Optimizing Strength Training for Running and Cycling Endurance Performance: a Review

Review Optimizing strength training for running and cycling endurance performance: A review

B. R. Rønnestad1, I. Mujika2,3

1Section for Sport Science, Lillehammer University College, Lillehammer, Norway, 2Department of Physiology, Faculty of Medicine and Odontology, University of the Basque Country, Leioa, Basque Country, Spain, 3School of Kinesiology and Health Research Center, Faculty of Medicine, Finis Terrae University, Santiago, Chile Corresponding author: Bent R. Rønnestad, PhD, Section for Sport Science, Lillehammer University College, PB. 952, 2604 Lillehammer, Norway. Tel: +47 61288193, Fax: +47 61288200, E-mail: [email protected] Accepted for publication 5 July 2013

Here we report on the effect of combining endurance Wmax, respectively) or time to exhaustion at Vmax and Wmax. training with heavy or explosive strength training on Combining endurance training with either explosive or endurance performance in endurance-trained runners heavy strength training can improve running perfor- and cyclists. Running economy is improved by perform- mance, while there is most compelling evidence of an ing combined endurance training with either heavy or additive effect on cycling performance when heavy explosive strength training. However, heavy strength strength training is used. It is suggested that the improved training is recommended for improving cycling economy. endurance performance may relate to delayed activation Equivocal findings exist regarding the effects on power of less efficient type II fibers, improved neuromuscular output or velocity at the lactate threshold. Concurrent efficiency, conversion of fast-twitch type IIX fibers into endurance and heavy strength training can increase more fatigue-resistant type IIA fibers, or improved running speed and power output at VO2max (Vmax and musculo-tendinous stiffness.

The effects of strength training on endurance athletic effect on endurance performance (Jensen, 1963; performance have long been the subject of debate among Paavolainen et al., 1991; Tanaka et al., 1993). However, athletes, coaches, and sport scientists. Strength training recent evidence contradicts the findings of those early includes both explosive strength training and heavy studies and points toward an additive effect of combining strength training that promote different training adapta- the endurance and strength training on running and tions. Heavy strength training can be defined as “all cycling performance (Tanaka & Swensen, 1998). At the training aiming to increase or maintain a muscle or a time of this review, there was a lack of good studies on muscle group’s ability to generate maximum force” already well-trained endurance athletes, especially in (Knuttgen & Kraemer, 1987) and is here equal to cycling. The purpose of this review is to provide an training with a load that allows between 1 repetition updated synopsis on the effect of combining endurance maximum (RM) and 15 RM. Explosive strength training training with heavy or explosive strength training on is here defined as exercises with external loading of endurance performance in endurance-trained runners 0–60% of 1 RM and maximal mobilization in the con- and cyclists. centric phase (0% of 1 RM equals body weight). Perfor- mance in most endurance events is mainly determined by The effects of strength training on factors the maximal sustained power production for a given competition distance, and the energy cost of maintaining determining endurance performance a given competition speed. In shorter endurance events Maximal oxygen consumption and during accelerations and sprint situations, anaerobic Maximal oxygen consumption (VO2max) has long been capacity and maximal speed may also contribute to per- associated with success in endurance sports (Saltin & formance. Strength training contributes to enhance Astrand, 1967; Costill et al., 1973; Bassett & Howley, endurance performance by improving the economy of 2000) and is one of the major characteristics that deter- movement, delaying fatigue, improving anaerobic mine endurance performance (Di Prampero, 2003; capacity, and enhancing maximal speed. Levine, 2008). Importantly, the highest VO2max value Some of the early studies that investigated the effect does not necessarily equate to the best endurance perfor- of combining endurance and strength training in mance, but the best endurance performance typically endurance-trained athletes did not identify any additive demands high VO2max values (Saltin & Astrand, 1967;

1 Rønnestad & Mujika Costill et al., 1973; Lucia et al., 1998; Bassett & Howley, by the same traditional method used in running (i.e.,

2000; Impellizzeri et al., 2005). In addition, VO2max sets short, 3–5 min, submaximal bouts of exercise), it the upper limit of intensity for prolonged steady-state appears there is little change after combining heavy exercise. strength or explosive strength training with endurance There is little evidence that strength training should be training (Bastiaans et al., 2001; Rønnestad et al., 2010a, the primary training mode to improve VO2max, and only a b; Aagaard et al., 2011). However, adding heavy strength trivial effect of concurrent strength and endurance train- training to endurance training can improve cycling ing on VO2max compared to endurance training alone in economy after only 8 weeks (Sunde et al., 2010). The trained cyclists (Hickson et al., 1988; Bishop et al., reasons for this discrepancy remain unclear, but the 1999; Bastiaans et al., 2001; Levin et al., 2009; lower performance level of the cyclists in the latter study Rønnestad et al., 2010a, b; Sunde et al., 2010; Aagaard may have affected the outcome of strength training. On et al., 2011), long-distance runners (Johnston et al., the other hand, by using a nontraditional protocol to 1997; Paavolainen et al., 1999; Spurrs et al., 2003; measure cycling economy during 5-min periods every Turner et al., 2003; Saunders et al., 2006; Mikkola et al., half hour throughout 3 h of submaximal cycling, a supe- 2007a, 2011; Storen et al., 2008; Taipale et al., 2010), rior improvement was observed during the last hour after cross-country skiers (Hoff et al., 1999, 2002; Osteras a period of concurrent heavy strength and endurance et al., 2002; Mikkola et al., 2007b; Losnegard et al., training (Rønnestad et al., 2011). Lowered heart rate at 2011; Rønnestad et al., 2012), or triathletes (Millet et al., the end of 2 h of submaximal cycling has also been 2002). However, the majority of the training interven- observed after 5 weeks of heavy strength training in tions investigating the effects of concurrent training triathletes (Hausswirth et al., 2010). Thus, divergent lasted only 8 to 12 weeks. Caution should be used when ﬁndings are evident on whether performing heavy long-term effects of concurrent training are considered. strength training together with ordinary endurance training improves cycling economy. This shortcoming may relate in part to methodological differences between Exercise economy studies. Nevertheless, there are no reports of a negative Exercise economy has been deﬁned as the oxygen con- effect of heavy strength and explosive strength training sumption required at a given absolute submaximal exer- on either cycling or running economy. cise intensity (Jones & Carter, 2000; Saunders et al., 2004). There is substantial interindividual variability in exercise economy in both running and cycling despite a Lactate threshold similar VO2max (Conley & Krahenbuhl, 1980; Horowitz The fraction of VO2max, which can be sustained during a et al., 1994). The importance of exercise economy is performance bout (performance VO2), is associated with underlined by the close relationship with endurance per- the degree of blood lactate accumulation during exercise formance in trained individuals with homogenous (Farrell et al., 1979; LaFontaine et al., 1981; Tanaka &

