Effects of different methods of strength training on indicators of muscle fatigue during and after strength training: a systematic review

Introduction: The development of strength has shown to be beneficial to sports performance and health. However, during strength training, they also produce alterations in muscle fatigue indicators, leading to a decrease in the ability to generate strength. Despite this, there is still not enough knowledge about the levels of muscle fatigue generated by different methods of strength training and how this information can be integrated into sports planning. Review and analyze the studies existing between January 2009 and January 2019 that have used indicators of muscle fatigue established in the search terms during and after strength training as measurement variables. Evidence acquisition: The study corresponds to a systematic review of previously published studies, following the PRISMA model. Articles published between 2009 and 2019 that measured muscle fatigue indicators during and after strength training were evaluated. The electronic search was conducted through Web of Science, Scopus, Sport Discus, PubMed, and Medline. We included all articles that used a strength protocol and also measured indicators of muscle fatigue and its possible effect on physical performance. Evidence synthesis: A total of 39 articles were found, which were stratified according to the protocol used: (i) plyometric training, (ii) Bodypump® training, (iii) occlusion training, (iv) variable resistance training, (v) conventional strength training, (vi) eccentric strength training, (vii) rest times in strength training and (viii) concurrent training. Conclusion: At the end of the systematic review, it was shown that the different training methodologies for strength development generate increases in muscle fatigue indicators, and the increase generated in the different muscle fatigue indicators depends both on the methodology used and on the type of population, sex, level of training and type of sport. The most-reported indicators are [La], HR and RPE, DOM, MR variation, and ammonium.


Introduction
Today, sports training is based on the development of the various manifestations of force 1 . Thus, several investigations have recognized muscle strength as the main capacity to produce a high level of muscle power 1,2 and neuronal adaptations 3 , which favor the development of muscular hypertrophy 4 . In this sense, optimal muscle development has been associated with sports performance and a better quality of life 5 . On the contrary, a decrease in muscle strength and neuromuscular control change the functional behavior of an athlete, limiting performance and possibly triggering an injury 6 .
In order to achieve optimal development of strength, power and muscular hypertrophy, traditional 7-13 and non-traditional training methods have been used, including plyometric exercises on land [14][15][16][17][18] , plyometrics in the aquatic environment 19 , occlusion training [20][21][22][23] , training with elastic bands 24 , electrostimulation training 11 , eccentric exercises 25 , and Bodypump® programs 26,27 . These methods have demonstrated, in several cases, increases in sports performance 4,25,27 . However, it has also been documented that strength training produces alterations in muscle fatigue indicators [28][29][30] . In this sense, fatigue has been defined as a reduction in the ability of the neuromuscular system to generate strength or to carry out work resulting from physical exercise 31,32 . Thus, a decrease in the production of strength, in its different manifestations during and after strength training, has been associated with increases in blood uric acid 33 , ammonium 32 , lactate concentrations ([La]) 34 , elevated heart rate (HR) 16 , increased perception of effort (RPE) 35 , increased muscle pain (DOMS) 36 , and decreased range of motion (ROM) 17 . These metabolic and physiological responses produced by strength exercise 37 have been identified as synonymous with fatigue 17,32,33 .
However, it is not yet fully established if these fatigue indicators always produce a decrease in performance 26 . That is why there is a need to establish whether indicators of muscle fatigue are constantly associated with a decrease in performance. As a result of the above, the objective of this systematic review was to review and analyze the studies existing between January 2009 and January 2019 that have used indicators of muscle fatigue established in the search terms during and after strength training as measurement variables. As a secondary objective, the programs were described, establishing the biochemical and physiological responses reported in each of the studies consulted.

