Physical Activity Modifies the Association between Dietary Protein and Lean Mass of Postmenopausal Women

Published:November 30, 2016DOI:https://doi.org/10.1016/j.jand.2016.10.009

      Abstract

      Background

      Maintenance of lean muscle mass and related strength is associated with lower risk for numerous chronic diseases of aging in women.

      Objective

      Our aim was to evaluate whether the association between dietary protein and lean mass differs by physical activity level, amino acid composition, and body mass index categories.

      Design

      We performed a cross-sectional analysis of a prospective cohort.

      Participants/setting

      Participants were postmenopausal women from the Women’s Health Initiative with body composition measurements by dual-energy x-ray absorptiometry (n=8,298).

      Main outcome measures

      Our study measured percent lean mass, percent fat mass, and lean body mass index.

      Statistical analyses performed

      Linear regression models adjusted for scanner serial number, age, calibrated energy intake, race/ethnicity, neighborhood socioeconomic status, and recreational physical activity were used to determine the relationship between protein intake and body composition measures. Likelihood ratio tests and stratified analysis were used to investigate physical activity and body mass index as potential effect modifiers.

      Results

      Biomarker-calibrated protein intake was positively associated with percent lean mass; women in the highest protein quintile had 6.3 percentage points higher lean mass than the lowest quintile (P<0.001). This difference rose to 8.5 percentage points for physically active women in the highest protein quintile (Pinteraction=0.023). Percent fat mass and lean body mass index were both inversely related to protein intake (both P<0.001). Physical activity further reduced percent fat mass (Pinteraction=0.022) and lean body mass index (Pinteraction=0.011). Leucine intake was associated with lean mass, as were branched chain amino acids combined (both P<0.001), but not independent of total protein. All associations were observed for normal-weight, overweight, and obese women.

      Conclusions

      Protein consumption up to 2.02 g/kg body weight daily is positively associated with lean mass in postmenopausal women. Importantly, those that also engage in physical activity have the highest lean mass across body mass index categories.

      Keywords

      To read this article in full you will need to make a payment

      Purchase one-time access:

      Academic & Personal: 24 hour online accessCorporate R&D Professionals: 24 hour online access
      One-time access price info
      • For academic or personal research use, select 'Academic and Personal'
      • For corporate R&D use, select 'Corporate R&D Professionals'

      Subscribe:

      Subscribe to Journal of the Academy of Nutrition and Dietetics
      Already a print subscriber? Claim online access
      Already an online subscriber? Sign in
      Institutional Access: Sign in to ScienceDirect

