Effects of upper body concurrent training in trained individuals: a review

(1)

Effects of upper body

concurrent training in trained individuals: a review

Björn Hansson

Självständigt arbete/idrottsvetenskaplig magisteruppsats,

15 högskolepoäng

(2)

Datum: 31-05-2017 Handledare: Peter Pagels Examinator: Jesper Augustsson

(3)

(4)

Abstract

Concurrent training (CT) is defined as the development of both endurance and strength within the same exercise program. CT has been studied for decades, but the results has been diverse.

However, very few have studied the effects of CT on the upper body musculature. Hence, this review set out to investigate the effects of combined strength and endurance training (ET) of the upper body on muscle hypertrophy, muscle strength and endurance variables. PubMed was searched with relevant search terms with varying combinations, such as concurrent training, combined strength and endurance training. After scanning the literature, a total of eight articles were included. The results suggest that muscle strength, exercise economy and time to exhaustion can effectively be improved by CT of the upper body. The effect of CT on upper body musculature were unclear. Some of the articles included suggests a decrease in whole body lean mass, which might simply be due to insufficient loading of the lower body musculature.

In order to maintain muscle mass during a CT protocol, endurance athletes should aim to perform ST which targets muscles active during ET. However, the limited empiric literature avail- able on CT of the upper body makes a conclusion hard to draw. This review shows that CT of the upper body is yet an unexplored and researchers should further investigate the effects of CT for the musculature of the upper body alone. If we gain more knowledge of the effects from concurrent training of the upper body, it could have several implications, both clinically and in a sport setting.

Nyckelord: Concurrent training, upper body, strength, endurance, combined train- ing

(5)

Table of content

1. Bakgrund 1–5

1.1 Concurrent training 2

1.2 Molecular basis of the interference effect 2

1.3 Concurrent training and endurance athletes 3-4

1.4 Concurrent training of the upper body 4

2. Syfte 6

3. Metod 7–8

4. Resultat 9–10

5. Diskussion 11–12

6. Referenser

(6)

1. Background

Athletes participates in a number of different sports that places different types of stress on the cardiovascular and musculoskeletal-system. For example, the marathon runner has to be able to work on a high percent of their individual VO2max for an extended period of time. On the other hand, the powerlifter has to be able to produce as much force as possible in one single repetition. Team sport athlete are often required to possess both power and endurance, due to repeated bursts and short rest periods between these. Also, due to recent research, endurance athletes and coaches are beginning to discover the benefits of developing strength and power on top of their regular endurance training regimen. Moreover, both strength training (ST) and endurance training (ET) is important in the prevention of several disorders which might impact physical capacity and metabolic health, such as sarcopenia (Pijnappels et al. 2008), diabetes type-II, and obesity (Kelley et al. 2002; Morino et al. 2005). Thus, in order to draw benefits from both to train ST and ET, these has to be trained simultaneously in certain periods of a training protocol Thus, the term concurrent training (CT) defines the development of strength and endurance concurrently within the same exercise program, on the same workout or separated by hours or days (Leveritt et al. 1999).

The adaptions to regular ST and ET are in general different. ST in conjunction with essential amino acids turns the muscle protein balance positive, thus increases the storage of protein in the body and results in hypertrophy. Specifically, traditional ST usually increases the cross- sectional area and number of myofibrils of the fast-twitch type II muscle fiber. The increase in force production after ST is partly due to the increased size of the skeletal muscle, however neurological changes are equally important (Erskine et al. 2014). ET induces a number of central and local adaptions to the human muscle. Central adaptions to the heart leads to an increased cardiac output, the most important contributor to the increased maximal oxygen uptake (Ekblom 1968). Local adaptions to the muscle includes; increases in oxidative enzyme activity, increased capillary density and mitochondrial number and/or volume (Hawley 2002).

