Are We Able to Match Non Sport-Speciﬁc Strength Training with Endurance Sports? A Systematic Review and Meta-Analysis to Plan the Best Training Programs for Endurance Athletes

: Non-sport-speciﬁc strength training is a way to increase endurance performance; however, which kind of exercise (maximal, plyometric, explosive or resistance strength training) gives the best results is still under debate. Scientiﬁc publications were analyzed according to the PRISMA checklist and statement. The initial search yielded 500 studies, 17 of which were included in this review using the PEDro Scale. Maximal strength training boosted the ability to express strength particularly in cross-country skiing and cycling, increasing endurance performance, measured as a decrease of the endurance performance tests. In running, explosive strength training did not generate advantages, whereas plyometric strength training led to an improvement in the endurance performance tests and work economy. In running it was possible to compare different types of non sport-speciﬁc strength training and the plyometric one resulted the best training methodology to enhance performance. However, studies on other sports only investigated the effects of maximal strength training. It resulted more effective in cross-country skiing (although only one study was eligible according to the inclusion criteria) and in the cycling component of the triathlon and, by contrast, induced modest effects on cyclists’ performance, suggesting different type of strength would probably be more effective. In conclusion, each sport might optimize performance by using appropriate non sport-speciﬁc strength training, which, however, should be studied individually. Glossary: Explosive strength—the ability to exert maximal forces in minimal time; maximum strength— the maximum force a muscle can exert in a single maximal voluntary contraction; plyometric strength— the explosive movements in which a concentric muscle action is enhanced by a previous eccentric contraction; resistance strength—the contraction ability against an opposing force.


Introduction
Endurance training leads to vascular and muscular adaptions, favoring the improvement of endurance performance. [1]. More recently, it has been shown that exercise economy is one of the factors determining performance in endurance sports [2]. Exercise economy is defined as the oxygen uptake required at a given submaximal speed [1] and this concept is frequently associated with the work economy that is expressed as aerobic metabolic rate or oxygen uptake at a given speed [3].
Many sports require a combination of strength and endurance training for successful performance and it is known that the inclusion of strength training in an endurance season training period can represent the key strategy to enhance the endurance performance [4]. Strength training increases muscle strength and power. Indeed, in well-trained athletes, the capacity to sustain a high intensity in endurance performances, without the influence of aerobic capacity, could be associated to the strength development [3]. The effectiveness of concurrent training-such as endurance and strength training in the same training program-has long been recognized, in fact, expert trainers believe that the addition of

Eligibility Criteria
Studies meeting the following criteria were included or excluded to this review.

Inclusion
Studies from 1 January 2009 to 31

Exclusion
• Reviews and Ph.D. theses; • Specific strength training interventions (i.e., strength exercises directly related to a specific sport activity); • Studies evaluating only one physiological or biomechanical parameter (i.e., VO 2 max, Lactate, WE, time trial (TT) or time trial to exhaustion (TTE)), to exclude the accidental effects that could improve the endurance performance; • Non-athlete subjects recruited.

Quality Assessment
The selected studies were rated using the Physiotherapy Evidence Database (PEDro) Scale. The PEDro scale accounts for the internal validity and interpretability of experimental trials. The scale scores internal validity through aspects of study design, such as randomization, allocation, similarity of key measures at baseline, and blinding of subjects, therapists, and assessors. Additionally, the scale measures the interpretability of research by examining between-group statistics, descriptions of point measures, and measures of variability. The 11-item scale ( Table 1) yields a maximum score of 10 points if all criteria are satisfied. Only papers reaching a minimum cut-off of 5 points on the PEDro scale were finally included in the analysis.  Linked table footnotes: Items in the PEDro scale. 1 = eligibility criteria were specified; 2 = subjects were randomly allocated to groups; 3 = allocation was concealed; 4 = the groups were similar at baseline regarding the most important prognostic indicators; 5 = blinding of all subjects; 6 = blinding of all therapists who administered the therapy; 7 = blinding of all assessors who measured at least 1 key outcome; 8 = measures of 1 key outcome were obtained from 85% of subjects initially allocated to groups; 9 = all subjects for whom outcome measures were available received the treatment or control condition as allocated or, where this was not the case, data for at least 1 key outcome were analysed by "intention to treat"; 10 = the results of between-group statistical comparisons are reported for at least 1 key outcome; 11 = the study provides both point measures and measures of variability for at least 1 key outcome.