      References

        • Zamboni M.
        • Mazzali G.
        • Fantin F.
        • Rossi A.
        • Di Francesco V.
        Sarcopenic obesity: A new category of obesity in the elderly.
        Nutr Metab Cardiovasc Dis. 2008; 18: 388-395
        • Hurley B.F.
        • Hanson E.D.
        • Sheaff A.K.
        Strength training as a countermeasure to aging muscle and chronic disease.
        Sports Med. 2011; 41: 289-306
        • Krieger J.W.
        • Sitren H.S.
        • Daniels M.J.
        • Langkamp-Henken B.
        Effects of variation in protein and carbohydrate intake on body mass and composition during energy restriction: A meta-regression 1.
        Am J Clin Nutr. 2006; 83: 260-274
        • Layman D.K.
        • Evans E.M.
        • Erickson D.
        • et al.
        A moderate-protein diet produces sustained weight loss and long-term changes in body composition and blood lipids in obese adults.
        J Nutr. 2009; 139: 514-521
        • Mojtahedi M.C.
        • Thorpe M.P.
        • Karampinos D.C.
        • et al.
        The effects of a higher protein intake during energy restriction on changes in body composition and physical function in older women.
        J Gerontol A Biol Sci Med Sci. 2011; 66: 1218-1225
        • Phillips S.M.
        • Van Loon L.J.
        Dietary protein for athletes: From requirements to optimum adaptation.
        J Sports Sci. 2011; 29: S29-S38
        • Bray G.A.
        • Smith S.R.
        • de Jonge L.
        • et al.
        Effect of dietary protein content on weight gain, energy expenditure, and body composition during overeating: A randomized controlled trial.
        JAMA. 2012; 307: 47-55
        • Laplante M.
        • Sabatini D.M.
        mTOR signaling in growth control and disease.
        Cell. 2012; 149: 274-293
        • Casperson S.L.
        • Sheffield-Moore M.
        • Hewlings S.J.
        • Paddon-Jones D.
        Leucine supplementation chronically improves muscle protein synthesis in older adults consuming the RDA for protein.
        Clin Nutr. 2012; 31: 512-519
        • Qin L.Q.
        • Xun P.
        • Bujnowski D.
        • et al.
        Higher branched-chain amino acid intake is associated with a lower prevalence of being overweight or obese in middle-aged East Asian and Western adults.
        J Nutr. 2011; 141: 249-254
        • Volpi E.
        • Campbell W.W.
        • Dwyer J.T.
        • et al.
        Is the optimal level of protein intake for older adults greater than the Recommended Dietary Allowance?.
        J Gerontol A Biol Sci Med Sci. 2013; 68: 677-681
        • Deutz N.E.
        • Bauer J.M.
        • Barazzoni R.
        • et al.
        Protein intake and exercise for optimal muscle function with aging: Recommendations from the ESPEN Expert Group.
        Clin Nutr. 2014; 33: 929-936
        • Brochu M.
        • Mathieu M.E.
        • Karelis A.D.
        • et al.
        Contribution of the lean body mass to insulin resistance in postmenopausal women with visceral obesity: A Monet study.
        Obesity (Silver Spring). 2008; 16: 1085-1093
        • O'Gorman D.J.
        • Krook A.
        Exercise and the treatment of diabetes and obesity.
        Med Clin North Am. 2011; 95: 953-969
      1. Design of the Women's Health Initiative clinical trial and observational study. The Women's Health Initiative Study Group.
        Control Clin Trials. 1998; 19: 61-109
        • Neuhouser M.L.
        • Tinker L.
        • Shaw P.A.
        • et al.
        Use of recovery biomarkers to calibrate nutrient consumption self-reports in the Women's Health Initiative.
        Am J Epidemiol. 2008; 167: 1247-1259
        • Chen Z.
        • Bassford T.
        • Green S.B.
        • et al.
        Postmenopausal hormone therapy and body composition—A substudy of the estrogen plus progestin trial of the Women's Health Initiative.
        Am J Clin Nutr. 2005; 82: 651-656
        • Patterson R.E.
        • Kristal A.R.
        • Tinker L.F.
        • Carter R.A.
        • Bolton M.P.
        • Agurs-Collins T.
        Measurement characteristics of the Women's Health Initiative food frequency questionnaire.
        Ann Epidemiol. 1999; 9: 178-187
        • Schakel S.F.
        Maintaining a nutrient database in a changing marketplace: Keeping pace with changing food products—A research perspective.
        J Food Comp Anal. 2001; 14: 315-322
      2. US Department of Agriculture. Dietary Reference Intakes: Estimated average requirements and recommended intakes. http://fnic.nal.usda.gov/dietary-guidance/dietary-reference-intakes/dri-tables-and-application-reports. Accessed June 30, 2016.

        • Ainsworth B.E.
        • Haskell W.L.
        • Herrmann S.D.
        • et al.
        2011 Compendium of Physical activities: A second update of codes and MET values.
        Med Sci Sports Exerc. 2011; 43: 1575-1581
        • US Department of Health and Human Services, Office of Disease Prevention and Health Promotion
        Physical Activity Guidelines for Americans.
        US Department of Health and Human Services, Washington2008
        • Shiroma E.J.
        • Sesso H.D.
        • Lee I.M.
        Physical activity and weight gain prevention in older men.
        Int J Obes (Lond). 2012; 36: 1165-1169
        • Qi L.
        • Nassir R.
        • Kosoy R.
        • et al.
        Relationship between diabetes risk and admixture in postmenopausal African-American and Hispanic-American women.
        Diabetologia. 2012; 55: 1329-1337
        • Beasley J.M.
        • Wertheim B.C.
        • LaCroix A.Z.
        • et al.
        Biomarker-calibrated protein intake and physical function in the Women's Health Initiative.
        J Am Geriatr Soc. 2013; 61: 1863-1871
        • Beasley J.M.
        • Shikany J.M.
        • Thomson C.A.
        The role of dietary protein intake in the prevention of sarcopenia of aging.
        Nutr Clin Pract. 2013; 28: 684-690
      3. STATA (for Macintosh) [computer program]. Release 14. College Station, TX: StataCorp LP; 2015.