Bibliographic search
The literature search was performed in accordance with the guidelines for the Preferred Reporting Items for Systematic Reviews and Meta-Analyses (PRISMA) 38 . The title, abstract, and keyword search fields were searched in each of the databases. The following keywords combined with Boolean operators (AND/ OR) were used: (["Ammonium" OR "Ammonium lactate" OR "Lactic acid" OR "Lactate" OR "Acid-base equilibrium" OR "Acid-base balance" OR "Heart rate" OR "Muscular fatigue" OR "Muscle fatigue" OR "Ratings of perceived exertion" OR "RPE scale"] AND ["Sports performance" OR "Athletic performance"] AND ["Strength training" OR "Resistance training" OR "Force training" OR "Concurrent training" OR "Isometric training" OR "Isokinetic training" OR "Concentric training" OR "Eccentric training" OR "Velocity based training" OR "Complex training" OR "Contrast training"]). Each of the keywords related to the methods of fatigue and force had the purpose of broadening the search. Two authors searched and reviewed the studies, both of whom decided whether the inclusion of studies was appropriate. In case of disagreement, a third author was consulted. The search strategy and study selection are presented in Figure 1.

Inclusion criteria
The importance of each study was evaluated according to the following inclusion criteria: a) experimental study design; b) healthy subjects of both genders; c) studies with strength training protocols; d) studies reporting indicators of muscle fatigue through ammonia, lactate, pH, HR, muscle fatigue and perception of effort; e) those with increased or decreased performance post-intervention, and f) studies published in English, Spanish, French, Portuguese or German. Studies that did not meet the inclusion criteria were excluded. Discrepancies found were resolved by consensus of the investigators.

Evaluation of methodological quality
The Physiotherapy Evidence Database (PEDro) scale 39,40 was used to assess study quality. The classification was based on three criteria: selection (maximum three stars), comparability (maximum three stars), and results (maximum four stars). Articles scoring eight to ten were considered to be of high methodological quality, four to seven moderate, and less than four low. Thus, the score obtained by the articles according to the PEDro scale indicated that 13 studies obtained a high score and 26 articles obtained a moderate score (Table 1).

Selected studies
The electronic search identified 3468 articles, of which 1952 were duplicated. The remaining 1516 articles were filtered by titles and abstracts, leaving 92 articles for full reading and analysis. After reviewing the 92 articles, 53 were removed, all for not meeting the inclusion criteria. By not including articles after a citation-oriented search, a total of 39 articles were obtained for a systematic review. These articles were stratified according to the protocol used: (i) plyometric training, (ii) Bodypump® training, (iii) occlusion training, (iv) variable resistance training, (v) conventional strength training, (vi) eccentric strength training, (vii) rest times in strength training and (viii) concurrent training.
At the end of the review, there was evidence from studies showing that strength training induces muscle fatigue as a result of physiological and biochemical responses related to strength training. Only those studies that related strength training to indicators of muscle fatigue are presented below ( The lifting protocol was 10 x 5-speed squats at 70% of the mass of the system (1RM) with rest intervals of 2 minutes between sets.
[La] = ↑ (p < 0.05) on SJ jump and maximum isometric force. To assess the effects of 12 weeks of the Bodypump® training program on neuromuscular aspects and metabolic variables, such as HR and lactate.

Body-pump®
Exercises for the upper extremities were performed using 1 kg weights. Squatting and ramming exercises were performed using weights corresponding to 10% of 1RM for the occupants (~ 5 kg). A straight metal bar (1 kg) and 1, 2, and 5 kg weights were attached to the bar and used during lower extremity exercises.
[La] and HR were ns.
Effects of heavy-duty training and its relationship between power loss and EMG rates and blood metabolite concentrations on exercise-induced dynamic fatigue

Strength training
Five series, with the load corresponding to 10 RM on the leg press with 120 s of rest between the series. After training, each subject performed an acute load resistance protocol with the same relative load (10 RM) as in the pre-workout test protocols.
[ Bench press and squat with overload Two leg press loads, separated by one week, consisting of 15 sets of 1 maximum repetition (MAX) and 5 sets of 10 maximum repetitions. [

Discussion
At the end of the systematic review and based on the main objective that sought to find evidence of alterations in muscle fatigue indicators during and after strength training, 39 studies were found between January 2009 and January 2019. Of which only In 4 there was evidence of increased performance despite having indicators of altered muscle fatigue. This may be due to the normal physiological response of the subjects. This evidence allowed us to visualize that there were protocols for the development of strength that generate alterations in muscle fatigue markers, such as [La], HR, RPE, DOMS, the variation of MR and ammonium. This shows that there are force protocols that, according to their characteristics, impact, and difficulty, should only be performed in some types of populations. Therefore, and for a better understanding, the different protocols for the development of strength and the changes they generate in muscle fatigue markers will be stratified separately.