VO2max (Costill, 1967; Conley & Krahenbuhl, 1980; Seals, 2008). Several methods have been devised to Horowitz et al., 1994). Accordingly, it is likely that any express the relationship between blood lactate concen- - improvement in exercise economy will be associated tration ([la ]) and fraction of VO2max (Bentley et al., 2007; with improved long-term endurance performance. Faude et al., 2009). A common term is lactate threshold, Numerous studies have reported improved running which describes an estimation of a breakpoint on the [la-] economy after 8–14 weeks of concurrent heavy strength curve as a function of exercise intensity (Tokmakidis and endurance training, while no substantial changes et al., 1998). Lactate threshold expressed as a percentage were observed in the control groups (Johnston et al., of VO2max is largely unaffected by exercise economy and

1997; Hoff & Helgerud, 2002; Millet et al., 2002; Storen VO2max, which might explain the small correlation et al., 2008; Guglielmo et al., 2009; Taipale et al., 2010). between lactate threshold expressed as % VO2max and Improved running economy is also evident after 6–12 time trial cycling performance in cyclists (Støren et al., weeks of combined explosive strength and endurance 2012). There are numerous ways to determine the power training in runners (Paavolainen et al., 1999; Spurrs output or speed at the lactate threshold, resulting in et al., 2003; Turner et al., 2003; Saunders et al., 2006; diverse “thresholds” on the [la-] vs power/speed curve, Taipale et al., 2010). Mikkola et al. (2007a) replaced which all seem to correlate well with long-term endur- some of the endurance training of young distance ance performance (Tokmakidis et al., 1998). Any right- runners with only one session a week of explosive ward movement of the [la-] curve results in improved strength training and did not ﬁnd changes in running power output/velocity at the lactate threshold regardless economy. Given that running economy can be improved of how the lactate threshold has been determined by 2–3 strength training sessions per week, it seems a (Tokmakidis et al., 1998). A higher velocity/power threshold of (explosive) strength training volume and output at the lactate threshold theoretically means that an frequency has to be overcome to achieve improved athlete can maintain a higher velocity/power output running economy. When cycling economy is measured during extended exercise. Numerous studies report a

2 Strength training and endurance performance high relationship between long-term performance and letes are matched for aerobic capacity (Bulbulian et al., velocity/power output at the lactate threshold in both 1986; Houmard et al., 1991; Paavolainen et al., 1999b; cycling and running, and the latter is useful for predict- Baumann et al., 2012). Concurrent endurance and heavy ing endurance performance in both runners and cyclists strength training can increase Wmax/Vmax or time to (e.g. Farrell et al., 1979; Coyle et al., 1988, 1991; Grant exhaustion at Wmax/Vmax (Hickson et al., 1988; Millet et al., 1997; Bishop et al., 1998; Lucia et al., 1998; et al., 2002; Rønnestad et al., 2010a, b; Sunde et al., Impellizzeri et al., 2005; Slattery et al., 2006). 2010; Taipale et al., 2010, 2013; Mikkola et al., 2011; Since the majority of studies reported improved Støren et al., 2012). However, this positive effect in running economy in response to a period of concurrent cyclists was not observed by using explosive strength strength and endurance training in endurance-trained training (Bastiaans et al., 2001) nor after short-term (6 individuals, it would be reasonable to expect an improve- weeks) strength training (Levin et al., 2009). ment in the exercise velocity or intensity associated with Another related factor important for endurance perfor- the lactate threshold. This expectation is based on the mance is the ability to generate high power output over a assumption that the main determinants of the lactate short period of time to get a good position at the start of threshold velocity are VO2max and exercise economy (Di a race, close a gap, make a critical pass, break away from Prampero et al., 1986), and that VO2max is not compro- the pack, or win a ﬁnal sprint. Peak power output is mised while concurrently performing strength and markedly affected by muscle cross-sectional area endurance training. However, the endurance training lit- (Izquierdo et al., 2004) – increased cross-sectional area erature comprises equivocal ﬁndings: some studies of the quadriceps muscle was associated with increased report little change in the lactate threshold of runners peak power output after combined heavy strength train- (Paavolainen et al., 1999; Hoff & Helgerud, 2002; ing and endurance training in well-trained cyclists Mikkola et al., 2011; Støren et al., 2012), while others (Rønnestad et al., 2010a). Similarly, anaerobic running observed substantial improvements in velocity at the power can increase substantially after a period of added lactate threshold (Mikkola et al., 2007a, 2011; explosive strength training (Paavolainen et al., 1999; Guglielmo et al., 2009; Taipale et al., 2013). Some Mikkola et al., 2007a). studies report improved power output at a certain [la-] (Koninckx et al., 2010; Rønnestad et al., 2010a, b), while others report no additional effect of performing Endurance performance strength training (Bishop et al., 1999; Sunde et al., 2010; Aagaard et al., 2011). Importantly, none of the studies on The traditional way of measuring cycling performance is long-distance runners and cyclists report a negative time trialing lasting between 30 and 60 min. However, effect of strength training on velocity or power output at the effects of strength training are contradictory with the lactate threshold. studies variously showing either improvements (Hickson et al., 1988; Koninckx et al., 2010; Rønnestad et al., 2010b; Aagaard et al., 2011) or a trivial effect (Bishop Other factors important for endurance performance et al., 1999; Bastiaans et al., 2001; Levin et al., 2009). The key performance and physiological measures of When positive effects are reported, heavy strength train-

