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Int J Sports Med 2020; 41(14): 1067-1076
DOI: 10.1055/a-1202-1663
Clinical Sciences

Indicators of Sarcopenia: Sex Differences in Competitive Runners Prior to Peak Muscle Mass

Todd C. Shoepe 
1   Health and Human Sciences, Loyola Marymount University Frank R Seaver College of Science and Engineering, Los Angeles, United States
,
William P. McCormack
1   Health and Human Sciences, Loyola Marymount University Frank R Seaver College of Science and Engineering, Los Angeles, United States
,
Joseph W. LaBrie
2   Health and Human Sciences, Loyola Marymount University, Los Angeles, United States
,
Grant T. Mello
1   Health and Human Sciences, Loyola Marymount University Frank R Seaver College of Science and Engineering, Los Angeles, United States
,
Hawley C. Almstedt
1   Health and Human Sciences, Loyola Marymount University Frank R Seaver College of Science and Engineering, Los Angeles, United States
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Abstract

Strength, muscle mass, and muscle quality have been observed to be compromised in low body-mass index individuals such as competitive runners, increasing their risk for sarcopenia. The purpose was to compare indices of sarcopenia in young runners to age, height, body-mass, and body-mass index-matched non-runners. Handgrip strength and arm composition from dual-energy x-ray absorptiometry (baseline-T1, T2=5.3±1.4, T3=11.5±0.7 months later) were assessed in 40 non-runners and 40 runners (19.3±0.7 vs. 19.2±1.1 years, 170.7±10.3 vs. 171.1±9.1 cm, 60.2±7.4 vs. 60.2±7.9 kg, 20.6±0.9 vs. 20.5±1.5 kg m-2). The unitless variable of muscle quality, was defined as the sum of right and left maximal handgrip (in kg) divided by the sum of bone-free lean mass of both arms (in kg). Female runners displayed the highest muscle quality (T1=15.3±1.7; T3=15.7±2.0) compared to male runners (T1=13.7±1.4, p < 0.001; T3=14.2±1.6, p < 0.001) and male non-runners (T1=12.4±1.8, p=0.001; T3=13.2±1.6, p < 0.001), while female non-runners (T1=14.6±2.5, p=0.154; T3=15.1 ±2.2, p=0.124) showed higher muscle quality than male non-runners. Higher muscle quality in low-body-mass index females persists over one-year during young-adulthood and while running contributes to whole-body muscle mass accrual, it does not appear to be significantly associated with improvements in the most commonly used upper-body diagnostic indicator of sarcopenia.

Key words

handgrip - strength - dynapenia - development - bone-free lean mass


Publication History

Received: 20 December 2019

Accepted: 09 June 2020

Article published online:
28 July 2020

© 2020. Thieme. All rights reserved.

Georg Thieme Verlag KG
Rüdigerstraße 14, 70469 Stuttgart, Germany

 

