Biological Sex Differences in Absolute and Relative Changes in Muscle Size following Resistance Training in Healthy Adults
A Systematic Review with Meta-Analysis
DOI:
https://doi.org/10.51224/SRXIV.400Keywords:
resistance training, biological sex, muscle hypertrophy, bayesianAbstract
Muscle hypertrophy may be influenced by biological differences between males and females. This systematic review with meta-analysis investigated absolute and relative changes in muscle size following resistance training (RT) between males and females and whether key variables (i.e., assessment of muscle size, individual characteristics, and RT characteristics) moderate the results. Studies were included if male and female participants were apparently healthy (18-50 years old) adults of any RT experience that completed the same RT intervention, and a valid measure of pre- to post-intervention changes in muscle size was included. Out of 2199 retrieved studies, a total of 27 studies were included in the statistical analysis. Bayesian methods were used to estimate an effect size (ES) and probability of direction (pd) for each outcome. Superior increases in absolute muscle size were estimated in males versus females [ES = 0.35 (95% HDI: 0.20 to 0.49); pd = 100%], however, relative increases in muscle size were similar between sexes [ES = 0.05 (95% HDI: –0.07 to 0.16); pd = 80%]. Sub-group analyses found that the balance of probability favoured relative type I muscle fibre hypertrophy in males versus females [ES = 0.57 (95% HDI: –0.02 to 1.16) pd = 97%] and relative type II muscle fibre hypertrophy in females versus males [ES = –0.36 (95% HDI: –0.97 to 0.23) pd = 89%]. Other variables assessed (i.e., body region, measurement, RT experience, set volume, relative load) did not have a meaningful impact on sex differences in relative muscle hypertrophy.
Metrics
References
Haun CT, Vann CG, Roberts BM, Vigotsky AD, Schoenfeld BJ, Roberts MD. A Critical Evaluation of the Biological Construct Skeletal Muscle Hypertrophy: Size Matters but So Does the Measurement. Front Physiol. 2019;10:247.
Hubal MJ, Gordish-Dressman H, Thompson PD, Price TB, Hoffman EP, Angelopoulos TJ, et al. Variability in muscle size and strength gain after unilateral resistance training. Med Sci Sports Exerc. 2005;37(6):964-72.
Handelsman DJ. Sex differences in athletic performance emerge coinciding with the onset of male puberty. Clin Endocrinol (Oxf). 2017;87(1):68-72.
Vingren JL, Kraemer WJ, Ratamess NA, Anderson JM, Volek JS, Maresh CM. Testosterone physiology in resistance exercise and training: the up-stream regulatory elements. Sports Med. 2010;40(12):1037-53.
Nuzzo JL. Narrative Review of Sex Differences in Muscle Strength, Endurance, Activation, Size, Fiber Type, and Strength Training Participation Rates, Preferences, Motivations, Injuries, and Neuromuscular Adaptations. J Strength Cond Res. 2023;37(2):494-536.
Tesch PA. Skeletal muscle adaptations consequent to long-term heavy resistance exercise. Med Sci Sports Exerc. 1988;20(5 Suppl):S132-4.
Nuzzo JL. Sex differences in skeletal muscle fiber types: A meta-analysis. Clin Anat. 2023.
Handelsman DJ, Hirschberg AL, Bermon S. Circulating Testosterone as the Hormonal Basis of Sex Differences in Athletic Performance. Endocr Rev. 2018;39(5):803-29.
Liu D, Sartor MA, Nader GA, Gutmann L, Treutelaar MK, Pistilli EE, et al. Skeletal muscle gene expression in response to resistance exercise: sex specific regulation. BMC Genomics. 2010;11:659.
Roberts BM, Nuckols G, Krieger JW. Sex Differences in Resistance Training: A Systematic Review and Meta-Analysis. J Strength Cond Res. 2020;34(5):1448-60.
Jones MD, Wewege MA, Hackett DA, Keogh JWL, Hagstrom AD. Sex Differences in Adaptations in Muscle Strength and Size Following Resistance Training in Older Adults: A Systematic Review and Meta-analysis. Sports Med. 2021;51(3):503-17.
Moesgaard L, Jessen S, Mackey AL, Hostrup M. Myonuclear addition is associated with sex-specific fiber hypertrophy and occurs in relation to fiber perimeter not cross-sectional area. J Appl Physiol (1985). 2022;133(3):732-41.