        • Jackson A.S.
        • Pollock M.L.
        Factor analysis and multivariate scaling of anthropometric variables for the assessment of body composition.
        Med Sci Sports. 1976; 8: 196-203
        • Katsanos C.S.
        • Kobayashi H.
        • Sheffield-Moore M.
        • Aarsland A.
        • Wolfe R.R.
        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. 2006; 291: E381-E387
        • Allison D.B.
        • Zannolli R.
        • Faith M.S.
        • et al.
        Weight loss increases and fat loss decreases all-cause mortality rate: Results from two independent cohort studies.
        Int J Obes Relat Metab Disord. 1999; 23: 603-611
        • De Schutter A.
        • Lavie C.J.
        • Kachur S.
        • Patel D.A.
        • Milani R.V.
        Body composition and mortality in a large cohort with preserved ejection fraction: Untangling the obesity paradox.
        Mayo Clin Proc. 2014; 89: 1072-1079
        • Oreopoulos A.
        • Kalantar-Zadeh K.
        • Sharma A.M.
        • Fonarow G.C.
        The obesity paradox in the elderly: Potential mechanisms and clinical implications.
        Clin Geriatr Med. 2009; 25 (viii): 643-659
        • Bea J.W.
        • Thomson C.A.
        • Wertheim B.C.
        • et al.
        Risk of mortality according to body mass index and body composition among postmenopausal women.
        Am J Epidemiol. 2015; 182: 585-596
        • Vellas B.J.
        • Hunt W.C.
        • Romero L.J.
        • Koehler K.M.
        • Baumgartner R.N.
        • Garry P.J.
        Changes in nutritional status and patterns of morbidity among free-living elderly persons: A 10-year longitudinal study.
        Nutrition. 1997; 13: 515-519
        • Beasley J.M.
        • LaCroix A.Z.
        • Neuhouser M.L.
        • et al.
        Protein intake and incident frailty in the Women's Health Initiative observational study.
        J Am Geriatr Soc. 2010; 58: 1063-1071
        • Prentice R.L.
        • Huang Y.
        • Kuller L.H.
        • et al.
        Biomarker-calibrated energy and protein consumption and cardiovascular disease risk among postmenopausal women.
        Epidemiology. 2011; 22: 170-179
        • Lagiou P.
        • Sandin S.
        • Lof M.
        • Trichopoulos D.
        • Adami H.O.
        • Weiderpass E.
        Low carbohydrate-high protein diet and incidence of cardiovascular diseases in Swedish women: Prospective cohort study.
        BMJ. 2012; 344: e4026
        • Trichopoulou A.
        • Psaltopoulou T.
        • Orfanos P.
        • Hsieh C.C.
        • Trichopoulos D.
        Low-carbohydrate-high-protein diet and long-term survival in a general population cohort.
        Eur J Clin Nutr. 2007; 61: 575-581
        • Sjogren P.
        • Becker W.
        • Warensjo E.
        • et al.
        Mediterranean and carbohydrate-restricted diets and mortality among elderly men: A cohort study in Sweden.
        Am J Clin Nutr. 2010; 92: 967-974
        • Hu F.B.
        • Stampfer M.J.
        • Manson J.E.
        • et al.
        Dietary protein and risk of ischemic heart disease in women.
        Am J Clin Nutr. 1999; 70: 221-227
        • Tinker L.F.
        • Sarto G.E.
        • Howard B.V.
        • et al.
        Biomarker-calibrated dietary energy and protein intake associations with diabetes risk among postmenopausal women from the Women's Health Initiative.
        Am J Clin Nutr. 2011; 94: 1600-1606
        • Sluijs I.
        • Beulens J.W.
        • van der A DL
        • Spijkerman A.M.
        • Grobbee D.E.
        • van der Schouw Y.T.
        Dietary intake of total, animal, and vegetable protein and risk of type 2 diabetes in the European Prospective Investigation into Cancer and Nutrition (EPIC)-NL study.
        Diabetes Care. 2010; 33: 43-48
        • Peterson M.D.
        • Sen A.
        • Gordon P.M.
        Influence of resistance exercise on lean body mass in aging adults: A meta-analysis.
        Med Sci Sports Exerc. 2011; 43: 249-258
        • Warburton D.E.
        • Nicol C.W.
        • Bredin S.S.
        Health benefits of physical activity: The evidence.
        CMAJ. 2006; 174: 801-809
      4. Zisser H, Gong P, Kelley CM, Seidman JS, Riddell MC. Exercise and diabetes. Int J Clin Pract Suppl. Feb(170):71-75.