  • References

  • 1 Beaudart C, Rizzoli R, Bruyère O. et al. Sarcopenia: Burden and challenges for public health. Arch Public Health 2014; 72: 45
    CrossrefPubMedSearch in Google Scholar
  • 2 Cruz-Jentoft AJ, Baeyens JP, Bauer JM. et al. Sarcopenia: European consensus on definition and diagnosis Report of the European Working Group on Sarcopenia in Older People. Age Ageing 2010; 39: 412-423
    CrossrefPubMedSearch in Google Scholar
  • 3 Cruz-Jentoft AJ, Bahat G, Bauer J. et al. Writing Group for the European Working Group on Sarcopenia in Older People 2 (EWGSOP2), and the Extended Group for EWGSOP2. Sarcopenia: Revised European consensus on definition and diagnosis. Age Ageing 2019; 48: 16-31
    CrossrefPubMedSearch in Google Scholar
  • 4 O’Brien TD, Reeves ND, Baltzopoulos V. et al. In vivo measurements of muscle specific tension in adults and children. Exp Physiol 2010; 95: 202-210
    CrossrefPubMedSearch in Google Scholar
  • 5 Goodpaster BH, Park SW, Harris TB. et al. The loss of skeletal muscle strength, mass, and quality in older adults: the health, aging and body composition study. J Gerontol A Biol Sci Med Sci 2006; 61: 1059-1064
    CrossrefPubMedSearch in Google Scholar
  • 6 Newman AB, Kupelian V, Visser M. et al. Strength, but not muscle mass, is associated with mortality in the health, aging and body composition study cohort. J Gerontol A Biol Sci Med Sci 2006; 61: 72-77
    CrossrefPubMedSearch in Google Scholar
  • 7 Hubal MJ, Gordish-Dressman H, Thompson PD. et al. Variability in muscle size and strength gain after unilateral resistance training. Med Sci Sports Exerc 2005; 37: 964-972
    PubMedSearch in Google Scholar
  • 8 Maughan R, Watson JS, Weir J. Relationships between muscle strength and muscle cross-sectional area in male sprinters and endurance runners. Eur J Appl Physiol Occup Physiol 1983; 50: 309-318
    CrossrefPubMedSearch in Google Scholar
  • 9 Pitcher CA, Elliott CM, Williams SA. et al. Childhood muscle morphology and strength: alterations over six months of growth. Muscle Nerve 2012; 46: 360-366
    CrossrefPubMedSearch in Google Scholar
  • 10 Dodds RM, Syddall HE, Cooper R. et al. Grip strength across the life course: Normative data from twelve British studies. PLoS One 2014; 9: e113637
    Search in Google Scholar
  • 11 Kanehisa H, Yata H, Ikegawa S. et al. A cross-sectional study of the size and strength of the lower leg muscles during growth. Eur J Appl Physiol Occup Physiol 1995; 72: 150-156
    CrossrefPubMedSearch in Google Scholar
  • 12 Miller AEJ, MacDougall J, Tarnopolsky M. et al. Gender differences in strength and muscle fiber characteristics. Eur J Appl Physiol Occup Physiol 1993; 66: 254-262
    CrossrefPubMedSearch in Google Scholar
  • 13 Maughan RJ, Watson JS, Weir J. Strength and cross-sectional area of human skeletal muscle. J Physiol 1983; 338: 37-49
    CrossrefPubMedSearch in Google Scholar
  • 14 Lexell J, Sjöström M, Nordlund AS. et al. Growth and development of human muscle: a quantitative morphological study of whole vastus lateralis from childhood to adult age. Muscle Nerve 1992; 15: 404-409
    CrossrefPubMedSearch in Google Scholar
  • 15 Faigenbaum A. Age-and sex-related differences and their implications for resistance exercise. In: Baechle T, Earle R, Hrsg. Essentials of Strength Training and Conditioning. 3. Aufl. Champaign, IL: Human Kinetics; 2000: 142-158
  • 16 Ichinose Y, Kanehisa H, Ito M. et al. Morphological and functional differences in the elbow extensor muscle between highly trained male and female athletes. Eur J Appl Physiol Occup Physiol 1998; 78: 109-114
    CrossrefPubMedSearch in Google Scholar
  • 17 Ivey F, Tracy B, Lemmer J. et al. Effects of strength training and detraining on muscle quality: Age and gender comparisons. J Gerontol A Biol Sci Med Sci 2000; 55: B152-B157
    CrossrefPubMedSearch in Google Scholar