Statistical Analysis
We conducted two meta-analyses using Statsdirect v3.3 (Statsdirect, Birkenhead, UK) with the aim to find which type of non-specific strength training improved better the endurance ability, thus the performance. Our primary outcome included the economy of gesture, assessed as WE; in a secondary outcome we assessed the endurance performance through the tests TT or TTE. The studies included in the meta-analyses were screened for inconsistency by using the I2 statistic, and pooled estimates of the effect of non-specific strength training (NST) on the endurance ability were obtained by DerSimonian-Laird's method in a random-effect model. The results of Vikmoen et al. (2017) [30] about work economy were duplicated in order to describe the impact of NST in running and cycling separately. Egger's test was used to assess the presence of publication bias.

Included Studies
The initial search yielded 500 publications. Duplicated studies were excluded (n = 348). Studies considered to be potentially relevant after reading the abstract (n = 152) were reviewed, reading the full text. Among those, more papers were excluded because they were not relevant (n = 26) or dealt with generic topics (n = 33) or reviews (n = 19). Of the remaining 74 articles, 57 papers were excluded they did not meet the inclusion criteria (21 = year of publication, 7 = Ph.D. theses, 15 = subjects training level and background level, 4 = strength intervention duration, 10 = strength intervention type). In the end, 17 studies were included in this review (Figure 1), focused on the following endurance sports: cross-country skiing (n = 1), triathlon (n = 2), cycling (n = 8) and running (n = 6).

Data Extraction and Outcome Measures
Data from the selected studies were extracted and summarized in three main tables as follows: All the study details, including purpose, athletes, research design and quality assessment, are shown in Table 2: author name and year of publication, characteristics of

Data Extraction and Outcome Measures
Data from the selected studies were extracted and summarized in three main tables as follows:

Study Characteristics
All the study details, including purpose, athletes, research design and quality assessment, are shown in Table 2: author name and year of publication, characteristics of athletes (number, gender, mean age, mean VO 2 max, experience and reported endurance training), research design (type of research and athletes assignment to a study groups) and quality assessment by the PEDro Scale. Among the 17 included studies, a total of 334 national and international athletes (n = 244 male, n = 90 female), with a mean age of 27.75 + 6.76 and a VO 2 max range between 52.4 and 80 mL/kg/min, were distributed in a specific group as follows: 10 studies used the randomized controlled trial (RCT) model [15,[17][18][19][20]23,26,[28][29][30], randomly allocating the participants into the control or intervention groups; four non-randomized studies stratified participants for gender, age and VO 2 max [16,22,25,27]; three studies [21,24,31] used the self-choice method to allocate the subjects in the groups. All subjects were "Highly trained" or "High level" athletes following usual endurance training ("ET declared"), performed in specific heart rate (HR) zones in nine studies [18,20,21,[24][25][26][27][28]30].

Aerobic Capacity and Work Economy
The aerobic capacity was evaluated by VO 2 max/peak or maximal aerobic speed (MAS). Two studies showed an increase of aerobic capacity [16,31] and one a decrease [24], whereas the others did not report a direct improvement in VO 2 max or MAS. In general, the VO 2 max or aerobic capacity parameters were not correlated to the improvement in WE. Of note, almost all studies assessed the increase of WE after NST (Table 4). Those studying running showed a significant increase of running economy (RE) (7%) [13] or speed (from 2.3% to 6.17%) [16][17][18][19]30], as well as in studies on cycling was reported a significant increase of cycling economy (CE) (4.7%) [22] or VO 2 value consumed during cycling test (−2.2%) [24] or speed at specific power outputs [30]. Similarly, the study on cross-country skiing showed a significant increase of double poling economy (+7.4%) [31]. By contrast, seven studies instead did not report any change on WE [20,21,23,[27][28][29]. Because WE represent one of the major parameters associated to endurance performance, we considered its modulation in response to each type of NST in the different sport disciplines, as detailed below.