Abou Sawan S, Hodson N, Babits P, Malowany JM, Kumbhare D, Moore DR. Satellite cell and myonuclear accretion is related to training-induced skeletal muscle fiber hypertrophy in young males and females. J Appl Physiol (1985). 2021;131(3):871-80.
Kruschke JK, Liddell TM. The Bayesian New Statistics: Hypothesis testing, estimation, meta-analysis, and power analysis from a Bayesian perspective. Psychon Bull Rev. 2018;25(1):178-206.
Page MJ, McKenzie JE, Bossuyt PM, Boutron I, Hoffmann TC, Mulrow CD, et al. The PRISMA 2020 statement: an updated guideline for reporting systematic reviews. BMJ. 2021;372:n71.
Hurlbut DE, Lott ME, Ryan AS, Ferrell RE, Roth SM, Ivey FM, et al. Does age, sex, or ACE genotype affect glucose and insulin responses to strength training? J Appl Physiol (1985). 2002;92(2):643-50.
Ivey FM, Roth SM, Ferrell RE, Tracy BL, Lemmer JT, Hurlbut DE, et al. Effects of age, gender, and myostatin genotype on the hypertrophic response to heavy resistance strength training. J Gerontol A Biol Sci Med Sci. 2000;55(11):M641-8.
Kojic F, Mandic D, Ilic V. Resistance training induces similar adaptations of upper and lower-body muscles between sexes. Sci Rep. 2021;11(1):23449.
Kosek DJ, Kim JS, Petrella JK, Cross JM, Bamman MM. Efficacy of 3 days/wk resistance training on myofiber hypertrophy and myogenic mechanisms in young vs. older adults. J Appl Physiol (1985). 2006;101(2):531-44.
Hakkinen K, Kallinen M, Izquierdo M, Jokelainen K, Lassila H, Malkia E, et al. Changes in agonist-antagonist EMG, muscle CSA, and force during strength training in middle-aged and older people. J Appl Physiol (1985). 1998;84(4):1341-9.
Hakkinen K, Kraemer WJ, Newton RU, Alen M. Changes in electromyographic activity, muscle fibre and force production characteristics during heavy resistance/power strength training in middle-aged and older men and women. Acta Physiol Scand. 2001;171(1):51-62.
Santos Junior ERT, de Salles BF, Dias I, Ribeiro AS, Simão R, Willardson JM. Classification and Determination Model of Resistance Training Status. Strength & Conditioning Journal. 2021;Publish Ahead of Print.
NSCA. Training Load Chart NSCA.com: NSCA; 2012 [Adapted from Landers, J. Maximum based on reps. NSCA J 6():60-1, 1984]. Available from: https://www.nsca.com/contentassets/61d813865e264c6e852cadfe247eae52/nsca_training_load_chart.pdf.
Refalo MC, Helms ER, Hamilton DL, Fyfe JJ. Towards an improved understanding of proximity-to-failure in resistance training and its influence on skeletal muscle hypertrophy, neuromuscular fatigue, muscle damage, and perceived discomfort: A scoping review. J Sports Sci. 2022:1-23.
Smart NA, Waldron M, Ismail H, Giallauria F, Vigorito C, Cornelissen V, et al. Validation of a new tool for the assessment of study quality and reporting in exercise training studies: TESTEX. Int J Evid Based Healthc. 2015;13(1):9-18.
Swinton P, Murphy A. Comparative effect size distributions in strength and conditioning and implications for future research. SportRxiv. 2022;Preprint.
Coleman M, Burke R, Augustin F, Pinero A, Maldonado J, Fisher J, et al. Gaining more from doing less? The effects of a one-week deload period during supervised resistance training on muscular adaptations. SportRxiv. 2023.
Depaoli S, van de Schoot R. Improving transparency and replication in Bayesian statistics: The WAMBS-Checklist. Psychol Methods. 2017;22(2):240-61.
Hammarstrom D, Ofsteng S, Koll L, Hanestadhaugen M, Hollan I, Apro W, et al. Benefits of higher resistance-training volume are related to ribosome biogenesis. J Physiol. 2020;598(3):543-65.
Schwanbeck SR, Cornish SM, Barss T, Chilibeck PD. Effects of Training With Free Weights Versus Machines on Muscle Mass, Strength, Free Testosterone, and Free Cortisol Levels. J Strength Cond Res. 2020;34(7):1851-9.