(7)

1.1 Concurrent training

The first ever scientist to study CT was Dr. Hickson at the University of Illinois. In his study (Hickson 1980), subjects were divided into three groups that trained either ST, ET or CT for 12 weeks. The CT group eventually saw a decline in strength during the 9-10th week, in contrast to the ST group who increased strength over the course of the whole study. These results have later been corroborated by a number of studies (Dudley and Djamil 1985; Hunter et al.

1987). Moreover, a number of studies suggests that CT might attenuate power output and hypertrophic development in the type I muscle fiber (Kraemer et al. 1995; Bell et al. 2000; Putman et al. 2004). Also, some studies published more recently show that CT might attenuate muscle growth and strength (Jones et al. 2013; Rønnestad et al. 2012; Chtara et al. 2008). Although several articles reported of an interference effect on the development of strength and muscle hypertrophy, there has been contradictory findings as well (Sale et al. 1990; McCarthy et al.

1995; Hendrickson et al. 2010; Shaw et al. 2009; Wilson et al. 2012). Interestingly, Lundberg et al. (2013) and Kazior et al. (2016) showed an increase in muscle cross-sectional area among subjects after CT was compared to ST.

1.2 Molecular basis of the interference effect

As previously described, ET and ST induces different responses and adaptions. Naturally, the signaling events preceding these divergent adaptions are also different. The mammalian target of rapamycin (mTOR) has been identified as a key mediator to muscle growth through an up regulation of protein synthesis after ST (Baar & Esser 1999; Terzis et al. 2007). Protein synthesis regulates the amount of muscle protein stored in the body. During ET, the upregulation of amp-activated protein kinase (AMPK) strongly regulates the activation of coactivator pe- roxisome proliferator-activated receptor-gamma coactivator 1 alpha (PGC-1a), an important regulator for mitochondrial biogenesis (Hardie et al. 2012). However, the molecular signaling from a single exercise mode might not be as exclusive as previously suggested. For example, two studies (Mascher et al. 2007; Mascher et al. 2011) have suggested that endurance exercise alone can increase mTOR signaling and protein synthesis. Also, a number of other studies has shown an increase in AMPK signaling from resistance exercise alone (Dreyer et al. 2006;

Vissing et al. 2013).

Although many authors have suggested an interference effect, little is known about the orches- trating mechanism. More recent research has studied the acute molecular response in an attempt to explain possible mechanisms behind the interference effect. Some of the first studies that

(8)

was published (Atherton et al. 2005; Bolster et al. 2002) suggested that, as previously mentioned, endurance training mainly activates AMPK. In turn, results suggest that this activation might inhibit the signaling cascade leading down to the activation of mTOR and thus protein- synthesis. However, this work originated from separated rat-muscle. A number of following studies have investigated the acute molecular response to CT in human subjects and results are equivocal. Coffey and his group (2009a; 2009b), studied both high intensity and prolonged medium intensity workouts in combination with ST with the same study design. Both of these studies suggest that CT may alter the acute anabolic signaling. However, several other studies reports no difference (Carrithers et al. 2007; Donges et al. 2012; Apro et al. 2013; Fernandez- Gonzalo et al. 2013) or even elevated anabolic molecular signaling (Lundberg et al. 2012; Pugh et al. 2015; Kazior et al. 2016) to CT compared to ST only. However, the isolation of AMPK as the key signaling molecule for the interference effect of ST is too simplistic, since there are many more key regulators for muscle metabolism that can interfere with signaling from ST.

Possible other mechanisms are discussed in detail elsewhere (Baar 2014; Murach and Bagley 2016).

There are a number of variables among the previously mentioned studies that likely have affected the diverse results. These will now be discussed briefly. For example, the response to muscle contractions in skeletal muscle among untrained subjects may lead to a global molecular signaling. In trained subjects, however, the molecular response will be more refined de- pending on what type of exercise the individual is accustomed with (Fernandez-Gonzalo et al.