Maximal Strength Training (MST)
The running studies using a MST protocol showed an increase in maximal strength ability, assessed by 1RM test, correlated to the improvement in the work economy in running (running economy-RE, measured as running speed (speed at 7 mmol/L + 2.6%, p = 0.049 [16]), or as running pace race (marathon pace +6.17%, p < 0.05 [17]) or as performance on "5 min all-out" in the triathlon study (+4.7%, p < 0.05 [30]). In the cycling studies four studies did not report the results or changing about work economy (cycling economy-CE) [21,23,27,28], while the others were in agreement with the running studies, as they showed an improvement in CE after MST, evaluated as percentage of VO 2 expression, correlated to the gain in RFD Squat test (70% of VO 2 max +4.7%, p < 0.05, r = 0.58 [23]), or as peak torque pedal stroke (p = 0.007 [25,26]) or as performance on "5 min all-out" (+7%, p < 0.05 [30] in the triathlon study), or evaluated as VO 2 during the test, correlated to the gain in the 1RM half squat test (VO 2 during cycling test −2.2%, p < 0.05 [24]). According to data from running or cycling studies, also in the cross-country skiing study [31] MST increased WE, measured with 5 min of double poling test (+7.4%, p < 0.05) (cf. with Figure 2). However, even if MST positively affected WE in all the sports considered, it was also associated with an increase of both strength ability, as expected, and muscles' cross-section area (CSA) in running [20], cycling [21,24,26,30] and cross-country skiing [31], as detailed in Table 4.

Explosive Strength Training (EST)
The EST in running studies [15,16] did not show a substantial improvement in RE. Indeed, by using EMG, Mikkola and coworkers [16] demonstrated that explosive performance was higher in athletes trained for maximal strength (see study groups in Tables 3 and 4) than explosive strength.

Explosive Strength Training (EST)
The EST in running studies [15,16] did not show a substantial improvement in RE. Indeed, by using EMG, Mikkola and coworkers [16] demonstrated that explosive performance was higher in athletes trained for maximal strength (see study groups in Tables  3 and 4) than explosive strength.

Resistance Strength Training (RST)
The RST was limited to running and always combined to other kind of strength training. Piacentini and colleagues [17] applied a protocol of RST and MST, whereas Sedano and colleagues [18] (data not shown in the meta-analysis) associated RST to PST, obtaining in both conditions an amelioration of the RE. The results on the effect of NST on our primary outcome (economy of gesture, assessed as WE) are detailed and summarized in Figure 2.
MST: Among running studies, only   [20] assessed MST alone, namely without any comparisons with other types of NST, but the authors did not report any significant improvement, whereas in cycling studies, MST improved both TT or TTE in almost all studies (Figure 3), as well as the Po test. The higher strength expression (1RM test) was correlated to the improvement in the TT "5 min all-out" (+7.2%, p < 0.01 [24]; +7%, p = 0.007 [25]) and in the "45 min TT" (+8%, p < 0.05 [23]) as well as the increased strength (RFD +16.2%) was associated to TTE amelioration (+17.2%, r = 0.64 [22]). Accordingly, the cycling-specific strength expression (peak pedal torque) was related to the increase in Po efficacy, measured with the specific Wingate test [26] but also in the Pm expression during TT test [25].
In agreement with the cycling studies, cross-country skiing study reported a gain in maximal strength that consequently led to an improvement in TT performance (upper body 1.1 km TT +7%, p < 0.05 [31]).
PST, EST and RST. PST could be also associated to different kinds of strength training. Indeed, it was considered as the principal protocol [19] or it was compared to EST [15] or to both RST and endurance training [18]. In both cases PST reported positive results on TT and TTE performance in the running studies, leading to an improvement in endurance performance [15,18,19]. Indeed, in the study of Ramirez-Campillo and colleagues [19] the improvement in the TT was correlated to the reduction in time spent in both 2.4 km and 20 m sprint performance tests.