VO2max, lactate threshold, and exercise economy explain ing is performed with multiple leg exercises. In contrast, >70% of the between-subject variance in long-duration studies failing to show much improvement were typi- endurance performances (Di Prampero et al., 1986). cally short term in duration, with a low volume of Other factors contribute to endurance performance strength training or using explosive strength training. In including running speed and power output at VO2max contrast, adding both explosive and heavy strength train-

(Vmax and Wmax, respectively) predict endurance perfor- ing to endurance training can improve running performance in endurance-trained runners and cyclists, respec- mance, while no change was observed in the control tively (Morgan et al., 1989; Noakes et al., 1990; Hawley groups performing endurance training only (Paavolainen & Noakes, 1992; Yoshida et al., 1993; Billat & et al., 1999; Spurrs et al., 2003; Støren et al., 2012). Koralsztein, 1996; Bentley et al., 1998; Lucia et al., Combining heavy strength training and regular 1998; Balmer et al., 2000; Stratton et al., 2009). Both endurance training increased mean power output pro-

Wmax and Vmax distinguish the endurance performance in duction during a ﬁnal 5-min all-out sprint after 3 h of well-trained cyclists and long distance runners, making submaximal cycling by 7%, while no changes occurred them a useful marker of endurance performance (Noakes in the endurance training group (Rønnestad et al., et al., 1990; Lucia et al., 1998). Wmax and Vmax are inﬂu- 2011). Not all studies, however, have reported that con- enced by VO2max and exercise economy, but also current training results in superior endurance perfor- incorporate anaerobic capacity and neuromuscular char- mance, especially in males (Kraemer et al., 2004; acteristics (Jones & Carter, 2000). Anaerobic power and Barnes et al., 2013). Nevertheless, there are no reports neuromuscular characteristics are also involved in long- of negative impacts of concurrent training on endurance duration endurance performance, especially when ath- performance.

3 Rønnestad & Mujika Potential mechanisms athlete to exercise longer until exhaustion (Hickson et al., 1988; Coyle et al., 1992; Horowitz et al., 1994). A A likely mechanism for improved performance after 12-week program of heavy strength training resulted in combined strength and endurance training is (altered) higher phosphocreatine and glycogen content and lower - muscle fiber type recruitment pattern. When measuring [la ] at the end of 30 min cycling at 72% of VO2max, cycling economy the traditional way, by measuring despite no change in VO2max (Goreham et al., 1999). The oxygen consumption during a short period of time at performed strength training program was almost identi- steady-state exercise intensities below the lactate cal to the strength training performed in the studies threshold, mainly type I fibers that are activated. In this reporting a superior effect of concurrent training in setting, may the effect of increasing the maximum long-term endurance performance, despite the observa- strength of type I fibers and postponing the activation of tion of no change in the traditional way of measuring the less economical type II fibers be trivial or small. cycling economy (Aagaard et al., 2011; Rønnestad This effect might explain why the literature seems is et al., 2011). The studies in which no additive perfor- equivocal on improvements in cycling economy in mance effect of concurrent training in cyclists was well-trained cyclists measured the traditional way. found performed either explosive strength training with Altered muscle fiber recruitment may also explain why low external load (Bastiaans et al., 2001), low volume of improvement of cycling economy in well-trained heavy strength training (Bishop et al., 1999), or lasted cyclists after a period of concurrent training is detected for a short duration (Levin et al., 2009). Thus, it seems first after about 2 h of submaximal cycling (Rønnestad that differences in a strength training program can et al., 2011). It is likely that after prolonged cycling will explain the different findings. Explosive strength train- some of the type I fibers be exhausted and the less ing and low-volume heavy strength training can induce economical type II fibers gradually increases their con- inferior strength and hypertrophic responses compared tribution to the exercise. It might be suggested that the to higher volume of heavy strength (Rønnestad et al., strength training increases the maximum strength of 2007; Holm et al., 2008). Unfortunately, no perfor- type I fibers and postpones their time to exhaustion and mance measurements were obtained in the study of thereby delaying the activation of type II fibers. Goreham et al. (1999), but the improved aerobic Strength training increases maximal force, and there- metabolism and conservation of limited glycogen stores fore peak force or muscle-fiber tension developed in are important for long-term endurance performance. each movement cycle at the same absolute exercise Interestingly, they did not observe any change in cycling intensity decreases to a lower percentage of the economy. maximal values. A cross-sectional study of cyclists with Another putative mechanism explaining improvement similar VO2max and Wmax reported lower EMG activity in in endurance-related measurements after concurrent the cyclists with higher compared with lower maximal training is increased maximum force, and/or increased strength (Bieuzen et al., 2007). rate of force development (RFD) facilitating better Another potentially contributing factor to improved blood flow to exercising muscles (Hoff et al., 1999, endurance performance is an increased proportion of 2002; Sunde et al., 2010; Aagaard et al., 2011; Støren type IIA fibers and reduced proportion of type IIX et al., 2012). Increases in RFD is often caused by fibers. A 16-week study in top-level cyclists combining increased neural activation and both heavy strength heavy strength training and endurance training in top- training with maximal velocity in the concentric phase level cyclists examined the proportional redistribution of the lift and explosive strength training can increase in type II muscle fibers (Aagaard et al., 2011). The neural activation (Mikkola et al., 2011). Superior increase in the more fatigue-resistant, yet high capabil- improvement in maximum force and RFD was accom- ity of power output, type IIA fibers may contribute to panied by superior improvement in exercise economy improved endurance performance. However, there have (Heggelund et al., 2013). Improvement in maximum also been reported no changes in fiber composition in force and/or RFD might lower the relative exercise endurance athletes after a period of concurrent strength intensity and induce less constriction of the blood flow. and endurance training (Bishop et al., 1999). The dif- Alternatively, improved RFD may reduce time to reach ferent findings might be related to differences in initial the desired force in each movement cycle. A shorter percentages of type IIX fibres (Bishop et al., 1999). contraction time or shorter time with relative high force According to the size principle of motor unit recruit- production in working muscles may increase blood flow ment (Henneman et al., 1965), the following mechanism to the muscles by reducing time where blood flow is may be hypothesized: a reduced reliance on the less restricted. Whether blood flow is enhanced after a period efficient type II muscle fibers and thus improved exer- of concurrent training has not been thoroughly investi- cise economy; slower emptying of glycogen stores; gated, but in theory, an increase in blood flow will reduced overall muscle fatigue; and a potentially increase delivery of O2 and substrates to the working increased capacity for high-intensity performance fol- muscles – contributing to enhanced endurance perfor- lowing prolonged exercise or an increased ability by the mance (but not necessarily improved exercise