2013). In a meta-analysis from Wilson and colleagues (2012) it was reported that the duration and frequency of endurance training in a CT protocol negatively correlates with hypertrophic and strength adaptions. Robineau et al. (2016) suggests that no less than 6 hours should separate the exercise modes to obtain optimal adaptions from CT. The individual training response may also differ among individuals (Hubal et al. 2005). According to a recent review (Mann et al.

2014), hereditary factors may account for up to 50 % of the differences in the baseline state and 47 % of the increase in Vo2 max after a training intervention. Finally, practical recommen- dations for CT are proposed elsewhere (Murach and Bagley 2016; Baar 2014).

1.3 Effects of concurrent training on endurance performance

ST for endurance athletes was for a long time controversial among coaches. Many endurance sports are so called “weight-bearing”, which implies that a higher total body weight will limit performance since the movement will be require more energy. The notion has been that ST will

(9)

increase the body weight of the athlete, thus limit endurance performance through increased cost of movement. Although ST has the potential to increase muscle mass, individual training variables such as volume, number of repetitions and intensity can alter the response away from hypertrophy. Emerging over the past decade, a number of studies have reported of increased chronic endurance performance, both long-term and short-term, when ST is added to an ET protocol (Paavolainen et al. 1999) (Millet et al. 2002) (Støren et al. 2008). These changes are most likely linked to an increased economy of movement (reduced cost), muscle tendon-stiff- ness and a number of neural adaptions (Rønnestad and Mujika 2014). Although one study has reported of an altered acute molecular response to ET when ST and ET was performed within the same training session (Coffey et al. 2009b), another study (Wang et al. 2011) reported of an augmented response to ET when ST were performed after a bout of low-intensity ET.

1.4 Concurrent training of the upper body

Despite decades of research on CT, very few have studied the effects of CT on the upper body musculature. Skeletal muscle has a number of different responsibilities due to their location on the body. Also, the percentage of the different muscle fibers (slow-twitch and fast-twitch) vary among muscles. The arm muscles have a higher percentage of type-II fibers, rely more heavily on carbohydrate utilization and extract less oxygen during exercise (Calbet et al. 2005; Helge 2010; Van Hall et al. 2003). Moreover, some studies suggest that there might be a difference in the adaption to ST in the muscles of the upper and lower body. It was reported in a review from Wernbom with collagues (2007) that there is an inverted u-curve relationship between volume on each exercise session and the hypertrophic response. Interestingly, Wernbom and his research group documented that the muscles of the upper body seem more sensitive to a higher volume, and the decrease in the hypertrophic response comes earlier compared to muscles of the lower body. Similarly, results documented in another study by Rønnestad et al.

(2007) suggests that muscles of the lower body had a higher increase in both strength and hypertrophic response when three sets were performed compared to a single set, in contrast to the muscles of the upper body that showed no difference. Thus, when comparing the muscles of the upper body to the muscles of the lower body, a better resilience towards high volume seem to be evident in the latter.

It’s evident that both ST and ET are important for athletes participating in a wide range of sports and that they’re equally important among the general population to prevent disease and improve daily functions. However, due to the low number of studies investigating the effects

(10)

of concurrent training in the upper body musculature, further attention should be directed towards this field of research.

(11)

2 Purpose

This review set out to investigate the chronic adaptions in the upper body from strength and endurance training when these are trained concurrently. More specifically, the chronic effect on muscle mass, strength and endurance adaptions were studied.

(12)

3 Method

PubMed (www.ncib.nlm.nih.gov/pubmed) were searched from March until the 15^th of April 2017 (Figure 1). Articles had to be published on original scientific investigations. Search terms included a variation of the following keywords ‘concurrent training’, ‘combined strength and endurance training’, ‘rowing’, ‘cross-country skiing’, ‘double poling’, ‘resistance training’,

‘upper-body’. The name of the authors of some articles were also used in the search. Further, reference lists of articles were used to find other relevant articles.

Figure 1.Flow diagram.

(13)

Search criterias were (I) published in a peer reviewed English journal, (II) studies must refer to the chronic effect on ST variables and/or ET variables (e.g Strength, Muscle-mass, Vo2 Peak, Exercise economy) of concurrently training endurance and strength training for the upper-body.