        • Magne N.
        • Melis A.
        • Chargari C.
        • et al.
        Recommendations for a lifestyle which could prevent breast cancer and its relapse: Physical activity and dietetic aspects.
        Crit Rev Oncol Hematol. 2011; 80: 450-459
        • Gaesser G.A.
        • Angadi S.S.
        • Sawyer B.J.
        Exercise and diet, independent of weight loss, improve cardiometabolic risk profile in overweight and obese individuals.
        Phys Sportsmed. 2011; 39: 87-97
        • Rajarajeswaran P.
        • Vishnupriya R.
        Exercise in cancer.
        Indian J Med Paediatr Oncol. 2009; 30: 61-70
        • Rolland Y.M.
        • Perry 3rd, H.M.
        • Patrick P.
        • Banks W.A.
        • Morley J.E.
        Loss of appendicular muscle mass and loss of muscle strength in young postmenopausal women.
        J Gerontol A Biol Sci Med Sci. 2007; 62: 330-335
        • Gallagher D.
        • Heymsfield S.B.
        • Heo M.
        • Jebb S.A.
        • Murgatroyd P.R.
        • Sakamoto Y.
        Healthy percentage body fat ranges: An approach for developing guidelines based on body mass index.
        Am J Clin Nutr. 2000; 72: 694-701
        • Sahni S.
        • Mangano K.M.
        • Hannan M.T.
        • Kiel D.P.
        • McLean R.R.
        Higher protein intake is associated with higher lean mass and quadriceps muscle strength in adult men and women.
        J Nutr. 2015; 145: 1569-1575
        • Isanejad M.
        • Mursu J.
        • Sirola J.
        • et al.
        Association of protein intake with the change of lean mass among elderly women: The Osteoporosis Risk Factor and Prevention—Fracture Prevention Study (OSTPRE-FPS).
        J Nutr Sci. 2015; 4: e41
        • Van Der Ploeg G.E.
        • Withers R.T.
        • Laforgia J.
        Percent body fat via DEXA: Comparison with a four-compartment model.
        J Appl Physiol. 2003; 94: 499-506
        • Williams J.E.
        • Wells J.C.
        • Wilson C.M.
        • Haroun D.
        • Lucas A.
        • Fewtrell M.S.
        Evaluation of Lunar Prodigy dual-energy x-ray absorptiometry for assessing body composition in healthy persons and patients by comparison with the criterion 4-component model.
        Am J Clin Nutr. 2006; 83: 1047-1054
      5. US Department of Agriculture. Food composition databases. May 2016. http://ndb.nal.usda.gov/ndb/foods. Accessed June 30, 2016.

      Biography

      J. A. Martinez is an assistant research professor, Department of Nutritional Sciences, University of Arizona Cancer Center, University of Arizona, Tucson.

      Biography

      B. C. Wertheim is an assistant scientific investigator, University of Arizona Cancer Center, University of Arizona, Tucson.

      Biography

      C. A. Thomson is a professor, Mel & Enid Zuckerman College of Public Health, University of Arizona, Tucson.

      Biography

      Z. Chen is a professor and chair, Department of Epidemiology and Biostatistics, Mel & Enid Zuckerman College of Public Health, University of Arizona, Tucson.

      Biography

      J. W. Bea is an assistant professor, Department of Medicine, and assistant research scientist, Department of Nutritional Sciences, University of Arizona Cancer Center, University of Arizona, Tucson.

      Biography

      R. Wallace is a professor, Department of Epidemiology, University of Iowa, Iowa City.

      Biography

      L. Snetselaar is a professor, Department of Epidemiology, University of Iowa, Iowa City.

      Biography

      M. Allison is a professor, Department of Family Medicine and Public Health, University of California, San Diego.

      Biography

      R. Nassir is an assistant professor, Department of Biochemistry and Molecular Medicine, University of California, Davis.

      Biography

      P. A. Thompson is a professor, Department of Pathology, Stony Brook University, Stony Brook, NY.