Plyometric training and muscle fatigue
Drinkwater et al. 14 , following an acute plyometric exercise intervention in recreational rugby players, observed significant decreases in maximum voluntary contractions (MVC) (p < 0.05) and torque development rate (p < 0.01), triggering peripheral fatigue and resulting in decreased performance. Skurvydas et al. 18 , using plyometrics in physically active male students, recorded that the strength of MVC decreased significantly after two continuous series of high-intensity jumps (p < 0.05), while the DOMS increased significantly (p < 0.05). Similarly, Brown et al.16 also showed increases in HR and [La] after an acute plyometric session in recreationally trained men and women (p < 0.05), and these components have been considered on several occasions as precursor variables of fatigue 17 .
Kamandulis et al. 30 , after nine sessions of plyometric intervention in physically active athletes, reported that increases in jumping training load lead to an increase in muscle fatigue markers, thus suppressing acute mechanical function after exercise; however, after three weeks of training and adequate recovery, an increase in overall muscle performance was observed. In this sense, it has been observed that between plyometric exercise sessions, and for adequate recovery, there must be a 72-hour rest period. In this way, alterations in muscle fatigue indicators 17,41 can be reduced, leading to performance 14 .
Chatzinikolaou et al. 17 showed that an acute session of plyometrics in healthy men, with a pause of 2 minutes between series (5 series of 10 repetitions) and 5 minutes of rest between jumping of obstacles and jumps with a fall from a plyometric box, can induce a substantial decrease in jump performance resulting from increases in [La] (p < 0.001), as well as substantial alterations in blood biomarkers of muscle damage (BSDM) such as CK, cortisol, uric acid, and C-reactive protein (p < 0.05). These variables were directly related to muscle damage up to 72 hours after the intervention. These findings are similar to those found by Thomas et al. 41 , who state that plyometric exercises require 72 hours to decrease exercise-induced levels of muscle fatigue.

Bodypump® Training and Muscle Fatigue
The Bodypump® is a methodology that consists of training with bars, occupying loads ranging from 45-60 minutes with a standardized sequence of music 26 . This program has shown to be effective in improving maximum strength and muscular endurance of the lower extremities in untrained women 27 . In this sense, in research carried out by Greco et al. 27 , there was no evidence of increases in [La] or HR after 12 weeks of training in sedentary women (p > 0.05). On the other hand, Oliveira et al. 26 , after an acute Bodypump® intervention, showed significant increases in [La] and HR (p < 0.05); variables considered as precursors of muscle fatigue 17 . However, Oliveira et al. 26 stated that there was no significant correlation between the electromyographic activity of the muscle and the [La] and HR. Although Bodypump® training produces acute fatigue 26 , this would be sufficient to increase the maximum strength and muscular endurance of the lower extremities in untrained subjects 26,27 .

Training with occlusion and muscle fatigue
In recent times, low load training with occlusion has attracted the attention of trainers as both a possible alternative to high endurance exercises in the context of rehabilitation 20 and a training method to increase muscle strength and hypertrophy 21 . In this sense, Okuno et al. 21 indicated that training with occlusion appears to be more favorable than traditional force training without occlusion 12,25 . Similarly, Curty et al. 42 concluded that training with occlusion in trained men had preventive effects on indicators of muscle fatigue and indirect responses induced by eccentric exercise. Therefore, training with occlusion would produce less metabolic stress 21,42 . Even training with occlusion would be recommended as a training method in those subjects who present with cardiovascular problems and who cannot perform strength exercises over 80% of 1RM 21 . Sieljacks et al. 43 mentioned that training with occlusion without reaching muscle failure in repetitions in untrained subjects allows for increases in muscle size and muscle function, while it also implies lower RPE, discomfort, and less appearance of DOMS. However, unlike the findings reported by Okuno et al. 21 , Curty et al. 42 , and Sieljacks et al. 43 , Poton, Polito 22 established that healthy, trained subjects who undergo occlusion training may have muscle fatigue due to the increase in [La], as well as an increase in RPE (p < 0.05).
In addition to what was previously reported by Poton, Polito 22 , there is a study conducted by Almeida et al. 23 . These researchers obtained a higher level of fatigue after the application of a force with the occlusion method; this fatigue was associated with increases in [La] and with increases in BSDM indicators, such as CK and lactate dehydrogenase (p < 0.05), as well as higher values in the fatigue index when compared to a traditional force method in subjects with experience in strength training. Therefore, these BSDMs would have a direct relationship with the increase in muscle fatigue indicators 17,23 . However, more studies are needed that can clarify the use of occlusive methods on indicators of muscle fatigue and sports performance. Each of the occlusive protocols analyzed in this review used a 1-minute pause between series.