(14)

4 Results

Eight studies were included. Together, the articles included a total of 164 participants, 149 among these were trained athletes and 15 were trained subjects.

There was a positive effect on muscle strength among subjects in the CT protocols, with seven out of 8 studies showing improvements in 1RM and isokinetic strength (Table 1). Moreover, five out of 8 studies showed improvements on endurance variables such as exercise economy and time to exhaustion (TTE) among CT groups. Few studies investigated the effects of CT on hypertrophic development of the upper body. Moreover, in the total three included, the results varied, making it hard to draw any conclusions.

(15)

Table 1. ET = Endurance training; ST = Strength training; CT = Concurrent training; C = Control, 1 RM = 1 Repetition-maximum; 4RF = 4 exercises leading to voluntary failure; 4RNF = 4 exercises not leading to voluntary failure; 2RF = 2 exercises leading to voluntary failure, FFM

= Fat-free mass; Muscle-CSA = Cross sectional area of the muscle fibres LBM = Lean body mass; HLLR = High-load low repetition training;

LLHR = Low-load high repetition training

(16)

5 Discussion

This review set out to investigate the chronic adaptions in the upper body to CT. The biggest challenge of this review was the limited empirical material. For example, only one study (Ab- ernethy and Quigley 1993) investigated CT for the upper body alone. Except for this study, all of the studies had subjects that performed ET that also involved the lower body musculature ET only. Furthermore, Abernethy and Quigley were the only authors that compared CT to a control group that performed ST and not ET.

The difference between the musculature of the upper body and the lower body was previously briefly described, with differences in fiber type distribution, adaptions to training and the resilience towards training volume. Some further interesting evidence arose from one of the studies used in this review. Abernethy and Quigley (1993) studied CT and found no interference in isokinetic strength development on any contracting speed in the elbow extensor. In contrast, Dudley and Djamil (1985) documented a decreased isokinetic strength development in the knee extensors and documented that high contracting speeds were affected negatively in the CT group. This would suggest that the pattern of strength development is different in the elbow and knee extensor.

As expected, upper body ST increased strength in the CT groups compared to ET only. Inter- estingly, there were some contradictory findings in the increase of muscle mass among subjects in the CT groups. For example, one study (Losnegard et al. 2011) found a trend towards greater increases in muscle CSA of the m. triceps brachii in the CT group compared ET group. In regard to hypertrophic development of the upper body, no differences were found in the increase of lean body mass (LBM) between CT and ET. Interestingly, results of two studies (Izquierdo-Gabarren et al. 2009; Losnegard et al. 2011) suggest a reduction in total LBM. Since subjects were trained athletes, one important variable that might explain the diverse findings is that the molecular responses to un-accustomed training in athletes might be insufficient to induce a chronic adaption in the specific muscle phenotype (Fernandez-Gon- zalo et al., 2013). Moreover, another possible explanation is the lack of proper ST for the

(17)

lower body in these studies and that ET alone might be insufficient to maintain lower body musculature.

Gaining more knowledge of the effects from concurrent training of the upper body can have several implications, both clinically and in a sport settings. Physical training is very important to the society of today. Not only for athletes seeking to compete at the highest possible level, but also for sedentary individuals who wants a healthy lifestyle. Some individuals are from birth or through unfortunate events bound to sit in a wheelchair, for life or through periods of their life. Physical training might become a tough and gruelling task for this population since exercise selection and modality are limited to upper body. Thus, gaining the most out of the time invested into training could aid these towards a healthier lifestyle.

Many sports require the development of endurance and strength concurrently, not only for the muscles of the lower body but also the upper body musculature (e.g rowers, cross-country skiers). A certain group that might be overlooked in the research on this area is wheelchair athletes. These individuals are competing in team sports in that require, similar to their able- bodied counterparts, explosive but yet fatigue resistant musculature. Complementing the literature with data of the upper body will certainly aid coaches in training planning, but also fill the theoretical gap in the research of concurrent exercise.

