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Female Sarcopenic Obesity

  • Fidel Hita-ContrerasEmail author
Chapter

Abstract

During the twentieth century, the overall life expectancy of the human population is rapidly increasing worldwide. The global share of older people (aged 60 years or over) increased from 9.2% in 1990 to 11.7% in 2013, and it is predicted that by 2050, it will reach 21.1% of the world population, with 392 million persons aged 80 years or over, more than three times the present [1]. Aging is associated with a progressive loss of tissue and organ function over time [2]. With aging, there is an increased risk of unfavorable changes in body composition, including a decrease in muscle and an increase in fat mass [3].

References

  1. 1.
    United Nations. World population ageing 2013 [Internet]. New York, USA: Department of Economic and Social Affairs, Population Division; 2013. Report No.: ST/ESA/SER.A/348. http://www.un.org/en/development/desa/population/publications/pdf/ageing/WorldPopulationAgeing2013.pdf.CrossRefGoogle Scholar
  2. 2.
    Flatt T. A new definition of aging? Front Genet. 2012;3:148.PubMedPubMedCentralCrossRefGoogle Scholar
  3. 3.
    Ding J, Kritchevsky SB, Newman AB, Taaffe DR, Nicklas BJ, Visser M, Lee JS, Nevitt M, Tylavsky FA, Rubin SM, Pahor M, Harris TB. Health ABC study, effects of birth cohort and age on body composition in a sample of community-based elderly. Am J Clin Nutr. 2007;85(2):405–10.PubMedCrossRefPubMedCentralGoogle Scholar
  4. 4.
    Frasca D, Blomberg BB, Paganelli R. Aging, obesity, and inflammatory age-related diseases. Front Immunol. 2017;8:1745.PubMedPubMedCentralCrossRefGoogle Scholar
  5. 5.
    Guh DP, Zhang W, Bansback N, Amarsi Z, Birmingham CL, Anis AH. The incidence of co-morbidities related to obesity and overweight: a systematic review and meta-analysis. BMC Public Health. 2009;9:88.PubMedPubMedCentralCrossRefGoogle Scholar
  6. 6.
    Zambon M, Mazzali G, Zoico E, Harris TB, Meigs JB, Di Francesco V, Fantin F, Bissoli L, Bosello O. Health consequences of obesity in the elderly: a review of four unresolved questions. Int J Obes. 2016;29:1011–29.CrossRefGoogle Scholar
  7. 7.
    Global Health Observatory (GHO) Obesity. Situation and trends. Geneva: World Health Organization; 2013.Google Scholar
  8. 8.
    Berdah J. Staying fit after fifty. Gynecol Obstet Fertil. 2006;34:920–6.PubMedCrossRefPubMedCentralGoogle Scholar
  9. 9.
    Davis SR, Lambrinoudaki I, Lumsden M, Mishra GD, Pal L, Rees M, Santoro N, Simoncini T. Menopause. Nat Rev Dis Primers. 2015;1:15004.CrossRefGoogle Scholar
  10. 10.
    Sternfeld B, Wang H, Quesenberry CP Jr, Abrams B, Everson-Rose SA, Greendale GA, Matthews KA, Torrens JI, Sowers M. Physical activity and changes in weight and waist circumference in midlife women: findings from the Study of Women’s Health Across the Nation. Am J Epidemiol. 2004;160:912e22.CrossRefGoogle Scholar
  11. 11.
    Lovejoy JC, Champagne CM, de Jonge L, Xie H, Smith SR. Increased visceral fat and decreased energy expenditure during the menopausal transition. Int J Obes. 2008;32:949–58.CrossRefGoogle Scholar
  12. 12.
    World Health Organization. Obesity: preventing and management of the global epidemic. Report of the WHO consultation. Technical report series. No. 894. Geneva: World Health Organization; 2000.Google Scholar
  13. 13.
    Rothman KJ. BMI-related errors in the measurement of obesity. Int J Obes. 2008;3(s3):s56–9.CrossRefGoogle Scholar
  14. 14.
    Hita-Contreras F. Traditional body mass index cut-offs in older people: time for a rethink with altered fat distribution, sarcopenia and shrinking height. Maturitas. 2018;113:A1–2.PubMedCrossRefPubMedCentralGoogle Scholar
  15. 15.
    Sorkin JD, Muller DC, Andres R. Longitudinal change in the heights of men and women: consequential effects on body mass index. Epidemiol Rev. 1999;21(2):247–60.PubMedCrossRefPubMedCentralGoogle Scholar
  16. 16.
    Alberti KG, Eckel RH, Grundy SM, Zimmet PZ, Cleeman JI, Donato KA, Fruchart JC, James WP, Loria CM, Smith SC Jr, International Diabetes Federation Task Force on Epidemiology and Prevention, National Heart, Lung, and Blood Institute; American Heart Association; World Heart Federation, International Atherosclerosis Society; International Association for the Study of Obesity. Harmonizing the metabolic syndrome: a joint interim statement of the International Diabetes Federation Task Force on Epidemiology and Prevention; National Heart, Lung, and Blood Institute; American Heart Association; World Heart Federation; International Atherosclerosis Society; and International Association for the Study of Obesity. Circulation. 2009;120:1640–5.CrossRefGoogle Scholar
  17. 17.