4 Strength training and endurance performance economy). On the other hand, a recent study on moder- intensities, thus improving running economy as ately trained cyclists by Barrett-O’Keefe et al. (2012) observed in the majority of the presented studies. This showed that 8 weeks of heavy strength training mechanism is unlikely to be equally important when improved work economy at a cadence of 60 rpm, cycling due to the lack of pronounced eccentric phase reduced muscular blood flow, while maintaining muscu- from which the elastic energy can be utilized. lar arterial-venous oxygen difference. The latter indicates that improvement in muscular efficiency is an Potential negative outcomes important mechanism behind improved work economy and improved endurance performance. A potential counterproductive outcome of strength train- Magnetic resonance imaging indicates that increased ing is that muscle hypertrophy could have a negative maximum strength reduces the amount of activated impact on weight-bearing endurance events. An increase muscle mass to generate the same absolute submaximal in myofiber cross-sectional area could reduce capillary power (Ploutz et al., 1994). If less muscle mass gener- to muscle fiber cross-sectional area ratio, thus increasing ates the same power after increased maximum strength, diffusion distance. In this respect, it is worth mentioning metabolic strain is concentrated on fewer fibers and that 8–16 weeks of supplemental strength training failed obviates the effect of increased maximum strength. In to increase total body mass nor compromise the devel- the opposite direction, activated muscle fibers might opment of VO2max in endurance athletes including exercise at the same relative intensity due to the increase cyclists (Bishop et al., 1999; Bastiaans et al., 2001; in maximum strength. If that is the case, then the strength Levin et al., 2009; Rønnestad et al., 2010a, b; Sunde training would presumably not affect exercise economy et al., 2010; Aagaard et al., 2011), runners (Johnston directly, measured as oxygen consumption, but poten- et al., 1997; Paavolainen et al., 1999; Spurrs et al., 2003; tially increase the endurance performance via increasing Turner et al., 2003; Saunders et al., 2006; Mikkola et al., the quantity of fresh muscle mass available when the 2007a, 2011; Storen et al., 2008), duathletes and final sprint is approaching. In a time trial setting, where triathletes (Hickson et al., 1988; Millet et al., 2002), and the objective is to cover a certain distance as fast as cross-country skiers (Hoff et al., 1999, 2002; Osteras possible, this adaptation could theoretically result in et al., 2002; Mikkola et al., 2007b; Losnegard et al., superior performance due to increased power output per 2011; Rønnestad et al., 2012). unit muscle mass. Even though strength training can be added to endur- One of the distinct differences between cycling and ance training without a concomitant increase in total running is the stretch-shortening cycle in running, while body mass, there seems to be a small, ∼3–6%, increase the leg movements in cycling are mainly composed of in measurements of muscle hypertrophy of the main concentric muscle actions. Thus, cyclists are not able to target muscles (Rønnestad et al., 2010a, 2012; Taipale store energy during an eccentric phase and utilize it in et al., 2010; Aagaard et al., 2011; Losnegard et al., the subsequent concentric phase to the same extent as 2011). An impaired hypertrophic response to strength runners. It is estimated that storage and return of elastic training is likely explained by recent developments energy during running approximates about half of the within molecular sports science. Endurance exercise mechanical work performed during the eccentric phase may negatively affect intracellular pathways important of a running stride (Cavagna et al., 1964). In accordance for myofibrillar protein synthesis (reviewed in Hawley, with the latter assertion, stiffness of the musculo- 2009). Activation of adenosine monophosphate- skeletal system in the lower body is associated with activated protein kinase by endurance exercise may enhanced running economy in a wide range of runners inhibit mammalian target of rapamycin signaling and (Craib et al., 1996; Jones, 2002; Trehearn & Buresh, suppress strength exercise-induced myofibrillar protein 2009). Muscle-tendon system is able to increase its stiff- synthesis (Nader, 2006; Hawley, 2009). Consequently, ness through both explosive strength training (Fouré acute intracellular signaling response to concurrent et al., 2011) and heavy strength training (Kubo et al., strength and endurance training does not promote ideal 2001, 2002). Furthermore, stiffness increases in the activation of pathways responsible for muscle hypertro- muscle-tendon system of the lower body after adding phy (Coffey et al., 2009). Observations of disparate both heavy strength training (Millet et al., 2002) and mRNA response to concurrent strength and endurance explosive strength training (Spurrs et al., 2003) to the training underline the importance of local factors in ongoing endurance training. Importantly, it is likely that explaining compromised strength training adaptations there may be an individual optimal stiffness in the to a large volume of concurrent training (Coffey et al., muscle-tendon system. There are apparent advantages of 2009). stiff tendons in some cases and compliant tendons in The observed impaired or absence of whole muscle or other cases (Fletcher et al., 2010). Improved utilization muscle fiber hypertrophy after combining strength train- of elastic energy in the muscle-tendon system in the ing with large volumes of endurance training (Hickson lower body would reduce the demand of adenosine tri- et al., 1988; Bishop et al., 1999; Rønnestad et al., 2010a, phosphate production even at low submaximal running b, 2012; Aagaard et al., 2011; Losnegard et al., 2011)