Moreover, the results of this review also suggest that endurance athletes should perform ST in order to maintain muscle mass during a ET protocol and aim to target muscle mass involved in the endurance performance. Further, this review shows that CT of the upper body is yet an unexplored area and researchers should investigate the effects of CT for the musculature of the upper body alone.

(18)

6 References

Abernethy, P.J., Quigley, B.M., 1993. Concurrent Strength and Endurance Training of the El- bow Extensors: J. Strength Cond. Res. 7, 234–240.

Apro, W., Wang, L., Ponten, M., Blomstrand, E., Sahlin, K., 2013. Resistance exercise induced mTORC1 signaling is not impaired by subsequent endurance exercise in human skeletal muscle. AJP Endocrinol. Metab. 305, E22–E32.

Atherton, P.J., Babraj, J., Smith, K., Singh, J., Rennie, M.J., Wackerhage, H., 2005. Selective activation of AMPK-PGC-1alpha or PKB-TSC2-mTOR signaling can explain specific adaptive responses to endurance or resistance training-like electrical muscle stimula- tion. FASEB J. Off. Publ. Fed. Am. Soc. Exp. Biol. 19, 786–788.

Baar, K., 2014. Using Molecular Biology to Maximize Concurrent Training. Sports Med. 44, 117–125.

Baar, K., Esser, K., 1999. Phosphorylation of p70S6kcorrelates with increased skeletal muscle mass following resistance exercise. Am. J. Physiol.-Cell Physiol. 276, C120–C127.

Bell, G.J., Syrotuik, D., Martin, T.P., Burnham, R., Quinney, H.A., 2000. Effect of concurrent strength and endurance training on skeletal muscle properties and hormone concentra- tions in humans. Eur. J. Appl. Physiol. 81, 418–427.

Bolster, D.R., Crozier, S.J., Kimball, S.R., Jefferson, L.S., 2002. AMP-activated protein kinase suppresses protein synthesis in rat skeletal muscle through down-regulated mammalian target of rapamycin (mTOR) signaling. J. Biol. Chem. 277, 23977–23980.

Calbet, J. a. L., Holmberg, H.-C., Rosdahl, H., van Hall, G., Jensen-Urstad, M., Saltin, B., 2005. Why do arms extract less oxygen than legs during exercise? Am. J. Physiol.

Regul. Integr. Comp. Physiol. 289, R1448-1458.

(19)

Carrithers, J.A., Carroll, C.C., Coker, R.H., Sullivan, D.H., Trappe, T.A., 2007. Concurrent exercise and muscle protein synthesis: implications for exercise countermeasures in space. Aviat. Space Environ. Med. 78, 457–462.

Chtara, M., Chaouachi, A., Levin, G.T., Chaouachi, M., Chamari, K., Amri, M., Laursen, P.B., 2008. Effect of concurrent endurance and circuit resistance training sequence on mus- cular strength and power development. J. Strength Cond. Res. 22, 1037–1045.

Coffey, V.G., Jemiolo, B., Edge, J., Garnham, A.P., Trappe, S.W., Hawley, J.A., 2009a. Effect of consecutive repeated sprint and resistance exercise bouts on acute adaptive responses in human skeletal muscle. AJP Regul. Integr. Comp. Physiol. 297, R1441–R1451.

Coffey, V.G., Pilegaard, H., Garnham, A.P., O’Brien, B.J., Hawley, J.A., 2009b. Consecutive bouts of diverse contractile activity alter acute responses in human skeletal muscle. J.

Appl. Physiol. 106, 1187–1197.

Donges, C.E., Burd, N.A., Duffield, R., Smith, G.C., West, D.W.D., Short, M.J., Mackenzie, R., Plank, L.D., Shepherd, P.R., Phillips, S.M., Edge, J.A., 2012. Concurrent resistance and aerobic exercise stimulates both myofibrillar and mitochondrial protein synthesis in sedentary middle-aged men. J. Appl. Physiol. Bethesda Md 1985 112, 1992–2001.