    Rollins KE, Javanmard-Emamghissi H, Awwad A, Macdonald IA, Fearon KCH, Lobo DN. Body composition measurement using computed tomography: does the phase of the scan matter? Nutrition. 2017;41:37–44.PubMedCrossRefPubMedCentralGoogle Scholar
  18. 18.
    Baumgartner RN, Wayne SJ, Waters DL, Janssen I, Gallagher D, Morley JE. Sarcopenic obesity predicts instrumental activities of daily living disability in the elderly. Obes Res. 2004;12:1995–2004.PubMedCrossRefPubMedCentralGoogle Scholar
  19. 19.
    Batsis JA, Mackenzie TA, Barre LK, Lopez-Jimenez F, Bartels SJ. Sarcopenia, sarcopenic obesity and mortality in older adults: results from the National Health and Nutrition Examination Survey III. Eur J Clin Nutr. 2014;68:1001–7.PubMedCrossRefPubMedCentralGoogle Scholar
  20. 20.
    Janssen I. Evolution of sarcopenia research. Appl Physiol Nutr Metab. 2010;35:707–12.PubMedCrossRefPubMedCentralGoogle Scholar
  21. 21.
    Curcio F, Ferro G, Basile C, Liguori I, Parrella P, Pirozzi F, Della-Morte D, Gargiulo G, Testa G, Tocchetti CG, Bonaduce D, Abete P. Biomarkers in sarcopenia: a multifactorial approach. Exp Gerontol. 2016;85:1–8.PubMedCrossRefPubMedCentralGoogle Scholar
  22. 22.
    Janssen I. The epidemiology of sarcopenia. Clin Geriatr Med. 2011;27:355–63.PubMedCrossRefPubMedCentralGoogle Scholar
  23. 23.
    Montero-Fernández N, Serra-Rexach JA. Role of exercise on sarcopenia in the elderly. Eur J Phys Rehabil Med. 2013;49:131.PubMedPubMedCentralGoogle Scholar
  24. 24.
    Rosenberg I. Summary comments: epidemiological and methodological problems in determining nutritional status of older persons. Am J Clin Nutr. 1989;50:1231–3.CrossRefGoogle Scholar
  25. 25.
    Morley JE, Baumgartner RN, Roubenoff R, Mayer J, Nair KS. Sarcopenia. J Lab Clin Med. 2001;137:231–43.PubMedCrossRefPubMedCentralGoogle Scholar
  26. 26.
    Baumgartner RN, Koehler KM, Gallagher D, Romero L, Heymsfield SB, Ross RR, Garry PJ, Lindeman RD. Epidemiology of sarcopenia among the elderly in New Mexico. Am J Epidemiol. 1998;147:755–63.PubMedPubMedCentralCrossRefGoogle Scholar
  27. 27.
    Janssen I, Heymsfield SB, Ross R. Low relative skeletal muscle mass (sarcopenia) in older persons is associated with functional impairment and physical disability. J Am Geriatr Soc. 2002;50:889–96.PubMedCrossRefPubMedCentralGoogle Scholar
  28. 28.
    Cruz-Jentoft AJ, Baeyens JP, Bauer JM, Boirie Y, Cederholm T, Landi F, Martin FC, Michel JP, Rolland Y, Schneider SM, Topinková E, Vandewoude M, Zamboni M. European working group on sarcopenia in older people, sarcopenia: European consensus on definition and diagnosis: report of the European Working group on sarcopenia in older people. Age Ageing. 2010;39(4):412–23.PubMedPubMedCentralCrossRefGoogle Scholar
  29. 29.
    Dam TT, Peters KW, Fragala M, Cawthon PM, Harris TB, McLean R, Shardell M, Alley DE, Kenny A, Ferrucci L, Guralnik J, Kiel DP, Kritchevsky S, Vassileva MT, Studenski S. An evidence-based comparison of operational criteria for the presence of sarcopenia. J Gerontol A Biol Sci Med Sci. 2014;69:584–90.PubMedPubMedCentralCrossRefGoogle Scholar
  30. 30.
    Fielding RA, Bruno V, Evans WJ, Bhasin S, Morley JE, Newman AB, Abellan van Kan G, Andrieu S, Bauer J, Breuille D, Cederholm T, Chandler J, De Meynard C, Donini L, Harris T, Kannt A, Keime Guibert F, Onder G, Papanicolaou D, Rolland Y, Rooks D, Sieber C, Souhami E, Verlaan S, Zamboni M. Sarcopenia: an undiagnosed condition in older adults. Current consensus definition: prevalence, etiology, and consequences. International working group on sarcopenia. J Am Med Dir Assoc. 2011;12:1–9.CrossRefGoogle Scholar
  31. 31.
    Morley JE, Abbatecola AM, Argiles JM, Baracos V, Bauer J, Bhasin S, Cederholm T, Coats AJ, Cummings SR, Evans WJ, Fearon K, Ferrucci L, Fielding RA, Guralnik JM, Harris TB, Inui A, Kalantar-Zadeh K, Kirwan BA, Mantovani G, Muscaritoli M, AB Newman F, Rosano GMR-F, Roubenoff R, Schambelan M, Sokol GH, Storer TW, Vellas B, von Haehling S, Yeh SS, Anker SD, Society on Sarcopenia, Cachexia and Wasting Disorders Trialist Workshop, Society on Sarcopenia, Cachexia and Wasting Disorders Trialist Workshop. Sarcopenia with limited mobility: an international consensus. J Am Med Dir Assoc. 2012;12:403–9.CrossRefGoogle Scholar
  32. 32.