5 Rønnestad & Mujika greatly reduces the risk of impaired capillary to muscle to moderate-trained persons. Athletes are advised to fiber ratio. In untrained subjects, strength training alone build up maximal strength in the important muscles can increase some aspects of the capillaries perfusing during the preparatory period. Two strength training skeletal muscle fibers (Hather et al., 1991; Green et al., sessions per week, designed as a “daily undulating 1999; McCall et al., 2004). In moderate-trained students, periodized program” is typically enough to achieve a an increase in capillary to fiber ratio has been observed sufficient increase in strength during a 12-week period. after concurrent strength and endurance training, while Athletes are advised to perform between 4 RM and 10 no change was evident after strength or endurance train- RM and 2–3 sets with approximately 2–3 min of rest ing alone (Bell et al., 2000). The only study performed between sets. Before endurance athletes start lifting on top-level endurance athletes did not observe a heavy loads, they must ensure that they have first devel- negative effect after 16 weeks of concurrent heavy oped a proper lifting technique with lighter loads. Note strength training and endurance training on muscle that in the beginning of a strength training period, it is capillarization (Aagaard et al., 2011). In addition, after a common to get “heavy” and “sore” legs in the first days period of concurrent strength and endurance training, after the strength training session. Therefore, it is impor- there is no impairment of the oxidative enzyme activity tant to commence at low level with the concurrent endur- in endurance-trained athletes (Hickson et al., 1988; ance training during the first 2–3 weeks of a strength Bishop et al., 1999; Bell et al., 2000). Thus, with regard training program. One approach to overcome this initial to muscle vascularization and oxidative potential, there strength training adaptation phase is to conduct it just seems to be no indications of negative effect of strength after the end of a competition season, when endurance training. training has a lower priority. During the competitive season or in training periods, development of strength is not prioritized, approximately one strength training Practical recommendations session per week (low volume) with high intensity seems To increase the probability of improved endurance per- to maintain the previous strength training adaptations formance subsequent to a strength training period, the (Rønnestad et al., 2010b, 2011b). strength training exercises should involve similar muscle Both explosive and maximal strength training have groups and imitate the sports-specific movements. This positive influences on endurance running performance advice is underpinned by adaptations in the neural and/or running economy in endurance athletes (e.g., system (like optimal activation of the involved muscles) Paavolainen et al., 1999; Millet et al., 2002; Spurrs as well as structural adaptations (like optimizing the et al., 2003; Støren et al., 2012). Recently, the enhanc- number of active cross-bridges in that particular range of ing effects of combining endurance training with either motion). An intended rather than the actual velocity heavy or explosive strength training on running perfor- appears to determine the velocity-specific training mance have been investigated. The studies that report a response (Behm & Sale, 1993; Heggelund et al., 2013). difference in adaptations after heavy or explosive This scenario means that even though the actual move- strength training point toward more favorable adapta- ment velocity is quite low, RFD might be increased if the tions as a result of heavy strength training (Guglielmo athlete focuses on performing the concentric phase of the et al., 2009; Mikkola et al., 2011; Barnes et al., 2013). lift as quick as possible. Superior adaptations in maximal strength and RFD are achievable after 8 weeks of heavy Conclusion strength training with maximal velocity in the concentric phase compared to moderate velocity in the concentric Recent research on highly trained athletes indicates that phase (Heggelund et al., 2013). This superiority was strength training can be successfully prescribed to accompanied by superior improvement in exercise enhance endurance performance (Table 1). For cycling economy during single leg knee extension in untrained performance, heavy strength training with maximal

Table 1. Effects of heavy and explosive strength training on endurance performance

Potential positive physiological and Evidence Potential negative physiological and Evidence of performance effect of beneﬁt performance effect negative outcome

Improved VO2max No Increased body mass No Improved exercise economy Yes Compromised relative VO2max No Improved anaerobic capacity Yes Increased diffusion distance No Improved lactate threshold Yes Reduced capillarization No Reduced or delayed fatigue Yes Reduced oxidative enzyme activity No Improved maximal strength Yes Improved rate of force development Yes Improved maximal speed Yes Improved endurance performance Yes

6 Strength training and endurance performance velocity during the concentric phase is preferred, while of strength training. In general a coach and athlete can both heavy strength training with maximal velocity employ with confidence concurrent endurance and during the concentric phase and explosive strength train- strength training to improve athletic endurance perfor- ing have additive effects on running performance. The mance. To optimize the effect of added strength training primary explanation for improved endurance perfor- to cycling performance, athletes should undertake heavy mance is most likely adaptations within the strength- strength training with maximal velocity during the con- trained muscle including postponed activation of less centric phase should be the training mode to recommend efficient type II fibers, improved neuromuscular effi- (instead of explosive strength training), while both ciency, conversion of fast-twitch type IIX fibers into explosive- and heavy strength training with maximal more fatigue-resistant type IIA fibers, and improved velocity during the concentric phase appear to have an musculo-tendinous stiffness. Importantly, no negative additive effect on running performance. effects of adding strength training to an endurance training program have been reported. Key words: aerobic capacity, concurrent training adaptations, exercise economy, neuromuscular function, Perspectives cycling, running.

The effects of strength training on endurance athletic Acknowledgements performance have been the subject of a long debate among athletes, coaches, and sport scientists. Incorpora- The authors gratefully acknowledge the editorial comments and tion of strength training in endurance athletes’ prepara- suggestions made by Prof. David Pyne (Physiology, Australian Institute of Sport) in the preparation of this manuscript. No sources tion has gradually received more attention during the last of funding were used to assist in the preparation of this article. The two decades with studies showing divergent ﬁndings. authors have no conﬂicts of interest that are directly relevant to the Some of this discrepancy seems to be related to the mode content of this article.

References

Aagaard P, Andersen JL, Bennekou M, training on performance in trained Billat LV, Koralsztein JP. Signiﬁcance of