Dreyer, H.C., Fujita, S., Cadenas, J.G., Chinkes, D.L., Volpi, E., Rasmussen, B.B., 2006. Re- sistance exercise increases AMPK activity and reduces 4E-BP1 phosphorylation and protein synthesis in human skeletal muscle: AMPK, muscle protein synthesis and resistance exercise. J. Physiol. 576, 613–624.

Dudley, G.A., Djamil, R., 1985. Incompatibility of endurance- and strength-training modes of exercise. J. Appl. Physiol. Bethesda Md 1985 59, 1446–1451.

Ekblom, B., 1968. Effect of physical training on oxygen transport system in man. Acta Physiol.

Scand. Suppl. 328, 1–45.

Erskine, R.M., Fletcher, G., Folland, J.P., 2014. The contribution of muscle hypertrophy to strength changes following resistance training. Eur. J. Appl. Physiol. 114, 1239–1249.

(20)

Fernandez-Gonzalo, R., Lundberg, T.R., Tesch, P.A., 2013. Acute molecular responses in untrained and trained muscle subjected to aerobic and resistance exercise training versus resistance training alone. Acta Physiol. 209, 283–294.

Hardie, D.G., Ross, F.A., Hawley, S.A., 2012. AMPK: a nutrient and energy sensor that main- tains energy homeostasis. Nat. Rev. Mol. Cell Biol. 13, 251–262.

Hawley, J.A., 2002. Adaptations of skeletal muscle to prolonged, intense endurance training.

Clin. Exp. Pharmacol. Physiol. 29, 218–222.

Helge, J.W., 2010. Arm and leg substrate utilization and muscle adaptation after prolonged low-intensity training. Acta Physiol. Oxf. Engl. 199, 519–528.

Hendrickson, N.R., Sharp, M.A., Alemany, J.A., Walker, L.A., Harman, E.A., Spiering, B.A., Hatfield, D.L., Yamamoto, L.M., Maresh, C.M., Kraemer, W.J., Nindl, B.C., 2010.

Combined resistance and endurance training improves physical capacity and performance on tactical occupational tasks. Eur. J. Appl. Physiol. 109, 1197–1208.

Hickson, R.C., 1980. Interference of strength development by simultaneously training for strength and endurance. Eur. J. Appl. Physiol. 45, 255–263.

Hubal, M.J., Gordish-Dressman, H., Thompson, P.D., Price, T.B., Hoffman, E.P., Angelopou- los, T.J., Gordon, P.M., Moyna, N.M., Pescatello, L.S., Visich, P.S., others, 2005. Var- iability in muscle size and strength gain after unilateral resistance training. Med Sci Sports Exerc 37, 964–72.

Hunter, G., Demment, R., Miller, D., 1987. Development of strength and maximum oxygen uptake during simultaneous training for strength and endurance. J. Sports Med. Phys.

Fitness 27, 269–275.

Izquierdo-Gabarren, M., González de Txabarri Expósito, R., García-Pallarés, J., Sánchez-Me- dina, L., Sáez de Villarreal E, S., Izquierdo, M., 2009. Concurrent Endurance and Strength Training Not To Failure Optimizes Performance Gains: Med. Sci. Sports Ex- erc. 1.

(21)

Jones, T.W., Howatson, G., Russell, M., French, D.N., 2013. Performance and neuromuscular adaptations following differing ratios of concurrent strength and endurance training. J.

Strength Cond. Res. 27, 3342–3351.

Kazior, Z., Willis, S.J., Moberg, M., Apró, W., Calbet, J.A.L., Holmberg, H.-C., Blomstrand, E., 2016. Endurance Exercise Enhances the Effect of Strength Training on Muscle Fiber Size and Protein Expression of Akt and mTOR. PloS One 11, e0149082.