Variable resistance and muscle fatigue training
Variable resistance (RV) corresponds to the change of intensity during the application of force training load, within the various variable resistances are intra-variable resistance, intra-repetition variable resistance, and intra-series variable resistance 44 . Some types of VR have reported increases in the indicators of muscle fatigue and inflammation in both athletes and sedentary people, evidencing increases in the DOMS and [La] 24 . On the other hand, VR protocols cause general and local fatigue in military athletes that is related to the increase in [La] (p < 0.001) and decreases in average power (p < 0.002) 1 . However, unlike the muscle fatigue reported by Ojeda et al. 1 , these same authors in other research did not report increases in muscle fatigue indicators after a VR protocol. This would allow inferring that the athletes were in an anabolic process and without the presence of muscle fatigue, reflecting an increase in explosive strength using a grenade throw 29 .

Conventional strength and muscle fatigue training
This type of training has been used over the years occupying high volume load protocols (muscular endurance) 45,46 , high-intensity exercises (maximum strength) 47,48 , or muscular hypertrophy programmes 12,13 . In this sense, it has been reported that high volume muscle endurance training performed at a low-intensity of 1RM increases DOMS levels in healthy sedentary subjects (p < 0.05), regardless of whether it is performed with short intervals (1 minute) or long intervals (3 minutes) of rest between series 36 . Similarly, Hardee et al. 35 , showed that high-volume power clean exercises, performed at low intensity on trained subjects, increase the RPE independent of rest time between series (p < 0.05), which is directly related to a decrease in output power (p < 0.05). Likewise, Date et al. 15 showed a significant increase in [La] in physically active males (p < 0.05) after power clean training that considered a high load volume. Similarly, Rogatzki et al. 45 showed that a protocol of muscular resistance, when compared with a protocol of hypertrophy and maximum strength, significantly increased the blood levels of ammonium and lactate in adolescents (p < 0.05). These findings are consistent with other research that reported muscle fatigue following the use of high volume, low-intensity loads 15,35,36 . In another study developed by Silva et al. 47 , it was concluded that acute interventions with high-intensity strength exercises (5RM) produce neither alterations in [La] nor increases in RPE. Therefore, an acute session of 4 series of 5RM could enhance performance in cyclists 47 .
On the other hand, Nicholson et al. 13 showed increases in [La] in maximum strength and hypertrophy programs in trained subjects (p < 0.001), while Walker et al. 12  physically active subjects (p < 0.05). However, Bartolomei et al. 49 , after comparing two strength protocols (high load volume versus high intensity) in subjects with strength experience, concluded that high volume training induces greater muscle fatigue due to the increase in [La]. Thus, endurance training up to muscle failure significantly reduces metabolic recovery and hormonal homeostasis 24-48 hours after exercise 50 . Likewise, Andreatta et al. 48 showed increases in [La] after the application of a high-intensity force protocol (80% of 1RM) in healthy subjects with strength experience. On the other hand, Silva et al. 47 showed no increase in [La] after a high-intensity protocol. Bartolomei et al. 49 also showed that the high-volume protocol generates greater muscle fatigue than a high-intensity protocol. This may be associated with the number of repetitions since Bartolomei et al. 49 evaluated only 3 repetitions versus 10 repetitions performed in the Andreatta et al. 48 protocol. The latter protocol could be considered a high-volume protocol 15 . Therefore, strength training up to muscle failure produces significant increases in metabolic stress, with greater muscle fatigue in the subjects who practice it 46 . This is why the large decreases in mechanical performance together with the high metabolic stress suggest a lower use of force protocols with high volume 46,51 .
In conventional strength protocols, BSDMs also have a close relationship to increased indicators of muscle fatigue. In this sense, Bartolomei et al. 49 , along with evidence of an increase in muscle fatigue indicators ([La]), also observed alterations in CK, cortisol, and IL-6 (p < 0.001) in high-volume training, which is possibly associated with post-exercise muscle damage. Other research also reported alterations in both fatigue indicators 28,34 and BSDM after high volume training 34 . Therefore, a direct association between indicators of muscle fatigue and muscle damage, along with decreased performance, would discourage high-volume strength protocols. 6. Eccentric strength and muscle fatigue training Both high-intensity and low-intensity eccentric exercises have been shown to produce muscle fatigue, resulting in decreased strength and therefore decreased performance 52 . In this sense, Fernandez-Gonzalo et al. 25 , after a first eccentric training session, showed significant increases in the [La] in the group of healthy and physically active males; however, these same variables after 15 sessions did not present alterations, so a muscular adaptation to the eccentric training was inferred. Gauche et al. 52 reported that the maximum voluntary contraction was significantly reduced after eccentric exercise in the biceps (p < 0.01), by 20% after high-intensity exercise and by 25% after low-intensity exercise in healthy untrained subjects. These voluntary maximum contraction values remained reduced after 48 hours for both high-intensity and low-intensity exercise (p < 0.001). These results are similar to conventional strength training in which low-intensity strength sessions have found to induce an increase in muscle fatigue 49 and a decrease in performance 48 . Finally, alterations in the BSDM continue to be directly related to markers of muscle fatigue; thus, Fernandez-Gonzalo et al. 25 , along with evidence of increases in the [La], also presented alterations in blood CK.

