It is well-established that both males and females can increase muscle size and strength in response to resistance training (RT) (29). Furthermore, several studies have shown RT has multiple benefits for overall health (39,41,58). Although there have not been any studies that use dose-response models to determine whether males and females respond differently to chronic RT, several studies have compared the adaptations of males and females using the same training protocol. However, whether there are sex-specific adaptations to the same training is still unclear.
In most studies, males increase absolute strength more than females (10,12,68). Yet, some find that the relative increase in muscle strength and hypertrophy are similar between sexes (1,21,28,30,32,36,40,67,70,78,85). However others find females have a greater relative strength increase (7,9,29,34,36,38,48,55,56,63,79). In one of the largest studies to date, Hubal et al. (29) found females have higher relative strength increases than males.
A key consideration in comparing the responses in males and females is that pre-training levels of muscle size and strength are generally greater in males, independent of training status (3,35,67). Another well-known set of differences between males and females are hormonal, which may influence muscle hypertrophy and strength adaptations. There also may be some differences in types of occupation that could cause basal strength differences. However, there is currently no review bringing together the major differences between sexes at the neuromuscular, muscular, and hormonal level in the context of RT.
Considering the importance of muscle strength and size to overall health and exercise performance, it is important to understand sex differences in response to RT if they exist. Therefore, the purpose of this study is to determine whether there are different responses to RT for strength or hypertrophy in young to middle-aged males and females.
Experimental Approach to the Problem
Research publications were considered eligible for this systematic review if they (a) were experimental in design, (b) were published in a peer-reviewed, English-language journal, (c) were conducted in human populations, (d) included at least 1 method of estimating changes in muscle mass and/or dynamic, isometric, or isokinetic strength, and (e) had subjects who were between 18 and 50 years old (Table 1).
Studies were considered ineligible for this review if (a) the training protocol lasted for <5 weeks, (b) the study involved subjects with medical conditions, pregnancy, or injuries impairing training capacity, (c) subjects were taking supplements or hormone replacement therapy. Case studies were not included. Studies that were not written in English, conference abstracts, thesis, or posters were also excluded from this review.
Our protocol was pre-registered with PROSPERO (CRD42018094276). The systematic review was performed in accordance with the guidelines provided by the Preferred Reporting Items for Systematic Reviews and Meta-Analyses (PRISMA). A literature review was conducted up until April 2018 using Medline and SportDiscus. Combinations of the following terms were used to produce search results: gender or sex AND strength training or RT or powerlifting AND strength or hypertrophy or 1 repetition maximum. Search terms were added using the NOT term to reduce the number of irrelevant studies according to exclusion criteria (concurrent, children, disease, supplement). Citations from studies were also scanned for additional studies (Figure 1).
A total of 1,162 studies were identified using the aforementioned search terms, and 24 were additionally identified through other sources. Eighty studies were identified as being eligible for the review. After full-text review, 30 were removed for not meeting the inclusion criteria. Ultimately, 50 studies were deemed to have satisfied the inclusion criteria. Of those studies, 10 were analyzed for hypertrophy measures, 17 for upper-body strength, and 23 for lower-body strength.
Coding of Studies
Studies were independently searched and coded by 2 of the authors (G.N. and B.M.R.) for the following variables: descriptive information (age, sex, training status), the number of subjects per group, training mode, duration of study, training frequency, repetition range, mode of muscle measurement (magnetic resonance imaging, fiber cross sectional area [fCSA], ultrasound, and computed tomography). Results were cross-checked between coders, and any discrepancies were resolved by mutual consensus.
Calculation of Effect Size
For each hypertrophy and strength outcome, a within-group effect size (ES) for each male and female group was calculated as the pretest-posttest change, divided by the pretest standard deviation (SD) (54). A study level ES was then calculated as the difference between the male group ES and female group ES. A small sample bias adjustment was applied to each ES (54). The sampling variance around each ES was calculated using the sample size in each study (6).
Meta-analyses were performed using robust variance random effects modeling for multilevel data structures, with adjustments for small samples using package robumeta in R (27,82). The study was used as the clustering variable to account for correlated group effects within studies. Observations were weighted by the inverse of the sampling variance. Separate analyses were conducted for hypertrophy, upper-body strength, and lower-body strength. A fail-safe N was performed to calculate the number of null studies needed to achieve a p value of 0.05 or greater using the Rosenthal approach.
All analyses were performed in R version 3.5 (The R Foundation for Statistical Computing, Vienna, Austria). Effects were considered significant at P ≤ 0.05. Data are reported as means ± SEM and 95% confidence intervals (CIs) unless otherwise specified.