    Muscaritoli M, Anker SD, Argiles J, Aversa Z, Bauer JM, Biolo G, Boirie Y, Bosaeus I, Cederholm T, Costelli P, Fearon KC, Laviano A, Maggio M, Fanelli FR, Schneider SM, Schols A, Sieber CC. Consensus definition of sarcopenia, cachexia and pre-cachexia: joint document elaborated by special interest groups (SIG) “cachexia-anorexia in chronic wasting diseases” and “nutrition in geriatrics”. Clin Nutr. 2010;29:154–9.PubMedCrossRefPubMedCentralGoogle Scholar
  33. 33.
    Cesari M, Fielding RA, Pahor M, Goodpaster B, Hellerstein M, van Kan GA, Anker SD, Rutkove S, Vrijbloed JW, Isaac M, Rolland Y, M’rini C, Aubertin-Leheudre M, Cedarbaum JM, Zamboni M, Sieber CC, Laurent D, Evans WJ, Roubenoff R, Morley JE, Vellas B, International Working Group on Sarcopenia, International Working Group on Sarcopenia. Biomarkers of sarcopenia in clinical trials-recommendations from the International Working Group on Sarcopenia. J Cachexia Sarcopenia Muscle. 2012;3:181–90.PubMedPubMedCentralCrossRefGoogle Scholar
  34. 34.
    Chien MY, Huang TY, Wu YT. Prevalence of sarcopenia estimated using a bioelectrical impedance analysis prediction equation in community-dwelling elderly people in Taiwan. J Am Geriatr Soc. 2008;56:1710–5.PubMedCrossRefPubMedCentralGoogle Scholar
  35. 35.
    Malafarina V, Uriz-Otano F, Iniesta R, Gil-Guerrero L. Sarcopenia in the elderly: diagnosis, physiopathology and treatment. Maturitas. 2012;71:109–14.PubMedCrossRefPubMedCentralGoogle Scholar
  36. 36.
    Kawakami R, Murakami H, Sanada K, Tanaka N, Sawada SS, Tabata I, Higuchi M, Miyachi M. Calf circumference as a surrogate marker of muscle mass for diagnosing sarcopenia in Japanese men and women. Geriatr Gerontol Int. 2015;15:969–76.PubMedCrossRefPubMedCentralGoogle Scholar
  37. 37.
    Laurentani F, Russo C, Bandinelli S, Bartali B, Cavazzini C, Di Iorio A, Corsi AM, Rantanen T, Guralnik JM, Ferrucci L. Age-associated changes in skeletal muscles and their effect on mobility: an operational diagnosis of sarcopenia. J Appl Physiol. 2003;95:1851–60.CrossRefGoogle Scholar
  38. 38.
    Peolsson A, Hedlund R, Oberg B. Intra- and inter-tester reliability and reference values for hand strength. J Rehabil Med. 2001;33:36–41.PubMedCrossRefPubMedCentralGoogle Scholar
  39. 39.
    Guralnik JM, Simonsick EM, Ferrucci L, Glynn RJ, Berkman LF, Blazer DG, Scherr PA, Wallace RB. A short physical performance battery assessing lower extremity function: association with self-reported dis-ability and prediction of mortality and nursing home admission. J Gerontol. 1994;49:M85–94.PubMedCrossRefPubMedCentralGoogle Scholar
  40. 40.
    Mathias S, Nayak US, Isaacs B. Balance in elderly patients: the get-up and go test. Arch Phys Med Rehabil. 1986;67:387–9.PubMedPubMedCentralGoogle Scholar
  41. 41.
    Baumgartner RN. Body composition in healthy aging. Ann N Y Acad Sci. 2000;904:437–48.PubMedCrossRefPubMedCentralGoogle Scholar
  42. 42.
    Molino S, Dossena M, Buonocore D, Verri M. Sarcopenic obesity: an appraisal of the current status of knowledge and management in elderly people. J Nutr Health Aging. 2016;20(7):780–8.PubMedCrossRefPubMedCentralGoogle Scholar
  43. 43.
    Kemmler W, Teschler M, Weißenfels A, Sieber C, Freiberger E, von Stengel S. Prevalence of sarcopenia and sarcopenic obesity in older German men using recognized definitions: high accordance but low overlap! Osteoporos Int. 2017;28:1881–91.PubMedCrossRefPubMedCentralGoogle Scholar
  44. 44.
    Han TS, Tajar A, Lean MEJ. Obesity and weight management in the elderly. Br Med Bull. 2011;97:169–96.PubMedCrossRefPubMedCentralGoogle Scholar
  45. 45.
    Newman AB, Kupelian V, Visser M, Simonsick E, Goodpaster B, Nevitt M, Kritchevsky SB, Tylavsky FA, Rubin SM, Harris TB, Health ABC Study Investigators. Sarcopenia: alternative definitions and associations with lower extremity function. J Am Geriatr Soc. 2003;51:1602–9.PubMedCrossRefPubMedCentralGoogle Scholar
  46. 46.