Rissanen J, Walker S, Pareja-Blanco F, Hakkinen K. Velocity-based resistance training: do women need greater velocity loss to maximize adaptations? Eur J Appl Physiol. 2022;122(5):1269-80.
Alway SE, Grumbt WH, Stray-Gundersen J, Gonyea WJ. Effects of resistance training on elbow flexors of highly competitive bodybuilders. J Appl Physiol (1985). 1992;72(4):1512-21.
Lundberg TR, Garcia-Gutierrez MT, Mandic M, Lilja M, Fernandez-Gonzalo R. Regional and muscle-specific adaptations in knee extensor hypertrophy using flywheel versus conventional weight-stack resistance exercise. Appl Physiol Nutr Metab. 2019;44(8):827-33.
Walsh S, Kelsey BK, Angelopoulos TJ, Clarkson PM, Gordon PM, Moyna NM, et al. CNTF 1357 G -> A polymorphism and the muscle strength response to resistance training. J Appl Physiol (1985). 2009;107(4):1235-40.
Reece TM, Godwin JS, Strube MJ, Ciccone AB, Stout KW, Pearson JR, et al. Myofiber hypertrophy adaptations following 6 weeks of low-load resistance training with blood flow restriction in untrained males and females. J Appl Physiol (1985). 2023;134(5):1240-55.
Cureton KJ, Collins MA, Hill DW, McElhannon FM, Jr. Muscle hypertrophy in men and women. Med Sci Sports Exerc. 1988;20(4):338-44.
O'Hagan FT, Sale DG, MacDougall JD, Garner SH. Response to resistance training in young women and men. Int J Sports Med. 1995;16(5):314-21.
Psilander N, Eftestol E, Cumming KT, Juvkam I, Ekblom MM, Sunding K, et al. Effects of training, detraining, and retraining on strength, hypertrophy, and myonuclear number in human skeletal muscle. J Appl Physiol (1985). 2019;126(6):1636-45.
McMahon G, Morse CI, Winwood K, Burden A, Onambele GL. Gender associated muscle-tendon adaptations to resistance training. PLoS One. 2018;13(5):e0197852.
Peterson MD, Pistilli E, Haff GG, Hoffman EP, Gordon PM. Progression of volume load and muscular adaptation during resistance exercise. Eur J Appl Physiol. 2011;111(6):1063-71.
Abe T, DeHoyos DV, Pollock ML, Garzarella L. Time course for strength and muscle thickness changes following upper and lower body resistance training in men and women. Eur J Appl Physiol. 2000;81(3):174-80.
Abou Sawan S, Hodson N, Malowany JM, West DWD, Tinline-Goodfellow C, Brook MS, et al. Trained Integrated Postexercise Myofibrillar Protein Synthesis Rates Correlate with Hypertrophy in Young Males and Females. Med Sci Sports Exerc. 2022;54(6):953-64.
Coratella G, Longo S, Ce E, Limonta E, Rampichini S, Bisconti AV, et al. Sex-Related Responses to Eccentric-Only Resistance Training in Knee-Extensors Muscle Strength and Architecture. Res Q Exerc Sport. 2018;89(3):347-53.
Nunes JP, Jacinto JL, Ribeiro AS, Mayhew JL, Nakamura M, Capel DMG, et al. Placing Greater Torque at Shorter or Longer Muscle Lengths? Effects of Cable vs. Barbell Preacher Curl Training on Muscular Strength and Hypertrophy in Young Adults. Int J Environ Res Public Health. 2020;17(16).
Fernandez-Gonzalo R, Lundberg TR, Alvarez-Alvarez L, de Paz JA. Muscle damage responses and adaptations to eccentric-overload resistance exercise in men and women. Eur J Appl Physiol. 2014;114(5):1075-84.
Ribeiro AS, Avelar A, Schoenfeld BJ, Ritti Dias RM, Altimari LR, Cyrino ES. Resistance training promotes increase in intracellular hydration in men and women. Eur J Sport Sci. 2014;14(6):578-85.
Wackerhage H, Schoenfeld BJ, Hamilton DL, Lehti M, Hulmi JJ. Stimuli and sensors that initiate skeletal muscle hypertrophy following resistance exercise. J Appl Physiol (1985). 2019;126(1):30-43.
Hansen M, Kjaer M. Influence of sex and estrogen on musculotendinous protein turnover at rest and after exercise. Exerc Sport Sci Rev. 2014;42(4):183-92.
