traditional high-intensity interval exercise for increasing the cardiorespiratory response and energy expenditure in recreationally active subjects. Eur J Appl Physiol 122(2):459–474. https://doi.org/10.1007/S00421-021-04849-4

    Article  PubMed  Google Scholar 

  41. Li Y, Liu J, Quan M, Zhuang J, Cao Z-B, Zhu Z et al (2022) Energy costs of household and eldercare activities in young to middle-aged chinese adults. J Phys Act Health 19(6):404–408. https://doi.org/10.1123/JPAH.2022-0011

    Article  PubMed  Google Scholar 

  42. Waijers PMCM, Feskens EJM, Ocké MC (2007) A critical review of predefined diet quality scores. Br J Nutr 97(2):219–231. https://doi.org/10.1017/S0007114507250421

    Article  CAS  PubMed  Google Scholar 

  43. Wyness L (2016) The role of red meat in the diet: nutrition and health benefits. Proc Nutr Soc 75(3):227–232. https://doi.org/10.1017/S0029665115004267

    Article  PubMed  Google Scholar 

  44. Phillips SM, Chevalier S, Leidy HJ (2016) Protein “requirements” beyond the RDA: implications for optimizing health. Appl Physiol Nutr Metab 41(5):565–572. https://doi.org/10.1139/apnm-2015-0550

    Article  CAS  PubMed  Google Scholar 

  45. Daly RM, O’Connell SL, Mundell NL, Grimes CA, Dunstan DW, Nowson CA (2014) Protein-enriched diet, with the use of lean red meat, combined with progressive resistance training enhances lean tissue mass and muscle strength and reduces circulating IL-6 concentrations in elderly women: a cluster randomized controlled trial. Am J Clin Nutr 99(4):899–910. https://doi.org/10.3945/ajcn.113.064154

    Article  CAS  PubMed  Google Scholar 

  46. Bouvard V, Loomis D, Guyton KZ, Grosse Y, El GF, Benbrahim-Tallaa L et al (2015) Carcinogenicity of consumption of red and processed meat. Lancet Oncol 16(16):1599–1600. https://doi.org/10.1016/S1470-2045(15)00444-1

    Article  PubMed  Google Scholar 

  47. Becerra-Tomás N, Babio N, Martínez-González MÁ, Corella D, Estruch R, Ros E et al (2016) Replacing red meat and processed red meat for white meat, fish, legumes or eggs is associated with lower risk of incidence of metabolic syndrome. Clin Nutr 35(6):1442–1449. https://doi.org/10.1016/J.CLNU.2016.03.017

    Article  PubMed  Google Scholar 

  48. Giugliano D, Ceriello A, Esposito K (2006) The effects of diet on inflammation: emphasis on the metabolic syndrome. J Am Coll Cardiol 48(4):677–685. https://doi.org/10.1016/J.JACC.2006.03.052

    Article  CAS  PubMed  Google Scholar 

  49. Nikawa T, Ulla A, Sakakibara I (2021) Polyphenols and their effects on muscle atrophy and muscle health. Molecules. https://doi.org/10.3390/MOLECULES26164887

    Article  PubMed  PubMed Central  Google Scholar 

  50. Nielsen T, Würtz A, Dahm C, Overvad K, Tjønneland A (2021) Substitution of unprocessed and processed red meat with poultry or fish and total and cause-specific mortality. Br J Nutr. https://doi.org/10.1017/S0007114521001252

    Article  PubMed  Google Scholar 

  51. Petermann-Rocha F, Parra-Soto S, Gray S, Anderson J, Welsh P, Gill J et al (2021) Vegetarians, fish, poultry, and meat-eaters: who has higher risk of cardiovascular disease incidence and mortality? A prospective study from UK Biobank. Eur Heart J 42(12):1136–1143. https://doi.org/10.1093/eurheartj/ehaa939