    Batsis JA, Mackenzie TA, Lopez-Jimenez F, Bartels SJ. Sarcopenia, sarcopenic obesity, and functional impairments in older adults: National Health and Nutrition Examination Surveys 1999–2004. Nutr Res. 2015;35:1031–9.PubMedPubMedCentralCrossRefGoogle Scholar
  47. 47.
    Bouchard DR, Dionne IJ, Brochu M. Sarcopenic/obesity and physical capacity in older men and women: data from the nutrition as a determinant of successful aging (NuAge)-the Quebec longitudinal study. Obesity (Silver Spring). 2009;17:2082–8.CrossRefGoogle Scholar
  48. 48.
    Oh C, Jho S, No J-K, Kim H-S. Body composition changes were related to nutrient intakes in elderly men but elderly women had a higher prevalence of sarcopenic obesity in a population of Korean adults. Nutr Res. 2015;35:1–6.PubMedCrossRefPubMedCentralGoogle Scholar
  49. 49.
    Öztürk ZA, Türkbeyler İH, Abiyev A, Kul S, Edizer B, Yakaryılmaz FD, Soylu G. Health related quality of life and fall risk associated with age related body composition changes; sarcopenia, obesity and sarcopenic obesity. Intern Med J. 2018;48(8):973–81.PubMedCrossRefPubMedCentralGoogle Scholar
  50. 50.
    Moreira MA, Zunzunegui MV, Vafaei A, da Câmara SM, Oliveira TS, Maciel ÁC. Sarcopenic obesity and physical performance in middle aged women: a cross-sectional study in Northeast Brazil. BMC Public Health. 2016;16:43.PubMedPubMedCentralCrossRefGoogle Scholar
  51. 51.
    Prado CMM, Wells JCK, Smith SR, Stephan BCM, Siervo M. Sarcopenic obesity: a critical appraisal of the current evidence. Clin Nutr. 2012;31:583–601.PubMedCrossRefPubMedCentralGoogle Scholar
  52. 52.
    Delmonico MJ, Harris TB, Visser M, Park SW, Conroy MB, Velasquez-Mieyer P, Boudreau R, Manini TM, Nevitt M, Newman AB, Goodpaster BH, Health, Aging, and Body. Longitudinal study of muscle strength, quality, and adipose tissue infiltration. Am J Clin Nutr. 2009;90:1579–85.PubMedPubMedCentralCrossRefGoogle Scholar
  53. 53.
    Grant RW, Dixit VD. Adipose tissue as an immunological organ. Obesity (Silver Spring). 2015;23:512–8.CrossRefGoogle Scholar
  54. 54.
    Guillet C, Boirie Y. Insulin resistance: a contributing factor to age-related muscle mass loss? Diabetes Metab. 2005;2:5S20–6.Google Scholar
  55. 55.
    Woodrow G. Body composition analysis techniques in the aged adult: indications and limitations. Curr Opin Clin Nutr Metab Care. 2009;12:8–14.PubMedCrossRefPubMedCentralGoogle Scholar
  56. 56.
    Biener A, Cawley J, Meyerhoefer C. The impact of obesity on medical care costs and labor market outcomes in the US. Clin Chem. 2018;64(1):108–17.PubMedCrossRefPubMedCentralGoogle Scholar
  57. 57.
    Kim J, Cho JJ, Park YS. Relationship between sarcopenic obesity and cardiovascular disease risk as estimated by the Framingham risk score. J Korean Med Sci. 2015;30:264–71.PubMedPubMedCentralCrossRefGoogle Scholar
  58. 58.
    Zhang H, Lin S, Gao T, Zhong F, Cai J, Sun Y, Ma A. Association between sarcopenia and metabolic syndrome in middle-aged and older non-obese adults: a systematic review and meta-analysis. Nutrients. 2018;10:E364.PubMedCrossRefPubMedCentralGoogle Scholar
  59. 59.
    Janssen I, Shepard DS, Katzmarzyk PT, Roubenoff R. The healthcare costs of sarcopenia in the United States. J Am Geriatr Soc. 2004;52:80–5.PubMedPubMedCentralCrossRefGoogle Scholar
  60. 60.
    Vincent HK, Vincent KR, Lamb KM. Obesity and mobility disability in the older adult. Obes Rev. 2010;11:568–79.PubMedCrossRefPubMedCentralGoogle Scholar
  61. 61.
    Lim S, Kim JH, Yoon JW, Kang SM, Choi SH, Park YJ, Kim KW, Lim JY, Park KS, Jang HC. Sarcopenic obesity: prevalence and association with metabolic syndrome in the Korean longitudinal study on health and aging (KLo-SHA). Diabetes Care. 2010;33:1652–4.PubMedPubMedCentralCrossRefGoogle Scholar
  62. 62.
    dos Santos EP, Gadelha AB, Safons MP, Nobrega OT, Oliveira RJ, Lima RM. Sarcopenia and sarcopenic obesity classifications and cardiometabolic risks in older women. Arch Gerontol Geriatr. 2014;59:56–61.PubMedCrossRefPubMedCentralGoogle Scholar
  63. 63.