  • 18 Anton MM, Spirduso WW, Tanaka H. Age-related declines in anaerobic muscular performance: weightlifting and powerlifting. Med Sci Sports Exerc 2004; 36: 143-147
    CrossrefPubMedSearch in Google Scholar
  • 19 Fabbri E, Chiles Shaffer N, Gonzalez-Freire M. et al. Early body composition, but not body mass, is associated with future accelerated decline in muscle quality. J Cachexia Sarcopenia Muscle 2017; 8: 490-499
    CrossrefPubMedSearch in Google Scholar
  • 20 Akima H, Kano Y, Enomoto Y. et al. Muscle function in 164 men and women aged 20--84 yr. Med Sci Sports Exerc 2001; 33: 220-226
    CrossrefPubMedSearch in Google Scholar
  • 21 Folland JP, Mc Cauley TM, Williams AG. Allometric scaling of strength measurements to body size. Eur J Appl Physiol 2008; 102: 739-745
    CrossrefPubMedSearch in Google Scholar
  • 22 LaBrie JW, Boyle S, Earle A. et al. Heavy episodic drinking is associated with poorer bone health in adolescent and young adult women. J Stud Alcohol Drugs 2018; 79: 391-398
    CrossrefPubMedSearch in Google Scholar
  • 23 Riebe D, Ehrman J, Ligouri G et al, Hrsg. ACSM Guidelines for Exercise Testing and Prescription. 10. Aufl. Philadelphia, PA: Wolters Kluwer; 2018
  • 24 Harriss D, MacSween A, Atkinson G. Ethical standards in sport and exercise science research: 2020 update. Int J Sports Med 2019; 40: 813-817
    Thieme ConnectPubMedSearch in Google Scholar
  • 25 Kutáč P, Bunc V, Sigmund M. Whole-body dual-energy X-ray absorptiometry demonstrates better reliability than segmental body composition analysis in college-aged students. PLoS One 2019; 14: e0215599
    CrossrefPubMedSearch in Google Scholar
  • 26 Balogun JA, Akomolafe CT, Amusa LO. Grip strength: Effects of testing posture and elbow position. Arch Phys Med Rehabil 1991; 72: 280-283
    PubMedSearch in Google Scholar
  • 27 Chen L-K, Liu L-K, Woo J. et al. Sarcopenia in Asia: consensus report of the Asian Working Group for Sarcopenia. J Am Med Dir Assoc 2014; 15: 95-101
    CrossrefPubMedSearch in Google Scholar
  • 28 Studenski SA, Peters KW, Alley DE. et al. The FNIH sarcopenia project: Rationale, study description, conference recommendations, and final estimates. J Gerontol A Biol Sci Med Sci 2014; 69: 547-558
    CrossrefPubMedSearch in Google Scholar
  • 29 Innes E. Handgrip strength testing: a review of the literature. Aust Occup Ther J 1999; 46: 120-140
    CrossrefPubMedSearch in Google Scholar
  • 30 Barbat-Artigas S, Rolland Y, Vellas B. et al. Muscle quantity is not synonymous with muscle quality. J Am Med Dir Assoc 2013; 14: 852.e1-852.e7
    CrossrefPubMedSearch in Google Scholar
  • 31 Gerodimos V, Karatrantou K, Dipla K. et al. Age-related differences in peak handgrip strength between wrestlers and nonathletes during the developmental years. J Strength Cond Res 2013; 27: 616-623
    CrossrefPubMedSearch in Google Scholar
  • 32 Wind AE, Takken T, Helders PJ. et al. Is grip strength a predictor for total muscle strength in healthy children, adolescents, and young adults?. Eur J Pediatr 2010; 169: 281-287
    CrossrefPubMedSearch in Google Scholar
  • 33 Rantanen T, Harris T, Leveille SG. et al. Muscle strength and body mass index as long-term predictors of mortality in initially healthy men. J Gerontol A Biol Sci Med Sci 2000; 55: M168-M173
    CrossrefPubMedSearch in Google Scholar
  • 34 Rantanen T, Volpato S, Luigi Ferrucci M. et al. Handgrip strength and cause-specific and total mortality in older disabled women: Exploring the mechanism. J Am Geriatr Soc 2003; 51: 636-641
    CrossrefPubMedSearch in Google Scholar
  • 35 Lynch N, Metter E, Lindle R. et al. Muscle quality. I. Age-associated differences between arm and leg muscle groups. J Appl Physiol (1985) 1999; 86: 188-194
    CrossrefPubMedSearch in Google Scholar