Larsson B, Olesen JL, Crameri R, cyclists. Eur J Appl Physiol 2001: 86: the velocity at VO2max and time to Magnusson SP, Kjaer M. Effects of 79–84. exhaustion at this velocity. Sports Med resistance training on endurance Baumann CW, Rupp JC, Ingalls CP, 1996: 22: 90–108. capacity and muscle fiber composition Doyle JA. Anaerobic work capacity’s Bishop D, Jenkins DG, Mackinnon LT. in young top-level cyclists. Scand J contribution to 5-km-race performance The relationship between plasma Med Sci Sports 2011: 21: in female runners. Int J Sports Physiol lactate parameters, W-peak and 1-h e298–e307. Perform 2012: 7: 170–174. cycling performance in women. Balmer J, Davison RCR, Bird SR. Peak Behm DG, Sale DG. Velocity specificity Med Sci Sports Exerc 1998: 30: power predicts performance power of resistance training. Sports Med 1270–1275. during an outdoor 16.1-km cycling time 1993: 15: 374–388. Bishop D, Jenkins DG, Mackinnon LT, trial. Med Sci Sports Exerc 2000: 32: Bell GJ, Syrotuik D, Martin TP, Burnham McEniery M, Carey MF. The effects of 1485–1490. R, Quenney HA. Effect of concurrent strength training on endurance Barnes KR, Hopkins WG, McGuigan MR, strength and endurance training on performance and muscle characteristics. Northuis ME, Kilding AE. Effects of skeletal muscle properties and hormone Med Sci Sports Exerc 1999: 31: resistance training on running economy concentrations in humans. Eur J Appl 886–891. and cross-country performance. Med Physiol 2000: 81: 418–427. Bulbulian R, Wilcox AR, Darabos BL. Sci Sports Exerc 2013: doi: Bentley DJ, Newell J, Bishop D. Anaerobic contribution to distance 10.1249/MSS.0b013e31829af603. Incremental exercise test design and running performance of trained Barrett-O’Keefe Z, Helgerud J, Wagner analysis: implications for performance cross-country athletes. Med PD, Richardson RS. Maximal strength diagnostics in endurance athletes. Sci Sports Exerc 1986: 18: training and increased work efficiency: Sports Med 2007: 37: 575–586. 107–113. contribution from the trained muscle Bentley DJ, Wilson GJ, Davie AJ, Zhou Cavagna GA, Saibene FP, Margaria R. bed. J Appl Physiol 2012: 113: S. Correlations between peak power Mechanical work in running. J Appl 1846–1851. output, muscular strength and cycle Physiol 1964: 19: 249–256. Bassett DR, Howley ET. Limiting factors time trial performance in triathletes. J Coffey VG, Pilegaard H, Garnham AP, for maximum oxygen uptake and Sports Med Phys Fitness 1998: 38: O’Brien BJ, Hawley JA. Consecutive determinants of endurance 201–207. bouts of diverse contractile activity performance. Med Sci Sports Exerc Bieuzen F, Lepers R, Vercruyssen F, alter acute responses in human skeletal 2000: 32: 70–84. Hausswirth C, Brisswalter J. Muscle muscle. J Appl Physiol 2009: 106: Bastiaans JJ, van Diemen AB, Veneberg activation during cycling at different 1187–1197. T, Jeukendrup AE. The effects of cadences: effect of maximal strength Conley DL, Krahenbuhl GS. Running replacing a portion of endurance capacity. J Electromyogr Kinesiol economy and distance running training by explosive strength 2007: 17: 731–738. performance of highly trained athletes.

7 Rønnestad & Mujika

Med Sci Sports Exerc 1980: 12: performance and selected physiological Holm L, Reitelseder S, Pedersen TG, 357–360. variables. J Sports Sci 1997: 15: Doessing S, Petersen SG, Flyvbjerg A, Costill DL. The relationship between 403–410. Andersen JL, Aagaard P, Kjaer M. selected physiological variables and Green H, Goreham C, Ouyang J, Changes in muscle size and MHC distance running performance. Ball-Burnett M, Ranney D. Regulation composition in response to resistance J Sports Med Phys Fitness 1967: 7: of fiber size, oxidative potential, and exercise with heavy and light loading 61–66. capillarization in human muscle by intensity. J Appl Physiol 2008: 105: Costill DL, Thomason H, Roberts E. resistance exercise. Am J Physiol 1999: 1454–1461. Fractional utilization of the aerobic 276: R591–R596. Horowitz JF, Sidossis LS, Coyle EF. High capacity during distance running. Med Guglielmo LG, Greco CC, Denadai BS. efficiency of type I muscle fibers Sci Sports 1973: 5: 248–252. Effects of strength training on running improves performance. Int J Sports Coyle EF, Coggan AR, Hopper MK, economy. Int J Sports Med 2009: 30: Med 1994: 15: 152–157. Walters TJ. Determinants of endurance 27–32. Houmard JA, Costill DL, Mitchell JB, in well-trained cyclists. J Appl Physiol Hather BM, Tesch PA, Buchanan P, Park SH, Chenier TC. The role of 1988: 64: 2622–2630. Dudley GA. Influence of eccentric anaerobic ability in middle distance Coyle EF, Feltner ME, Kautz SA, actions on skeletal muscle running performance. Eur J Appl Hamilton MT, Montain SJ, Baylor AM, adaptations to resistance training. Physiol Occup Physiol 1991: 62: Abraham LD, Petrek GW. Acta Physiol Scand 1991: 143: 40–43. Physiological and biomechanical 177–185. Impellizzeri FM, Marcora SM, Rampinini factors associated with elite endurance Hausswirth C, Argentin S, Bieuzen F, E, Mognoni P, Sassi A. Correlations cycling performance. Med Sci Sports Le Meur Y, Couturier A, Brisswalter J. between physiological variables and Exerc 1991: 23: 93–107. Endurance and strength training effects performance in high level cross country Coyle EF, Sidossis LS, Horowitz JF, on physiological and muscular off road cyclists. Br J Sports Med Beltz JD. Cycling efficiency is related parameters during prolonged cycling. 2005: 39: 747–751. to the percentage of type I muscle J Electromyogr Kinesiol 2010: 20: Izquierdo M, Ibáñez J, Häkkinen K, fibers. Med Sci Sports Exerc 1992: 24: 330–339. Kraemer WJ, Ruesta M, Gorostiaga 782–788. Hawley JA. Molecular responses to EM. Maximal strength and power, Craib MW, Mitchell VA, Fields KB, strength and endurance training: are muscle mass, endurance and serum Cooper TR, Hopewell R, Morgan DW. they incompatible. Appl Physiol Nutr hormones in weightlifters and road The association between flexibility and Metab 2009: 34: 355–361. cyclists. J Sports Sci 2004: 22: running economy in sub-elite male Hawley JA, Noakes TD. Peak power 465–478. distance runners. Med Sci Sports Exerc output predicts maximal oxygen uptake Jensen CR. Effects of 5 training 1996: 28: 737–743. and performance time in trained combinations of swimming and weight Di Prampero PE. Factors limiting cyclists. Eur J Appl Physiol Occup training on swimming the front crawl. maximal performance in humans. Eur J Physiol 1992: 65: 79–83. Res Quart 1963: 34: 471–477. Appl Physiol 2003: 90: 420–429. Heggelund J, Fimland MS, Helgerud J, Johnston RE, Quinn TJ, Kertzer R, Di Prampero PE, Atchou G, Bruckner JC, Hoff J. Maximal strength training Vroman NB. Strength training in Moia C. The energetics of endurance improves work economy, rate of force female distance runners: impact on running. Eur J Appl Physiol Occup development and maximal strength running economy. J Strength Cond Res Physiol 1986: 55: 259–266. more than conventional strength 1997: 11: 224–229. Farrell PA, Wilmore JH, Coyle EF, training. Eur J Appl Physiol 2013: 113: Jones AM. Running economy is Billing JE, Costill DL. Plasma lactate 1565–1573. negatively related to sit-and-reach test accumulation and distance running Henneman E, Somjen G, Carpenter DO. performance in international-standard performance. Med Sci Sports Exerc Functional significance of cell size in distance runners. Int J Sports Med 1979: 25: 1091–1097. spinal motorneurons. J Neurophysiol 2002: 23: 40–43. Faude O, Kindermann W, Meyer T. 1965: 28: 560–580. Jones AM, Carter H. The effect of Lactate threshold concepts: how valid Hickson RC, Dvorak BA, Gorostiaga EM, endurance training on parameters of are they? Sports Med 2009: 39: Kurowski TT, Foster C. Potential for aerobic fitness. Sports Med 2000: 29: 469–490. strength and endurance training to 373–386. Fletcher JR, Esau SP, MacIntosh BR. amplify endurance performance. Knuttgen HG, Kraemer WJ. Terminology Changes in tendon stiffness and J Appl Physiol 1988: 65: and measurement in exercise running economy in highly trained 2285–2290. performance. J Appl Sports Sci Res distance runners. Eur J Appl Physiol Hoff J, Gran A, Helgerud J. Maximal 1987: 1: 1–10. 2010: 110: 1037–1046. strength training improves aerobic Koninckx E, Van Leemputte M, Hespel P. Fouré A, Nordez A, McNair P, Cornu C. endurance performance. Scand J Med Effect of isokinetic cycling versus Effects of plyometric training on both Sci Sports 2002: 12: 288–295. weight training on maximal power active and passive parts of the Hoff J, Helgerud J. Maximal strength output and endurance performance in plantarflexors series elastic component training enhances running economy and cycling. Eur J Appl Physiol 2010: 109: stiffness of muscle-tendon complex. aerobic endurance performance. In: 699–708. Eur J Appl Physiol 2011: 111: Hoff J, Helgerud J, eds. Football Kraemer WJ, Vescovi JD, Volek JS, Nindl 539–548. (soccer): new developments in physical BC, Newton RU, Patton JF, Dziados Goreham C, Green HJ, Ball-Burnett M, training research. Trondheim: NTNU, JE, French DN, Häkkinen K. Effects of Ranney D. High-resistance training and 2002: 39–55. concurrent resistance and aerobic muscle metabolism during prolonged Hoff J, Helgerud J, Wisloff U. Maximal training on load-bearing performance exercise. Am J Physiol 1999: 276: strength training improves work and the Army physical fitness test. Mil E489–E496. economy in trained female Med 2004: 169: 994–999. Grant S, Craig I, Wilson J, Aitchison T. cross-country skiers. Med Sci Sports Kubo K, Kanehisa H, Fukunaga T. Effects The relationship between 3 km running Exerc 1999: 31: 870–877. of resistance and stretching training