Different times of rest in the training of strength and muscular fatigue
It has been established that strength training for 6 consecutive days induces significant alterations in DOMS, stress, and perceived recovery, which is directly related to a decrease in 1RM, thus inducing muscle fatigue in both men and women 53 . Also, DOMS levels have been reported to increase significantly (p < 0.05) with either short 1-minute rest intervals or long 3-minute rest intervals between series 36 . Paulo et al. 54 indicated that a 1-minute break between series results in greater production of average power in exercise sessions aimed at developing muscle power in healthy young people. However, Miranda et al. 55 , in the context of neural activation, stated that a 3-minute rest interval between series may represent a neuromuscular window between a state of fatigue and a state of the total recovery in trained women. These same researchers examined the effect of the different recovery periods (24,48, and 72 hours) between sessions of strength training using press banking in trained subjects. At the end, they concluded that a recovery period of only 24 hours induces an increase in [La] and RPE (p < 0.05) 56 , variables that are considered as indicators of muscular fatigue 35 and that are directly related to the decrease in performance 48 . When comparing the kinematic, metabolic, endocrine, and perceptual responses of three overloaded squatting protocols in trained subjects, Tufano et al. 57 concluded that muscle fatigue occurs by increasing [La] and RPE, regardless of the organization of rest time used. Thus, Ammar et al. 58 showed increases in [La] and RPE (p < 0.01) in weightlifters. These findings were independent of training schedules during the day (morning, afternoon, or night), and BSDM continued to be elevated after 48 hours of recovery (p < 0.05). Thus, [La] and RPE have also been altered in other studies 12,17,36,59 and declared as precursors of muscle fatigue 17 .
In general terms, and based on the systematic review, it is suggested that strength sessions be separated by 72 hours to reduce exercise-induced muscle fatigue levels 41 . Finally, Ammar et al. 58 and Tufano et al. 57 also showed an increase in BSDM simultaneously with increases in muscle fatigue indicators, so this history continues to demonstrate a close relationship between muscle fatigue indicators and BSDM.