  • 36 Mitchell WK, Atherton PJ, Williams J. et al. Sarcopenia, dynapenia, and the impact of advancing age on human skeletal muscle size and strength; a quantitative review. Front Physiol 2012; 3: 260
    Search in Google Scholar
  • 37 Fragala MS, Cadore EL, Dorgo S. et al. Resistance training for older adults: position statement from the national strength and conditioning association. J Strength Cond Res 2019; 33: 2019-2052
    CrossrefPubMedSearch in Google Scholar
  • 38 Konopka AR, Harber MP. Skeletal muscle hypertrophy after aerobic exercise training. Exerc Sport Sci Rev 2014; 42: 53-61
    CrossrefPubMedSearch in Google Scholar
  • 39 Steffl M, Bohannon RW, Sontakova L. et al. Relationship between sarcopenia and physical activity in older people: A systematic review and meta-analysis. Clin Interv Aging 2017; 12: 835
    CrossrefPubMedSearch in Google Scholar
  • 40 Russ DW, Gregg-Cornell K, Conaway MJ. et al. Evolving concepts on the age-related changes in “muscle quality”. J Cachexia Sarcopenia Muscle 2012; 3: 95-109
    CrossrefPubMedSearch in Google Scholar
  • 41 Nosaka K, Clarkson PM, McGuiggin ME. et al. Time course of muscle adaptation after high force eccentric exercise. Eur J Appl Physiol Occup Physiol 1991; 63: 70-76
    CrossrefPubMedSearch in Google Scholar
  • 42 Radaelli R, Bottaro M, Wilhelm EN. et al. Time course of strength and echo intensity recovery after resistance exercise in women. J Strength Cond Res 2012; 26: 2577-2584
    CrossrefPubMedSearch in Google Scholar
  • 43 Narici MV, Roi GS, Landoni L. et al. Changes in force, cross-sectional area and neural activation during strength training and detraining of the human quadriceps. Eur J Appl Physiol Occup Physiol 1989; 59: 310-319
    CrossrefPubMedSearch in Google Scholar
  • 44 Moritani T, deVries HA. Neural factors versus hypertrophy in the time course of muscle strength gain. Am J Phys Med 1979; 58: 115-130
    PubMedSearch in Google Scholar
  • 45 Delmonico MJ, Harris TB, Visser M. et al. Longitudinal study of muscle strength, quality, and adipose tissue infiltration. Am J Clin Nutr 2009; 90: 1579-1585
    CrossrefPubMedSearch in Google Scholar
  • 46 Berg HE, Larsson L, Tesch PA. Lower limb skeletal muscle function after 6 wk of bed rest. J Appl Physiol (1985) 1997; 82: 182-188
    CrossrefPubMedSearch in Google Scholar
  • 47 Roelofs EJ, Smith-Ryan AE, Melvin MN. et al. Muscle size, quality, and body composition: Characteristics of division I cross-country runners. J Cond Strength Res 2015; 29: 290-296
    CrossrefPubMedSearch in Google Scholar
  • 48 Pichard C, Kyle UG, Gremion G. et al. Body composition by x-ray absorptiometry and bioelectrical impedance in female runners. Med Sci Sports Exerc 1997; 29: 1527-1534
    CrossrefPubMedSearch in Google Scholar
  • 49 Ogden CL, Li Y, Freedman DS. et al. Smoothed percentage body fat percentiles for US children and adolescents, 1999-2004. Natl Health Stat Report 2011; 43: 1-7
    PubMedSearch in Google Scholar
  • 50 US Department of Health and Human Services, Centers for Disease Control and Prevention Centers for Disease Control and Prevention (CDC), National Center for Health Statistics (NCHS), National Health and Nutrition Examination Survey Data. In. Hyattsville, MD. 2019;
  • 51 Jones EJ, Bishop PA, Woods AK. et al. Cross-sectional area and muscular strength. Sports Med 2008; 38: 987-994
    CrossrefPubMedSearch in Google Scholar
  • 52 Reed RL, Pearlmutter L, Yochum K. et al. The relationship between muscle mass and muscle strength in the elderly. J Am Geriatr Soc 1991; 39: 555-561
    CrossrefPubMedSearch in Google Scholar
  • 53 Aagaard P, Suetta C, Caserotti P. et al. Role of the nervous system in sarcopenia and muscle atrophy with aging: Strength training as a countermeasure. Scand J Med Sci Sports 2010; 20: 49-64
    CrossrefPubMedSearch in Google Scholar
  • 54 Goodpaster BH, Carlson CL, Visser M. et al. Attenuation of skeletal muscle and strength in the elderly: The Health ABC Study. J Appl Physiol (1985) 2001; 90: 2157-2165