    Aibar-Almazán A, Martínez-Amat A, Cruz-Díaz D, Jiménez-García JD, Achalandabaso A, Sánchez-Montesinos I, de la Torre-Cruz MM, Hita-Contreras F. Sarcopenia and sarcopenic obesity in Spanish community-dwelling middle-aged and older women: association with balance confidence, fear of falling and fall risk. Maturitas. 2018;107:26–32.PubMedCrossRefPubMedCentralGoogle Scholar
  64. 64.
    Janssen I, Katzmarzyk PT, Ross R. Body mass index is inversely related to mortality in older people after adjustment for waist circumference. J Am Geriatr Soc. 2005;53:2112–8.PubMedCrossRefPubMedCentralGoogle Scholar
  65. 65.
    Lang T, Streeper T, Cawthon P, Baldwin K, Taaffe DR, Harris TB. Sarcopenia: etiology, clinical consequences, intervention, and assessment. Osteoporos Int. 2010;21:543–59.PubMedCrossRefPubMedCentralGoogle Scholar
  66. 66.
    Tian S, Xu Y. Association of sarcopenic obesity with the risk of all-cause mortality: a meta-analysis of prospective cohort studies. Geriatr Gerontol Int. 2016;16:155–66.PubMedCrossRefPubMedCentralGoogle Scholar
  67. 67.
    Trouwborst I, Verreijen A, Memelink R, Massanet P, Boirie Y, Weijs P, Tieland M. Exercise and nutrition strategies to counteract sarcopenic obesity. Nutrients. 2018;10:E605.PubMedPubMedCentralCrossRefGoogle Scholar
  68. 68.
    Hita-Contreras F, Martínez-Amat A, Cruz-Díaz D, Pérez-López FR. Osteosarcopenic obesity and fall prevention strategies. Maturitas. 2015;80(2):126–32.PubMedCrossRefPubMedCentralGoogle Scholar
  69. 69.
    Poirier P, Giles TD, Bray GA, Hong Y, Stern JS, Pi-Sunyer FX, Eckel RH. Obesity and cardiovascular disease: pathophysiology, evaluation, and effect of weight loss: an update of the 1997 American Heart Association Scientific Statement on Obesity and Heart Disease from the Obesity Committee of the Council on Nutrition, Physical Activity and Metabolism. Circulation. 2006;113:898–918.PubMedCrossRefPubMedCentralGoogle Scholar
  70. 70.
    Li Z, Heber D. Sarcopenic obesity in the elderly and strategies for weight management. Nutr Rev. 2012;70:57–64.PubMedCrossRefPubMedCentralGoogle Scholar
  71. 71.
    Maltais ML, Perreault K, Courchesne-Loyer A, Lagacé JC, Barsalani R, Dionne IJ. Effect of resistance training and various sources of protein supplementation on body fat mass and metabolic profile in Sarcopenic overweight older adult men: a pilot study. Int J Sport Nutr Exerc Metab. 2016;26:71–7.PubMedCrossRefPubMedCentralGoogle Scholar
  72. 72.
    Mendoza N, De Teresa C, Cano A, Godoy D, Hita-Contreras F, Lapotka M, Llaneza P, Manonelles P, Martínez-Amat A, Ocón O, Rodríguez-Alcalá L, Vélez M, Sánchez-Borrego R. Benefits of physical exercise in postmenopausal women. Maturitas. 2016;93:83–8.PubMedCrossRefPubMedCentralGoogle Scholar
  73. 73.
    Naseeb MA, Volpe SL. Protein and exercise in the prevention of sarcopenia and aging. Nutr Res. 2017;40:1–20.PubMedCrossRefPubMedCentralGoogle Scholar
  74. 74.
    Sgrò P, Sansone M, Sansone A, Sabatini S, Borrione P, Romanelli F, Di Luigi L. Physical exercise, nutrition and hormones: three pillars to fight sarcopenia. Aging Male. 2019;22(2):75–88.PubMedCrossRefPubMedCentralGoogle Scholar
  75. 75.
    Brioche T, Kireev RA, Cuesta S, Gratas-Delamarche A, Tresguerres JA, Gomez-Cabrera MC, Viña J. Growth hormone replacement therapy prevents sarcopenia by a dual mechanism: improvement of protein balance and of antioxidant defences. J Gerontol A Biol Sci Med Sci. 2014;69:1186–98.PubMedCrossRefPubMedCentralGoogle Scholar
  76. 76.
    Brent MB, Brüel A, Thomsen JS. PTH (1-34) and growth hormone in prevention of disuse osteopenia and sarcopenia in rats. Bone. 2018;110:244–53.PubMedCrossRefPubMedCentralGoogle Scholar
  77. 77.
    Crane JD, Macneil LG, Tarnopolsky MA. Long-term aerobic exercise is associated with greater muscle strength throughout the life span. J Gerontol A Biol Sci Med Sci. 2013;68:631–8.PubMedCrossRefPubMedCentralGoogle Scholar
  78. 78.