The quality of studies is important for analysis of systematic reviews and meta-analysis. However, due to the nature of studies on sex differences, it is difficult to blind subjects, therapists, assessors, conceal allocation, or randomly allocate, which are integral parts of quality assessment. Because this eliminates half of the questions in most scales, we felt it was unworthy to perform these types of quality assessments.
The analysis of hypertrophy comprised 12 outcomes from 10 studies. There was no significant difference between males and females (ES = 0.07 ± 0.06; 95% CI: −0.09 to 0.23; P = 0.31; Figure 2). Heterogeneity was low (I2 = 0) (Figure 3).
The analysis of upper-body strength comprised 19 outcomes from 17 studies. There was a significant effect favoring females (ES = −0.60 ± 0.16; 95% CI: −0.93 to −0.26; P = 0.002; Figure 4). Heterogeneity was high (I2 = 72.1). Adding training status (trained or untrained), single or multijoint strength measurements (e.g., leg extension or leg press), training duration (weeks), or sessions per week as covariates did not substantially reduce heterogeneity (I2 = 69.7) (Figure 5).
The analysis of lower-body strength comprised 23 outcomes from 23 studies. There was no significant difference between sexes (ES = −0.21 ± 0.16; 95% CI: −0.54 to 0.12; P = 0.20; Figure 6).
Heterogeneity was high (I2 = 74.7). Adding training status (trained or untrained), single or multijoint strength measurements (e.g., leg extension or leg press), training duration (weeks), or sessions per week as covariates did not substantially reduce heterogeneity (I2 = 77.4) (Figure 7).
Because of the limited sample size, we completed a sensitivity analysis on all 3 outcomes where 1 study at a time was removed to determine whether that a particular study had any significant impact on the outcomes. However, we did not identify any influential studies.
A rank correlation test for funnel plot asymmetry was performed for the upper-body strength results because there was a significant finding (Figure 8). It was not significant (P = 0.41). We also used a fail-safe N to calculate the number of null studies needed to achieve a p value of 0.05 or greater using the Rosenthal approach. The fail-safe N was 294. Thus, there was no evidence of publication bias for the upper-body strength outcomes.
This review meta-analyzed studies that compared strength or direct measures of hypertrophy in males and females who used the same RT program. A majority of the studies were completed in untrained individuals. The main finding was that effect sizes in hypertrophy and lower-body strength were similar between sexes. However, there was a significant effect in favor of females for upper-body strength (ES = −0.60; 95% CI: −0.93 to −0.26; P = 0.002).
Muscular strength increases in response to RT are a combination of neurological and muscular adaptations. Initial, rapid improvements in strength seem to result primarily from neurological adaptation, whereas subsequent gains are primarily the result of muscular adaptations (53). In one of the first studies comparing untrained males and females, Wilmore et al., found that strength was similar when normalized to body weight after 10 weeks of intensive RT (90). Interestingly, relative upper-body strength increased 29% in females compared with 17% in males, whereas relative increases in lower-body strength were similar (90). These data were the first data to indicate there may be differences in strength changes between sexes. However, a limitation was that both groups experienced considerable decreases in body fat percentage over the course of the study, indicating they were likely not in an optimal nutritional environment for gaining or maintaining muscle mass or strength (90). More recent data have indicated that both sexes respond to upper-body strength in a similar manner (18). Yet, in the largest study to date with ∼342 females and ∼243 males, there was a significant difference in relative upper strength changes in favor of females (29). Herein, we cover a number of potential variables that could help explain the differences in strength we and others have found.
Neuromuscular adaptations are one factor that could explain the larger increase for females in upper-body strength. However, one study compared the number of motor units in the biceps brachii and vastus medialis but found no differences between sexes (50). The same research group also found no difference in motor unit activation for elbow flexion or knee extension (50). Others have found that males are no better able to activate motor units than females (5,91). Yet, neuromuscular fatigue from RT is generally greater in males than females, and acute recovery may be slower in males (20). Because the included studies are short in nature, this could have an effect on strength adaptations if subjects are not fully recovered during testing. The average untrained female may also have a lower initial level of fitness compared with a male (74). This could cause a ceiling effect for motor skills that may explain differences in upper-body strength because the studies were conducted in mostly untrained subjects. Ultimately, there are very few known differences at the neuromuscular level between sexes that could explain our findings, but more research is warranted.