Haizlip KM, Harrison BC, Leinwand LA. Sex-based differences in skeletal muscle kinetics and fiber-type composition. Physiology (Bethesda). 2015;30(1):30-9.
Chidi-Ogbolu N, Baar K. Effect of Estrogen on Musculoskeletal Performance and Injury Risk. Front Physiol. 2018;9:1834.
Morton RW, Sato K, Gallaugher MPB, Oikawa SY, McNicholas PD, Fujita S, et al. Muscle Androgen Receptor Content but Not Systemic Hormones Is Associated With Resistance Training-Induced Skeletal Muscle Hypertrophy in Healthy, Young Men. Front Physiol. 2018;9:1373.
West DW, Burd NA, Churchward-Venne TA, Camera DM, Mitchell CJ, Baker SK, et al. Sex-based comparisons of myofibrillar protein synthesis after resistance exercise in the fed state. J Appl Physiol (1985). 2012;112(11):1805-13.
Dreyer HC, Fujita S, Glynn EL, Drummond MJ, Volpi E, Rasmussen BB. Resistance exercise increases leg muscle protein synthesis and mTOR signalling independent of sex. Acta Physiol (Oxf). 2010;199(1):71-81.
Tinline-Goodfellow CT, Lees MJ, Hodson N. The skeletal muscle fiber periphery: A nexus of mTOR-related anabolism. Sports Med Health Sci. 2023;5(1):10-9.
Damas F, Phillips S, Vechin FC, Ugrinowitsch C. A review of resistance training-induced changes in skeletal muscle protein synthesis and their contribution to hypertrophy. Sports Med. 2015;45(6):801-7.
Plotkin DL, Roberts MD, Haun CT, Schoenfeld BJ. Muscle Fiber Type Transitions with Exercise Training: Shifting Perspectives. Sports (Basel). 2021;9(9).
Serrano N, Colenso-Semple LM, Lazauskus KK, Siu JW, Bagley JR, Lockie RG, et al. Extraordinary fast-twitch fiber abundance in elite weightlifters. PLoS One. 2019;14(3):e0207975.
Hunter SK. Sex differences in human fatigability: mechanisms and insight to physiological responses. Acta Physiol (Oxf). 2014;210(4):768-89.
Hunter SK. Sex differences and mechanisms of task-specific muscle fatigue. Exerc Sport Sci Rev. 2009;37(3):113-22.
Hunter SK. Sex differences in fatigability of dynamic contractions. Exp Physiol. 2016;101(2):250-5.
Refalo MC, Helms ER, Hamilton DL, Fyfe JJ. Influence of Resistance Training Proximity-to-Failure, Determined by Repetitions-in-Reserve, on Neuromuscular Fatigue in Resistance-Trained Males and Females. Sports Med Open. 2023;9(1):10.
Refalo MC, Hamilton DL, Paval DR, Gallagher IJ, Feros SA, Fyfe JJ. Influence of resistance training load on measures of skeletal muscle hypertrophy and improvements in maximal strength and neuromuscular task performance: A systematic review and meta-analysis. J Sports Sci. 2021:1-23.
Wang Y, Luo D, Liu J, Song Y, Jiang B, Jiang H. Low skeletal muscle mass index and all-cause mortality risk in adults: A systematic review and meta-analysis of prospective cohort studies. PLoS One. 2023;18(6):e0286745.
Taber CB, Vigotsky A, Nuckols G, Haun CT. Exercise-Induced Myofibrillar Hypertrophy is a Contributory Cause of Gains in Muscle Strength. Sports Med. 2019;49(7):993-7.
Kavvoura A, Zaras N, Stasinaki AN, Arnaoutis G, Methenitis S, Terzis G. The Importance of Lean Body Mass for the Rate of Force Development in Taekwondo Athletes and Track and Field Throwers. J Funct Morphol Kinesiol. 2018;3(3).
Hunter SK. The Relevance of Sex Differences in Performance Fatigability. Med Sci Sports Exerc. 2016;48(11):2247-56.
Enns DL, Tiidus PM. The influence of estrogen on skeletal muscle: sex matters. Sports Med. 2010;40(1):41-58.
Downloads
Additional Files
Posted
Versions
- 2024-09-22 (2)
- 2024-04-28 (1)
Categories
License
Copyright (c) 2024 Martin Charles Refalo, Greg Nuckols, Andrew Galpin, Iain Gallagher, D. Lee Hamilton, Jackson Fyfe (Author)
This work is licensed under a Creative Commons Attribution 4.0 International License.