    CrossrefPubMedSearch in Google Scholar
  • 55 Sinha R, Dufour S, Petersen KF. et al. Assessment of skeletal muscle triglyceride content by 1H nuclear magnetic resonance spectroscopy in lean and obese adolescents: relationships to insulin sensitivity, total body fat, and central adiposity. Diabetes 2002; 51: 1022-1027
    CrossrefPubMedSearch in Google Scholar
  • 56 Addison O, Marcus RL, LaStayo PC. et al. Intermuscular fat: A review of the consequences and causes. Int J Endocrinol 2014; 2014: 309570
    CrossrefPubMedSearch in Google Scholar
  • 57 Gorgey A, Dudley G. Skeletal muscle atrophy and increased intramuscular fat after incomplete spinal cord injury. Spinal Cord 2007; 45: 304-309
    CrossrefPubMedSearch in Google Scholar
  • 58 Visser M, Gallagher D, Deurenberg P. et al. Density of fat-free body mass: Relationship with race, age, and level of body fatness. Am J Physiol 1997; 272: E781-E787
    PubMedSearch in Google Scholar
  • 59 Young HJ, Jenkins NT, Zhao Q. et al. Measurement of intramuscular fat by muscle echo intensity. Muscle Nerve 2015; 52: 963-971
    CrossrefPubMedSearch in Google Scholar
  • 60 Trexler ET, Smith-Ryan AE, Roelofs EJ. et al. Body composition, muscle quality and scoliosis in female collegiate gymnasts: A pilot study. Int J Sports Med 2015; 36: 1087-1092
    Thieme ConnectPubMedSearch in Google Scholar
  • 61 Melvin MN, Smith-Ryan AE, Wingfield HL. et al. Muscle characteristics and body composition of NCAA division I football players. J Strength Cond Res 2014; 28: 3320-3329
    CrossrefPubMedSearch in Google Scholar
  • 62 Guglielmi G, Ponti F, Agostini M. et al. The role of DXA in sarcopenia. Aging Clin Exp Res 2016; 28: 1047-1060
    CrossrefPubMedSearch in Google Scholar
  • 63 Shoepe TC, Ramirez DA, Rovetti RJ. et al. The effects of 24 weeks of resistance training with simultaneous elastic and free weight loading on muscular performance of novice lifters. J Hum Kinet 2011; 29: 93-106.
    CrossrefPubMedSearch in Google Scholar
  • 64 Widrick JJ, Stelzer JE, Shoepe TC. et al. Functional properties of human muscle fibers after short-term resistance exercise training. Am J Physiol Regul Integr Comp Physiol 2002; 283: R408-R416.
    CrossrefPubMedSearch in Google Scholar
  • 65 Krivickas LS, Suh D, Wilkins J. et al. Age- and gender-related differences in maximum shortening velocity of skeletal muscle fibers. Am J Phys Med Rehabil 2001; 80: 447-455
    CrossrefPubMedSearch in Google Scholar
  • 66 Jeon Y, Choi J, Kim HJ. et al. Sex-and fiber-type-related contractile properties in human single muscle fiber. J Exerc Rehabil 2019; 15: 537-545
    CrossrefPubMedSearch in Google Scholar
  • 67 Jee H, Lim J-Y. Discrepancies between skinned single muscle fibres and whole thigh muscle function characteristics in young and elderly human subjects. Biomed Res Int 2016; 1-8
    CrossrefPubMedSearch in Google Scholar
  • 68 Staron RS, Hagerman FC, Hikida RS. et al. Fiber type composition of the vastus lateralis muscle of young men and women. J Histochem Cytochem 2000; 48: 623-629
    CrossrefPubMedSearch in Google Scholar
  • 69 Saltin B, Henriksson J, Nygaard E. et al. Fiber types and metabolic potentials of skeletal muscles in sedentary man and endurance runners. Ann NY Acad Sci 1977; 301: 3-29
    CrossrefPubMedSearch in Google Scholar
  • 70 Costill D, Fink W, Flynn M. et al. Muscle fiber composition and enzyme activities in elite female distance runners. Int J Sports Med 1987; 8: S103-S106
    Thieme ConnectPubMedSearch in Google Scholar
  • 71 Buehring B, Krueger D, Libber J. et al. Dual-energy X-ray absorptiometry measured regional body composition least significant change: effect of region of interest and gender in athletes. J Clin Densitom 2014; 17: 121-128
    CrossrefPubMedSearch in Google Scholar