It is well established that sex differences exist in skeletal muscle mass and distribution (35). Females often have less total and lean body mass, a higher body fat percentage, and a smaller muscle fiber cross-sectional area (65,78). One explanation of why differences could occur in strength or hypertrophy is muscle phenotype. Females have a greater proportion of type I fibers (65,75) in the vastus lateralis and the biceps brachii (3,50,69). There are currently no studies that compare the number of muscle fibers between sexes, but a classic study has shown the muscle fiber number decreases with age in males, although our data did not include those over 50 (44). Furthermore, there seem to be similar responses in muscle protein synthesis between sexes (47,76,86), and muscle damage due to RT is also similar between, yet the inflammatory response may be attenuated in females compared with males (80). However, there are some data to indicate that although there are similar indirect markers of muscle damage after RT, males could have longer-lasting muscle soreness than females (11). On a single fiber level, force per CSA and contractile velocity of type I and type II fibers are similar when comparing sexes (83). Taken together, there are relatively few differences in skeletal muscle between sexes, which helps explain our finding that hypertrophy is similar.
It was once postulated that females achieved small increases in muscle size after RT because of low androgen levels whereby a lesser amount of work-induced muscle hypertrophy would prevent them from gaining strength to the same extent as males (85). Although it is true that absolute hypertrophy and gains in strength are larger in males after RT, it seems that relative increases in both muscularity and lower-body strength are similar between the sexes, and relative gains in upper-body strength may be larger in females. Indeed, it is well established that females have lower levels of testosterone, free-testosterone, and insulin-like growth factor-binding protein 1 compared with males (65). Heavy training decreases gonadotropin-releasing hormone pulsatility in females (66). Males exhibit lower serum cortisol due to chronic RT, whereas females do not (78). Females do not experience elevations in postexercise testosterone compared with males (16,86). This differential change in testosterone has led to speculation that females may have an attenuated potential for resistance exercise-induced hypertrophy, which we did not find in our analysis (72). Another difference is that males have more upper-body muscle, which has more androgen receptors (37). Gentil et al. (18) suggest that this could affect strength gains over time. Another potential confounder is the menstrual cycle. Some evidence suggests that females who complete training during the follicular phase can have larger strength gains and more muscle growth (59, 81, 88) while females may take longer to recover during the luteal phase (46), and most of the studies included did not adjust for menstrual cycle. However, other evidence suggests that the changes in protein kinetics across the menstrual cycle may not play a large role in muscle accrual (51). Although some studies suggest that hormonal differences play a role in changes, larger and well-controlled studies are needed to understand why that occurs or how it affects strength or hypertrophy adaptations.
In a recent review, Hunter presents evidence that sex differences in muscle fatigue of repeated dynamic contractions are specific to the task requirements (31). Females may have less skeletal muscle fatigue compared with males during single-limb isometric contractions. It has also been suggested that there are independent responses to fatiguing contractions (31). Likewise, shortening velocity is a potential factor to tease out the contribution of voluntary activation and contractile mechanisms (73). There is also evidence that female tendons have a smaller capacity for adaptation to training (52,87), which may be exacerbated by oral contraceptive use (26) and could potentially affect strength adaptations.
Although a strength of this study is that it is the first meta-analysis completed on sex differences, there are several limitations. First, most subjects included in the analysis are untrained individuals. It is possible that a longer training duration or other factors could change the results. In addition, the untrained subjects could have different levels of basal activity between studies as it is often not well described in exercise science research. The studies included also vary with regard to mode, duration, and intensity of exercise utilized. However, our analysis of upper-body strength found no evidence publication bias and no single studies of major influence. It has been argued (1) that many of the earlier studies conducted on sex comparisons for both strength and muscular hypertrophic changes were hampered by low statistical power resulting from small sample sizes (all ≤20 subjects). Another potential limitation is missing studies due to unused search terms or databases. There is also a possibility that male subjects could be more familiar with upper-body movements (e.g., bench press) that could have resulted in females having greater neuromuscular adaptations. Finally, heterogeneity was high for the outcomes of studies assessing both upper and lower-body strength, yet incorporating training status, testing modality, duration, or sessions did not substantially decrease heterogeneity. Although there was a mean effect in favor of females for upper-body strength gains and no significant difference between the sexes for lower-body strength gains, more research is needed to understand the sources of this heterogeneity.
We found that males and females adapted to RT with similar effect sizes for hypertrophy and lower-body strength, but females had a larger effect size for relative upper-body strength. Current research indicates there are few differences at the skeletal muscle level between sexes. However, hormonal fluctuations, daily physical activity, and exercise recovery may play a role in our findings. In sum, well-designed studies with a primary goal of comparing male and females are relatively few, and our understanding of sex differences in the physiology of RT is incomplete, which makes studies on sex-differences warranted.
Given the moderate effect size favoring females in the upper-body strength analysis, it is possible that untrained females display a higher capacity to increase upper-body strength than males. Further research is required to clarify why this difference occurs only in the upper body and whether the differences are due to neural, muscular, or motor learning adaptations. In practice, it is important to know that both males and females can considerably increase muscle strength and size with RT. Because there are is a paucity of studies comparing multiple RT programs between sexes, it is currently difficult to know if exercise prescription should be different between sexes.
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