    Zampieri S, Pietrangelo L, Loefler S, Fruhmann H, Vogelauer M, Burggraf S, Pond A, Grim-Stieger M, Cvecka J, Sedliak M, Tirpáková V, Mayr W, Sarabon N, Rossini K, Barberi L, De Rossi M, Romanello V, Boncompagni S, Musarò A, Sandri M, Protasi F, Carraro U, Kern H. Lifelong physical exercise delays age associated skeletal muscle decline. J Gerontol A Biol Sci Med Sci. 2015;70:163–73.PubMedCrossRefPubMedCentralGoogle Scholar
  79. 79.
    Nilwik R, Snijders T, Leenders M, Groen BB, van Kranenburg J, Verdijk LB, van Loon LJ. The decline in skeletal muscle mass with aging is mainly attributed to a reduction in type II muscle fiber size. Exp Gerontol. 2013;48:492–8.PubMedCrossRefPubMedCentralGoogle Scholar
  80. 80.
    Donges CE, Duffield R, Drinkwater EJ. Effects of resistance or aerobic exercise training on interleukin-6, C-reactive protein, and body composition. Med Sci Sports Exerc. 2010;42:304–13.PubMedCrossRefPubMedCentralGoogle Scholar
  81. 81.
    Peterson MD, Sen A, Gordon PM. Influence of resistance exercise on lean body mass in aging adults: a meta-analysis. Med Sci Sports Exerc. 2011;43(2):249–58.PubMedPubMedCentralCrossRefGoogle Scholar
  82. 82.
    Liu CJ, Chang WP, Araujo de Carvalho I, Savage KEL, Radford LW, Amuthavalli Thiyagarajan J. Effects of physical exercise in older adults with reduced physical capacity: meta-analysis of resistance exercise and multimodal exercise. Int J Rehabil Res. 2017;40:303–14.PubMedCrossRefPubMedCentralGoogle Scholar
  83. 83.
    Gadelha AB, Paiva FM, Gauche R, De Oliveira RJ, Lima RM. Effects of resistance training on sarcopenic obesity index in older women: a randomized controlled trial. Arch Gerontol Geriatr. 2016;65:168–73.PubMedCrossRefPubMedCentralGoogle Scholar
  84. 84.
    Park J, Kwon Y, Park H. Effects of 24-week aerobic and resistance training on carotid artery intima-media thickness and flow velocity in elderly women with sarcopenic obesity. J Atheroscler Thromb. 2017;24(11):1117–24.PubMedPubMedCentralCrossRefGoogle Scholar
  85. 85.
    Chen HT, Chung YC, Chen YJ, Ho SY, Wu HJ. Effects of different types of exercise on body composition, muscle strength, and IGF-1 in the elderly with sarcopenic obesity. J Am Geriatr Soc. 2017;65(4):827–32.PubMedCrossRefPubMedCentralGoogle Scholar
  86. 86.
    Martínez-Amat A, Aibar-Almazán A, Fábrega-Cuadros R, Cruz-Díaz D, Jiménez-García JD, Pérez-López FR, Achalandabaso A, Barranco-Zafra R, Hita-Contreras F. Exercise alone or combined with dietary supplements for sarcopenic obesity in community-dwelling older people: a systematic review of randomized controlled trials. Maturitas. 2018;110:92–103.PubMedCrossRefPubMedCentralGoogle Scholar
  87. 87.
    Natsume T, Ozaki H, Kakigi R, Kobayashi H, Naito H. Effects of training intensity in electromyostimulation on human skeletal muscle. Eur J Appl Physiol. 2018;118:1339–47.PubMedCrossRefPubMedCentralGoogle Scholar
  88. 88.
    Filipovic A, Grau M, Kleinöder H, Zimmer P, Hollmann W, Bloch W. Effects of a whole-body electrostimulation program on strength, sprinting, jumping, and kicking capacity in elite soccer players. J Sports Sci Med. 2016;15:639–48.PubMedPubMedCentralGoogle Scholar
  89. 89.
    Kemmler W, Schliffka R, Mayhew JL, von Stengel S. Effects of whole-body electromyostimulation on resting metabolic rate, body composition, and maximum strength in postmenopausal women: the training and electrostimulation trial. J Strength Cond Res. 2010;4:1880–7.CrossRefGoogle Scholar
  90. 90.
    Kemmler W, Teschler M, Weissenfels A, Bebenek M, Fröhlich M, Kohl M, von Stengel S. Effects of whole-body electromyostimulation versus high intensity resistance exercise on body composition and strength: a randomized controlled study. Evid Based Complement Alternat Med. 2016;2016:9236809.PubMedPubMedCentralCrossRefGoogle Scholar
  91. 91.
    Stenholm S, Harris TB, Rantanen T, Visser M, Kritchevsky SB, Ferrucci L. Sarcopenic obesity: definition, cause and consequences. Curr Opin Clin Nutr Metab Care. 2008;11:693–700.PubMedPubMedCentralCrossRefGoogle Scholar
  92. 92.
    Malafarina V, Uriz-Otano F, Iniesta R, Gil-Guerrero L. Effectiveness of nutritional supplementation on muscle mass in treatment of sarcopenia in old age: a systematic review. J Am Med Dir Assoc. 2013;14:10–7.PubMedCrossRefPubMedCentralGoogle Scholar
  93. 93.
    Bauer J, Biolo G, Cederholm T, Cesari M, Cruz-Jentoft AJ, Morley JE, Phillips S, Sieber C, Stehle P, Teta D, Visvanathan R, Volpi E, Boirie Y. 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. 2013;14:542–59.PubMedCrossRefPubMedCentralGoogle Scholar
  94. 94.