Kelley, D.E., He, J., Menshikova, E.V., Ritov, V.B., 2002. Dysfunction of mitochondria in human skeletal muscle in type 2 diabetes. Diabetes 51, 2944–2950.

Kraemer, W.J., Patton, J.F., Gordon, S.E., Harman, E.A., Deschenes, M.R., Reynolds, K., Newton, R.U., Triplett, N.T., Dziados, J.E., 1995. Compatibility of high-intensity strength and endurance training on hormonal and skeletal muscle adaptations. J. Appl.

Physiol. Bethesda Md 1985 78, 976–989.

Leveritt, M., Abernethy, P.J., Barry, B.K., Logan, P.A., 1999. Concurrent strength and endurance training. Sports Med 28, 413–427.

Losnegard, T., Mikkelsen, K., Rønnestad, B.R., Hallén, J., Rud, B., Raastad, T., 2011. The effect of heavy strength training on muscle mass and physical performance in elite cross country skiers: Heavy strength training in cross country skiing. Scand. J. Med. Sci.

Sports 21, 389–401.

Lundberg, T.R., Fernandez-Gonzalo, R., Gustafsson, T., Tesch, P.A., 2013. Aerobic exercise does not compromise muscle hypertrophy response to short-term resistance training. J.

Appl. Physiol. 114, 81–89.

Lundberg, T.R., Fernandez-Gonzalo, R., Gustafsson, T., Tesch, P.A., 2012. Aerobic Exercise Alters Skeletal Muscle Molecular Responses to Resistance Exercise: Med. Sci. Sports Exerc. 44, 1680–1688.

Mann, T.N., Lamberts, R.P., Lambert, M.I., 2014. High Responders and Low Responders: Fac- tors Associated with Individual Variation in Response to Standardized Training. Sports Med. 44, 1113–1124.

(22)

Mascher, H., Andersson, H., Nilsson, P.-A., Ekblom, B., Blomstrand, E., 2007. Changes in signalling pathways regulating protein synthesis in human muscle in the recovery period after endurance exercise. Acta Physiol. 191, 67–75.

Mascher, H., Ekblom, B., Rooyackers, O., Blomstrand, E., 2011. Enhanced rates of muscle protein synthesis and elevated mTOR signalling following endurance exercise in human subjects: Protein synthesis after aerobic exercise. Acta Physiol. 202, 175–184.

McCarthy, J.P., Agre, J.C., Graf, B.K., Pozniak, M.A., Vailas, A.C., 1995. Compatibility of adaptive responses with combining strength and endurance training. Med. Sci. Sports Exerc. 27, 429–436.

Millet, G.P., Jaouen, B., Borrani, F., Candau, R., 2002. Effects of concurrent endurance and strength training on running economy and .VO(2) kinetics. Med. Sci. Sports Exerc. 34, 1351–1359.

Morino, K., Petersen, K.F., Dufour, S., Befroy, D., Frattini, J., Shatzkes, N., Neschen, S., White, M.F., Bilz, S., Sono, S., Pypaert, M., Shulman, G.I., 2005. Reduced mitochondrial density and increased IRS-1 serine phosphorylation in muscle of insulin-resistant offspring of type 2 diabetic parents. J. Clin. Invest. 115, 3587–3593.

Murach, K.A., Bagley, J.R., 2016. Skeletal Muscle Hypertrophy with Concurrent Exercise Training: Contrary Evidence for an Interference Effect. Sports Med. 46, 1029–1039.

Paavolainen, L., Häkkinen, K., Hämäläinen, I., Nummela, A., Rusko, H., 1999. Explosive- strength training improves 5-km running time by improving running economy and muscle power. J. Appl. Physiol. Bethesda Md 1985 86, 1527–1533.

Pijnappels, M., van der Burg, P.J.C.E., Reeves, N.D., van Dieën, J.H., 2008. Identification of elderly fallers by muscle strength measures. Eur. J. Appl. Physiol. 102, 585–592.