Concurrent training and muscle fatigue
In this type of training, Taipale et al. 59 showed significant increases (p < 0.05) in [La] after a resistance run intervention followed by a strength protocol or vice versa in both trained men and women, but also showed increases in CK concentrations. This last variable can play a determining role in the decrease of strength production capacities during recovery 12,17,36,59 . On the other hand, not all research 60 has shown an increase in variables that induce fatigue and muscle damage after a concurrent protocol. Johnston et al. 60 only reported an increase in [La] and not BSDM after each speed protocol followed by strength training, but not when strength was trained and then speed. Due to the lack of evidence, more studies are needed to address the variables involved, and thus clarify the order of exercises at the time of concurrent training and mitigate possible decreases in performance in athletes.

Conclusions
At the end of the systematic review, it was shown that the different training methodologies for strength development generate increases in muscle fatigue indicators, and the increase generated in the different muscle fatigue indicators depends both on the methodology used and on the type of population, sex, level of training and type of sport.
At the same time, it became evident that there are different ways of quantifying fatigue in strength training. Among the most commonly used fatigue indicators are [La], HR, RPE, DOMS, MR variation, and ammonium. The most-reported indicators are [La], HR, and RPE. Finally, considering that more studies are still needed to determine the real effect of these training methods on fatigue indicators, and in light of the facts, there are indications that plyometric training, training with variable resistance and conventional strength training with high volume loads are the ones that could incur the greatest increase in muscle fatigue.

Limitations
One limitation of the study is to a lack of homogeneity associated with the study outcomes, study design, and time points of follow-up across the studies, they do not allow to perform a meta-analysis.

Practical Applications
Based on the results of the systematic review, and to minimize muscle fatigue levels, increasing load volumes, and enhancing athlete performance, some considerations for stratified methods are presented: 1. Plyometric training: As it has a great impact, it should be applied to athletes capable of lifting twice their body weight in a squat. It is also suggested that the pause between series should be greater than 2 minutes and there should be a minimum of 72 hours between sessions. Although an indicator of fatigue for this method is the impossibility of reaching the training heights established for athletes, [La] was used as an indicator of fatigue in most of the research consulted.
2. Bodypump® training: This methodology can be applied to non-physically trained subjects, while the most reported fatigue indicators are HR and [La].
3. Training with occlusion: This type of protocol can be used in both trained and untrained subjects. In most of the investigations consulted, they used a 1-minute pause between series. This pause triggered increases in muscle fatigue indicators in some studies. As a result, new research is suggested to clarify the optimal pause time between series, while the suggested fatigue indicators are perceived DOMS, RPE, and [La].
4. Variable endurance training: This type of protocol should be aimed at athletes, being discouraged in physically inactive subjects. Although it is important, in order to establish the pause, to consider the variation of the intensity within the series, pauses of 15 seconds are suggested. The fatigue indicators with the greatest evidence are perceived DOMS and [La].
5. Conventional strength training: This type of protocol can be used in inactive subjects as well as athletes. However, and with the purpose of mitigating muscular fatigue alterations, it is suggested to avoid high volume loads, privileging high-intensity sessions. It is recommended that the pause time between series be greater than 3 minutes and the rest between each session should be around 72 hours, while the suggested fatigue indicators are RPE, DOMS perceived, and [La].
6. Eccentric training: This type of protocol should be used in physically active subjects. Evidence showed that high-intensity executions have less alteration in muscle fatigue indicators, but more studies are needed to determine the effect of these protocols on fatigue indicators. However, the suggested rest time between each session should be around 72 hours, while the suggested fatigue indicators are [La].
7. Different rest times in strength training: This section suggests starting with strength protocols that include a minimum break of 3 minutes between sets, and then generating individualized guidelines for each strength protocol. However, the 72 hours of rest between each session are independent of the type of strength training, while the fatigue indicators are [La] and RPE.
8. Concurrent training: this type of protocol should be occupied by trained subjects. After the review, it is suggested to first train strength exercises and then speed exercises, but more evidence is needed to clarify the order of execution of concurrent training. Finally, the fatigue indicators used for these protocols are [La].