    Wolfe RR, Miller SL, Miller KB. Optimal protein intake in the elderly. Clin Nutr. 2008;27:675–84.PubMedCrossRefPubMedCentralGoogle Scholar
  95. 95.
    Levine ME, Suarez JA, Brandhorst S, Balasubramanian P, Cheng CW, Madia F, Fontana L, Mirisola MG, Guevara-Aguirre J, Wan J, Wan J, Passarino G, Kennedy BK, Wei M, Cohen P, Crimmins EM, Longo VD. Low protein intake is associated with a major reduction in IGF-1, cancer, and overall mortality in the 65 and younger but not older population. Cell Metab. 2014;19:407–17.PubMedPubMedCentralCrossRefGoogle Scholar
  96. 96.
    Hayes A, Cribb PJ. Effect of whey protein isolate on strength, body composition and muscle hypertrophy during resistance training. Curr Opin Clin Nutr Metab Care. 2008;11:40–4.PubMedCrossRefPubMedCentralGoogle Scholar
  97. 97.
    Antonione R, Caliandro E, Zorat F, Guarnieri G, Heer M, Biolo G. Whey protein ingestion enhances postprandial anabolism during short-term bed rest in young men. J Nutr. 2008;138:2212–6.PubMedCrossRefPubMedCentralGoogle Scholar
  98. 98.
    Katsanos CS, Chinkes DL, Paddon-Jones D, Zhang X, Aarsland A, Wolfe RR. Whey protein ingestion in elderly results in greater muscle protein accrual than ingestion of its constituent essential amino acid content. Nutr Res. 2008;28:651–8.PubMedPubMedCentralCrossRefGoogle Scholar
  99. 99.
    Wall BT, Hamer HM, de Lange A, Kiskini A, Groen BB, Senden JM, Gijsen AP, Verdijk, van Loon LJ. Leucine co-ingestion improves post-prandial muscle protein accretion in elderly men. Clin Nutr (Edinburgh, Scotland). 2013;32:412–9.CrossRefGoogle Scholar
  100. 100.
    J. Cruz-Jentoft A. Beta-hydroxy-beta-methyl butyrate (HMB): from experimental data to clinical evidence in sarcopenia. Curr Protein Pept Sci. 2018;19:668–72.CrossRefGoogle Scholar
  101. 101.
    Lucotti P, Setola E, Monti LD, Galluccio E, Costa S, Sandoli EP, Fermo I, Rabaiotti G, Gatti R, Piatti P. Beneficial effects of a long-term oral L-arginine treatment added to a hypocaloric diet and exercise training program in obese, insulin-resistant type 2 diabetic patients. Am J Physiol Endocrinol Metab. 2006;291:906–12.CrossRefGoogle Scholar
  102. 102.
    Jain SK, Micinski D, Huning L, Kahlon G, Bass PF, Levine SN. Vitamin D and L-cysteine levels correlate positively with GSH and negatively with insulin resistance levels in the blood of type 2 diabetic patients. Eur J Clin Nutr. 2014;68:1148–53.PubMedPubMedCentralCrossRefGoogle Scholar
  103. 103.
    Van Vliet S, Burd NA, van Loon LJ. The skeletal muscle anabolic response to plant- versus animal-based protein consumption. J Nutr. 2015;145:1981–91.PubMedCrossRefPubMedCentralGoogle Scholar
  104. 104.
    Cardon-Thomas DK, Riviere T, Tieges Z, Greig CA. Dietary protein in older adults: adequate daily intake but potential for improved distribution. Nutrients. 2017;9:E184.PubMedCrossRefPubMedCentralGoogle Scholar
  105. 105.
    Farsijani S, Morais JA, Payette H, Gaudreau P, Shatenstein B, Gray-Donald K, Chevalier S. Relation between mealtime distribution of protein intake and lean mass loss in free-living older adults of the NuAge study. Am J Clin Nutr. 2016;104:694–703.PubMedCrossRefPubMedCentralGoogle Scholar
  106. 106.
    Farnsworth E, Luscombe ND, Noakes M, Wittert G, Argyiou E, Clifton PM. Effect of a high-protein, energy-restricted diet on body composition, glycemic control, and lipid concentrations in overweight and obese hyperinsulinemic men and women. Am J Clin Nutr. 2003;78:31–9.PubMedCrossRefPubMedCentralGoogle Scholar
  107. 107.
    Weigle DS, Breen PA, Matthys CC, Callahan HS, Meeuws KE, Burden VR, Purnell JQ. A high-protein diet induces sustained reductions in appetite, ad libitum caloric intake, and body weight despite compensatory changes in diurnal plasma leptin and ghrelin concentrations. Am J Clin Nutr. 2005;82:41–8.PubMedCrossRefPubMedCentralGoogle Scholar
  108. 108.
    Coker RH, Miller S, Schutzler S, Deutz N, Wolfe RR. Whey protein and essential amino acids promote the reduction of adipose tissue and increased muscle protein synthesis during caloric restriction-induced weight loss in elderly, obese individuals. Nutr J. 2012;11:105.PubMedPubMedCentralCrossRefGoogle Scholar
  109. 109.