8 Strength training and endurance performance

programmes on the viscoelastic and predicted velocity at VO2max among strength training in well-trained properties of human tendon structures well-trained male runners. Med Sci endurance athletes. Eur J Appl Physiol in vivo. J Physiol 2002: 538: Sports Exerc 1989: 21: 78–83. 2012b: 112: 1457–1466. 219–226. Nader GA. Concurrent strength and Rønnestad BR, Kojedal O, Losnegard T, Kubo K, Kanehisa H, Ito M, Fukunaga T. endurance training: from molecules to Kvamme B, Raastad T. Effect of heavy Effects of isometric training on the man. Med Sci Sports Exerc 2006: 38: strength training on muscle thickness, elasticity of human tendon structures in 1965–1970. strength, jump performance, and vivo. J Appl Physiol 2001: 91: 26–32. Noakes TD, Myburgh KH, Schall R. Peak endurance performance in well-trained LaFontaine TP, Londeree BR, Spath WK. treadmill running velocity during the Nordic Combined athletes. Eur J Appl

The maximal steady state versus VO2max test predicts running Physiol 2012: 112: 2341–2352. selected running events. Med Sci performance. J Sports Sci 1990: 8: Rønnestad BR, Nymark BS, Raastad T. Sports Exerc 1981: 13: 190–193. 35–45. Effects of in-season strength Levin GT, McGuigan MR, Laursen PB. Osteras H, Helgerud J, Hoff J. Maximal maintenance training frequency in Effect of concurrent resistance and strength-training effects on professional soccer players. J Strength endurance training on physiologic and force-velocity and force-power Cond Res 2011b: 25: 2653–2660. performance parameters of well-trained relationships explain increases in Saltin B, Astrand PO. Maximal oxygen endurance cyclists. J Strength Cond aerobic performance in humans. uptake in athletes. J Appl Physiol 1967: Res 2009: 23: 2280–2286. Eur J Appl Physiol 2002: 88: 23: 353–358.