Discussion
The purpose of this systematic review and meta-analysis was to understand whether different non sport-specific strength training, namely strength exercises that do not recall the sport-specific movements, could be related to best performances in specific endurance sports (running, cycling, triathlon and cross-country skiing).
In general, the aerobic parameters (VO 2 max or MAS) did not change from pre-to post-intervention, while the endurance performance increased. The gain in endurance performance, therefore, could only be linked to mechanical factors and these-as expectedwere different in the different sports. In agreement with these findings, Authors [32,33] showed that aerobic capacity was not inhibited by concurrent training (endurance and strength training). Rather, a better neuromuscular coordination delaying the onset of fatigue after strength intervention and a skeletal muscles changes in fiber composition might be the mechanism responsible for the increase of aerobic performance [34][35][36]. Therefore, we looked across literature for the type(s) of non-sport-specific strength training (MST, PST, EST and RST) reported as more efficient in increasing endurance ability, focusing on WE (running economy, cycling economy, double poling economy) ( Figure 2) and endurance performance tests (TT, TTE and Po) (Figure 3). Even if different study designs and methodologies could possibly influence the results, the quality of the studies considered was acceptable, considering the PEDro score. In these studies, all NST intervention types impacted on performance (cf. with Figures 2 and 3, positive combined effect size), improving several physiological parameters relevant for endurance athletes. However, considering the aforementioned 4 endurance sports, we found data on the comparison between different types of NST only for running, whereas for the other disciplines only MST was considered. Indeed, maximal strength training is the most studied type of exercise among non-sport-specific strength training across the plentiful literature, while scarce data is available on plyometric, explosive or resistance strength training. Therefore, the data reported in this meta-analysis could help in prompting new studies on endurance sports.
As reported in Figure 2, the work economy was positively affected by MST in general, which in running resulted more efficient than explosive [16] or resistance [17] training. However, when it was compared to plyometric [15] training, MST showed less efficacy in ameliorating running economy. This scarce effect of MST was evident also in cycling, as in all the studies reporting cycling economy values most of those resulted smaller than the overall effect [21,[23][24][25][26]28]. Therefore, it is reasonable to hypothesize that nonsport-specific strength training other than MST might be considered to improve work economy in cycling. By contrast, when cycling is considered as the component of triathlon discipline, its work economy seems positively affected by MST [30], as well as the running component [30]. Even if only one study on cross-country skiing was included in this metaanalysis, the MST was clearly able to improve work economy [31], suggesting that this type of non-sport-specific strength training might be effective in cross-country skiing athletes.
As shown in Figure 3, the non-sport-specific strength training effects on endurance performance were variable. Among studies on running, only three reported data on endurance performance [15,19,20], considering plyometric or maximal strength training. MST resulted ineffective on endurance performance in running [20] as well as PST. This result of PST in endurance performance in running might be due to the low frequency [15] or time [19] of training protocols (see Table 3).
Significant improvements in endurance performance were obtained by MST in cycling [22][23][24][25][26][27]; however, the variability of these results reinforces the idea that different types of non-sport-specific strength training might be preferable in this discipline. Unfortunately, the lack of data on endurance performance in the triathlon did not allow us to speculate on running and cycling components.
Summarizing, in running the better non-sport-specific strength training seems to be PST, even if MST could induce some improvements. By contrast, EST might be inappropriate for best performance in running. Although MST was the only non-sport-specific strength training studied in cycling, our analysis suggests that other types of exercises might be more effective. Indeed, as we found in running, we can speculate that PST or other strength trainings might be preferable in cycling. By contrast, for both triathlon and cross-country skiing, MST can be recommended.
In conclusion, the results of our meta-analysis support the hypothesis that appropriate non-sport-specific strength training can optimize performances in specific endurance sport disciplines.

Limitations
Only studies on running compared different types of non-sport-specific strength training, and all the other sport disciplines were investigated according to MST exclusively. Only two publications concerned triathlon and just one was focused on cross-country skiing. Therefore, further research is needed to obtain more data for all the types of nonsport-specific strength training included in this review. Some of the studies that matched the items of the PEDro scale, did not report data on the investigated outcomes, therefore they were not included in the meta-analysis, that could be also influenced by different methodologies and assessment tests of the relevant parameters among studies.

Perspective
Although the literature on NST is increasing, the idea of looking at NST in terms of sport-specificity is innovative. Consequently, to the best of our knowledge this is the first meta-analysis assessing which type of NST is more efficient to achieve a better performance in endurance sports. Our findings indicate that MST is the most studied type of NST applied to endurance sports, even if it may not be the best. Indeed, for instance, best running performances were obtained by PST. Therefore, it is more than plausible that future optimal matching of NST with sport disciplines will boost athletic performance. These results are of primary importance for coaches focused on planning the best training programs for elite endurance athletes. Our approach, however, also highlights how additional studies are necessary to reach a full understanding of this topic in view of its relevant practical applications.

Data Availability Statement:
The data presented in this study are available within the article.

Conflicts of Interest:
The authors declare no conflict of interest.