    Chanet A, Verlaan S, Salles J, Giraudet C, Patrac V, Pidou V, Pouyet C, Hafnaoui N, Blot A, Cano N, Farigon N, Bongers A, Jourdan M, Luiking Y, Walrand S, Boirie Y. Supplementing breakfast with a vitamin D and leucine-enriched whey protein medical nutrition drink enhances postprandial muscle protein synthesis and muscle mass in healthy older men. J Nutr. 2017;147:2262–71.PubMedCrossRefPubMedCentralGoogle Scholar
  110. 110.
    Damms-Machado A, Weser G, Bischoff SC. Micronutrient deficiency in obese subjects undergoing low calorie diet. Nutr J. 2012;11:34.PubMedPubMedCentralCrossRefGoogle Scholar
  111. 111.
    Van Dronkelaar C, van Velzen A, Abdelrazek M, van der Steen A, Weijs PJM, Tieland M. Minerals and sarcopenia; the role of calcium, iron, magnesium, phosphorus, potassium, selenium, sodium, and zinc on muscle mass, muscle strength, and physical performance in older adults: a systematic review. J Am Med Dir Assoc. 2017;19:6–11.e3.PubMedCrossRefPubMedCentralGoogle Scholar
  112. 112.
    Scott D, Blizzard L, Fell J, Ding C, Winzenberg T, Jones GA. Prospective study of the associations between 25-hydroxy-vitamin D, sarcopenia progression and physical activity in older adults. Clin Endocrinol (Oxf). 2010;73:581–7.CrossRefGoogle Scholar
  113. 113.
    Muir SW, Montero-Odasso M. Effect of vitamin D supplementation on muscle strength, gait and balance in older adults: a systematic review and meta-analysis. J Am Geriatr Soc. 2011;59:2291–300.PubMedCrossRefPubMedCentralGoogle Scholar
  114. 114.
    Weinheimer EM, Sands LP, Campbell WW. A systematic review of the separate and combined effects of energy restriction and exercise on fat-free mass in middle-aged and older adults: implications for sarcopenic obesity. Nutr Rev. 2010;68:375–88.PubMedCrossRefPubMedCentralGoogle Scholar
  115. 115.
    Villareal D, Aguirre L, Gurney B, Waters D, Colombo E, Armamento-Villareal R, Qualls C. Aerobic or resistance exercise, or both, in dieting obese older adults. N Engl J Med. 2017;376:1943–55.PubMedPubMedCentralCrossRefGoogle Scholar
  116. 116.
    Liao CD, Tsauo JY, Wu YT, Cheng CP, Chen HC, Huang YC, Chen HC, Liou TH. Effects of protein supplementation combined with resistance exercise on body composition and physical function in older adults: a systematic review and meta-analysis. Am J Clin Nutr. 2017;106:1078–91.PubMedCrossRefPubMedCentralGoogle Scholar
  117. 117.
    Hita-Contreras F, Bueno-Notivol J, Martínez-Amat A, Cruz-Díaz D, Hernandez AV, Pérez-López FR. Effect of exercise alone or combined with dietary supplements on anthropometric and physical function measures in community-dwelling elderly people with sarcopenic obesity: a meta-analysis of randomized controlled trials. Maturitas. 2018;116:24–35.PubMedCrossRefPubMedCentralGoogle Scholar
  118. 118.
    Kim H, Kim M, Kojima N, Fujino K, Hosoi E, Kobayashi H, Somekawa S, Niki Y, Yamashiro Y, Yoshida H. Exercise and nutritional supplementation on community dwelling elderly japanese women with sarcopenic obesity: a randomized controlled trial. J Am Med Dir Assoc. 2016;17(11):1011–9.PubMedCrossRefPubMedCentralGoogle Scholar
  119. 119.
    Wittmann K, Sieber C, von Stengel S, Kohl M, Freiberger E, Jakob F, Lell M, Engelke K, Kemmler W. Impact of whole body electromyostimulation on cardiometabolic risk factors in older women with sarcopenic obesity: the randomized controlled FORMOsA-sarcopenic obesity study. Clin Interv Aging. 2016;11:1697–706.PubMedPubMedCentralCrossRefGoogle Scholar
  120. 120.
    Kemmler, Weissenfels A, Teschler M, Willert S, Bebenek M, Shojaa M, Kohl M, Freiberger E, Sieber C, Von Stengel S. Whole-body electromyostimulation and protein supplementation favorably affect sarcopenic obesity in community dwelling older men at risk: the randomized controlled FranSO study. Clin Interv Aging. 2017;12:1503–13.PubMedPubMedCentralCrossRefGoogle Scholar
  121. 121.
    Kemmler W, Grimm A, Bebenek M, Kohl M, von Stengel S. Effects of combined whole-body electromyostimulation and protein supplementation on local and overall muscle/fat distribution in older men with sarcopenic obesity: the randomized controlled franconia sarcopenic obesity (FranSO) study. Calcif Tissue Int. 2018;103(3):266–77.PubMedCrossRefPubMedCentralGoogle Scholar

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© Springer Nature Switzerland AG 2019

Authors and Affiliations

  1. 1.Department of Health Sciences, Faculty of Health SciencesUniversity of JaénJaénSpain

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