    Article  PubMed  Google Scholar 

  52. Cordeiro EM, de Oliveira GV, Volino-Souza M, Velozo O, do C, Alvares TS, (2020) Effects of fish protein hydrolysate ingestion on postexercise aminoacidemia compared with whey protein hydrolysate in young individuals. J Food Sci 85(1):21–27. https://doi.org/10.1111/1750-3841.14970

    Article  CAS  PubMed  Google Scholar 

  53. Ho FK, Gray SR, Welsh P, Petermann-Rocha F, Foster H, Waddell H et al (2020) Associations of fat and carbohydrate intake with cardiovascular disease and mortality: prospective cohort study of UK Biobank participants. BMJ. https://doi.org/10.1136/bmj.m688

    Article  PubMed  PubMed Central  Google Scholar 

  54. Clark MA, Springmann M, Hill J, Tilman D (2019) Multiple health and environmental impacts of foods. Proc Natl Acad Sci USA 116(46):23357. https://doi.org/10.1073/PNAS.1906908116

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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Acknowledgements

The authors thank all participants of the study.

Funding

This research was funded by a grant from the European Regional Development Fund (Fondo Europeo de Desarrollo Regional [FEDER]). B.B.-P. is supported by a grant from the Universidad de Castilla‐La Mancha co-financed by the European Social Fund (2020-PREDUCLM-16746). R.F.-R. was supported by a grant from the Spanish Ministry of Education, Culture and Sport (FPU 19/00167). Dr. Mesas is financially supported by a ‘Beatriz Galindo’ contract (BEAGAL18/00093) from the Spanish Ministry of Education, Culture and Sport. This work was also supported by the National Agency for Research and Innovation (POS_EXT_2020_20_1_165371). The funders had no role in the study design, data analysis, interpretation of the results, or preparation to publish the manuscript.

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Authors and Affiliations

  1. Health and Social Research Center, Universidad de Castilla-La Mancha, C/Santa Teresa Jornet, s/n, 16071, Cuenca, Spain

    Bruno Bizzozero-Peroni, Vicente Martínez-Vizcaíno, Miriam Garrido-Miguel, Rubén Fernández-Rodríguez & Arthur Eumann Mesas

  2. Instituto Superior de Educación Física, Universidad de la República, 40000, Rivera, Uruguay

    Bruno Bizzozero-Peroni

  3. Facultad de Ciencias de la Salud, Universidad Autónoma de Chile, 1101, Talca, Chile

    Vicente Martínez-Vizcaíno

  4. Facultad de Enfermería, Universidad de Castilla-La Mancha, 02006, Albacete, Spain

    Miriam Garrido-Miguel

  5. Facultad de Fisioterapia y Enfermería, Universidad de Castilla-La Mancha, 45002, Toledo, Spain

    Ana Torres-Costoso, Asunción Ferri-Morales & Noelia M. Martín-Espinosa

  6. Postgraduate Program in Public Health, Universidade Estadual de Londrina, Londrina, Paraná, 86057-970, Brazil

    Arthur Eumann Mesas

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  1. Bruno Bizzozero-Peroni
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Contributions

Conceptualization, BB-P, AEM, and VM-V; methodology and formal analysis, BB-P and AEM; writing—original draft, BB-P and AEM; writing—review and editing, BB-P, AEM, VM-V, MG-M, RF-R, AT-C, AF-G, and NMM-E; funding acquisition, AEM and VM-V; supervision, AEM and VM-V. All authors approved the final manuscript.

Corresponding author

Correspondence to Miriam Garrido-Miguel.

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The authors declare that they have no competing interests.

Ethics approval and consent to participate

The study protocol was approved by the Clinical Research Ethics Committee of the “Virgen de la Luz” of Cuenca (REG: 2016jPI1116) and adhered to the principles of the Declaration of Helsinki. Informed consent to participate was obtained from all subjects involved in the study.

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Bizzozero-Peroni, B., Martínez-Vizcaíno, V., Garrido-Miguel, M. et al. The association between meat consumption and muscle strength index in young adults: the mediating role of total protein intake and lean mass percentage. Eur J Nutr 62, 673–683 (2023). https://doi.org/10.1007/s00394-022-03014-7

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