Levine BD. VO2max: what do we know, 255–263. Saunders PU, Pyne DB, Telford RD, and what do we still need to know. J Paavolainen L, Häkkinen K, Hämäläinen Hawley JA. Factors affecting running Physiol 2008: 586: 25–34. I, Nummela A, Rusko H. economy in trained distance runners. Losnegard T, Mikkelsen K, Rønnestad Explosive-strength training improves Sports Med 2004: 34: 465–485. BR, Hallén J, Rud B, Raastad T. The 5-km running time by improving Saunders PU, Telford RD, Pyne DB, effect of heavy strength training on running economy and muscle power. Peltola EM, Cunningham RB, Gore CJ, muscle mass and physical performance J Appl Physiol 1999: 86: Hawley JA. Short-term plyometric in elite cross country skiers. 1527–1533. training improves running economy in Scand J Med Sci Sports 2011: 21: Paavolainen L, Häkkinen K, Rusko H. highly trained middle and long distance 389–401. Effects of explosive type strength runners. J Strength Cond Res 2006: 20: Lucia A, Pardo J, Durantez A, Hoyos J, training on physical performance 947–954. Chicharro JL. Physiological differences characteristics in cross-country skiers. Slattery KM, Wallace LK, Murphy AJ, between professional and elite road Eur J Appl Physiol Occup Physiol Coutts AJ. Physiological determinants cyclists. Int J Sports Med 1998: 19: 1991: 62: 251–255. of three-kilometer running performance 342–348. Paavolainen LM, Nummela AT, Rusko in experienced triathletes. J Strength McCall GE, Byrnes WC, Dickinson A, HK. Neuromuscular characteristics and Cond Res 2006: 20: 47–52. Pattany PM, Fleck SJ. Muscle ﬁber muscle power as determinants of 5-km Spurrs RW, Murphy AJ, Watsford ML. hypertrophy, hyperplasia, and capillary running performance. Med Sci Sports The effect of plyometric training on density in college men after resistance Exerc 1999b: 31: 124–130. distance running performance. Eur J training. J Appl Physiol 1996: 81: Ploutz LL, Tesch PA, Biro RL, Dudley Appl Physiol 2003: 89: 1–7. 2004–2012. GA. Effect of resistance training on Storen O, Helgerud J, Stoa EM, Hoff J. Mikkola J, Rusko H, Nummela A, Pollari muscle use during exercise. J Appl Maximal strength training improves T, Hakkinen K. Concurrent endurance Physiol 1994: 76: 1675–1681. running economy in distance runners. and explosive type strength training Rønnestad BR, Egeland W, Kvamme NH, Med Sci Sports Exerc 2008: 40: improves neuromuscular and anaerobic Refsnes PE, Kadi F, Raastad T. 1087–1092. characteristics in young distance Dissimilar effects of one- and three-set Støren O, Ulevåg K, Larsen MH, Støa runners. Int J Sports Med 2007a: 28: strength training on strength and EM, Helgerud J. Physiological 602–611. muscle mass gains in upper and lower determinants of the cycling time trial. Mikkola J, Vesterinen V, Taipale R, body in untrained subjects. J Strength J Strength Cond Res 2012: doi: Capostagno B, Häkkinen K, Nummela Cond Res 2007: 21: 157–163. 10.1519/JSC.0b013e31827f5427. A. Effect of resistance training Rønnestad BR, Hansen EA, Raastad T. Stratton E, O’Brien BJ, Harvey J, Blitvich regimens on treadmill running and Effect of heavy strength training on J, McNicol AJ, Janissen D, Paton C, neuromuscular performance in thigh muscle cross-sectional area, Knez W. Treadmill velocity best recreational endurance runners. J Sports performance determinants, and predicts 5000-m run performance. Int J Sci 2011: 29: 1359–1371. performance in well-trained cyclists. Sports Med 2009: 30: 40–45. Mikkola JS, Rusko HK, Nummela AT, Eur J Appl Physiol 2010a: 108: Sunde A, Støren O, Bjerkaas M, Larsen Paavolainen LM, Hakkinen K. 965–975. MH, Hoff J, Helgerud J. Maximal Concurrent endurance and explosive Rønnestad BR, Hansen EA, Raastad T. strength training improves cycling type strength training increases In-season strength maintenance training economy in competitive cyclists. J activation and fast force production of increases well-trained cyclists’ Strength Cond Res 2010: 24: leg extensor muscles in endurance performance. Eur J Appl Physiol 2157–2165. athletes. J Strength Cond Res 2007b: 2010b: 110: 1269–1282. Taipale RS, Mikkola J, Nummela A, 21: 613–620. Rønnestad BR, Hansen EA, Raastad T. Vesterinen V, Capostagno B, Walker S, Millet GP, Jaouen B, Borrani F, Candau Strength training improves 5-min Gitonga D, Kraemer WJ, Häkkinen K. R. Effects of concurrent endurance and all-out performance following 185 min Strength training in endurance strength training on running economy of cycling. Scand J Med Sci Sports runners. Int J Sports Med 2010: 31: and .VO(2) kinetics. Med Sci Sports 2011: 21: 250–259. 468–476. Exerc 2002: 34: 1351–1359. Rønnestad BR, Hansen EA, Raastad T. Taipale RS, Mikkola J, Vesterinen V, Morgan DW, Baldini FD, Martin PE, High volume of endurance training Nummela A, Häkkinen K. Kohrt WM. Ten kilometer performance impairs adaptations to 12 weeks of Neuromuscular adaptations during

9 Rønnestad & Mujika

combined strength and endurance physiological mechanisms. J Physiol Trehearn TL, Buresh RJ. Sit-and-reach training in endurance runners: maximal 2008: 586: 55–63. ﬂexibility and running economy of men versus explosive strength training or a Tanaka H, Swensen T. Impact of and women collegiate distance runners. mix of both. Eur J Appl Physiol 2013: resistance training on endurance J Strength Cond Res 2009: 23: 158–162. 113: 325–335. performance. A new form of Turner AM, Owings M, Schwane JA. Tanaka H, Costill DL, Thomas R, Fink cross-training? Sports Med 1998: 25: Improvement in running economy after WJ, Widrick JJ. Dry-land resistance 191–200. 6 weeks of plyometric training. J training for competitive swimming. Tokmakidis SP, Leger LA, Pilianidis TC. Strength Cond Res 2003: 17: 60–67. Med Sci Sports Exerc 1993: 25: Failure to obtain a unique threshold on Yoshida T, Udo M, Iwai K, Yamaguchi T. 952–959. the blood lactate concentration curve Physiological characteristics related to Tanaka H, Seals DR. Endurance exercise during exercise. Eur J Appl endurance running performance in performance in Masters athletes: Physiol Occup Physiol 1998: 77: female distance runners. J Sports Sci age-associated changes and underlying 333–342. 1993: 11: 57–62.