Pugh, J.K., Faulkner, S.H., Jackson, A.P., King, J.A., Nimmo, M.A., 2015. Acute molecular responses to concurrent resistance and high-intensity interval exercise in untrained skeletal muscle. Physiol. Rep. 3, e12364–e12364.

(23)

Putman, C., Xu, X., Gillies, E., MacLean, I., Bell, G., 2004. Effects of strength, endurance and combined training on myosin heavy chain content and fibre-type distribution in humans. Eur. J. Appl. Physiol. 92.

Robineau, J., Babault, N., Piscione, J., Lacome, M., Bigard, A.X., 2016. Specific Training Ef- fects of Concurrent Aerobic and Strength Exercises Depend on Recovery Duration: J.

Strength Cond. Res. 30, 672–683.

Rønnestad, B.R., Egeland, W., Kvamme, N.H., Refsnes, P.E., Kadi, F., Raastad, T., 2007. Dis- similar effects of one-and three-set strength training on strength and muscle mass gains in upper and lower body in untrained subjects. J. Strength Cond. Res. 21, 157–163.

Rønnestad, B.R., Hansen, E.A., Raastad, T., 2012. High volume of endurance training impairs adaptations to 12 weeks of strength training in well-trained endurance athletes. Eur. J.

Appl. Physiol. 112, 1457–1466.

Rønnestad, B.R., Mujika, I., 2014. Optimizing strength training for running and cycling endurance performance: A review: Strength training and endurance performance. Scand. J.

Med. Sci. Sports 24, 603–612.

Sale, D.G., MacDougall, J.D., Jacobs, I., Garner, S., 1990. Interaction between concurrent strength and endurance training. J. Appl. Physiol. Bethesda Md 1985 68, 260–270.

Shaw, B.S., Shaw, I., Brown, G.A., 2009. Comparison of Resistance and Concurrent Re- sistance and Endurance Training Regimes in the Development of Strength: J. Strength Cond. Res. 23, 2507–2514.

Støren, O., Helgerud, J., Støa, E.M., Hoff, J., 2008. Maximal strength training improves running economy in distance runners. Med. Sci. Sports Exerc. 40, 1087–1092.

Terzis, G., Georgiadis, G., Stratakos, G., Vogiatzis, I., Kavouras, S., Manta, P., Mascher, H., Blomstrand, E., 2007. Resistance exercise-induced increase in muscle mass correlates with p70S6 kinase phosphorylation in human subjects. Eur. J. Appl. Physiol. 102, 145–

152.

(24)

Van Hall, G., Jensen-Urstad, M., Rosdahl, H., Holmberg, H.-C., Saltin, B., Calbet, J. a. L., 2003. Leg and arm lactate and substrate kinetics during exercise. Am. J. Physiol. En- docrinol. Metab. 284, E193-205.

Vissing, K., McGee, S.L., Farup, J., Kjølhede, T., Vendelbo, M.H., Jessen, N., 2013. Differen- tiated mTOR but not AMPK signaling after strength vs endurance exercise in training- accustomed individuals: Divergent exercise and protein signaling. Scand. J. Med. Sci.

Sports 23, 355–366.

Wang, L., Mascher, H., Psilander, N., Blomstrand, E., Sahlin, K., 2011. Resistance exercise enhances the molecular signaling of mitochondrial biogenesis induced by endurance exercise in human skeletal muscle. J. Appl. Physiol. 111, 1335–1344.

Wernbom, M., Augustsson, J., Thomeé, R., 2007. The influence of frequency, intensity, volume and mode of strength training on whole muscle cross-sectional area in humans.

Sports Med. Auckl. NZ 37, 225–264.

Wilson, J.M., Marin, P.J., Rhea, M.R., Wilson, S.M.C., Loenneke, J.P., Anderson, J.C., 2012.

Concurrent Training: A Meta-Analysis Examining Interference of Aerobic and Re- sistance Exercises. J. Strength Cond. Res. 26, 2293–2307.