Detraining

Valoración del paciente: Diagnóstico del

10 Chapter

Detraining

Laurent BOSQUET1 & Iñigo MUJIKA2

1 Faculty of Sport Sciences, University of Poitiers, France Department of Physiology, Faculty of Medicine and Odontology, University of the Basque Country, Leioa, Basque Country

2

99

Laurent BOSQUET & Iñigo MUJIKA

Laurent BOSQUET, Ph.D. Laurent Bosquet earned a Ph.D. in Physical Activity Sciences from the University of Montreal (Canada) and a Ph.D. in Sport Sciences from the University of Poitiers (France). A former Professor at the University of Montreal, Laurent is a Professor at the University of Poitiers and the Dean of the Faculty of Sport Sciences. His research interest focuses on the optimization of training methods for different populations, including elite athletes, elders or patients suffering from heart diseases. He is the head of the MOVE laboratory (University of Poitiers), associate researcher at the Montreal Institute of Geriatrics, associate researcher at the Rehabilitation Center of the Montreal Heart Institute, and member of the research board at the French Soccer Federation.

Iñigo MUJIKA, Ph.D. Iñigo Mujika earned Ph.D.s in Biology of Muscular Exercise (University of Saint-Etienne, France) and Physical Activity and Sport Sciences (University of The Basque Country). He is a Level III Swimming and Triathlon Coach. His research interests include training methods and recovery, tapering, detraining and overtraining. He has performed extensive research on the physiological aspects associated with endurance sports performance, published over 80 articles in peer reviewed journals, two books and 13 book chapters, and given over 160 lectures in international conferences. Iñigo was Senior Physiologist at the Australian Institute of Sport, physiologist and trainer for Euskaltel Euskadi cycling team, and Head of Research and Development at Athletic Club Bilbao football club. He is Director of Physiology and Training at USP Araba Sport Clinic, Physiologist of the Spanish Swimming Federation, Associate Editor for the International Journal of Sports Physiology and Performance, and Associate Professor at the University of the Basque Country.

100

Detraining

Chapter 10

Detraining

Laurent BOSQUET1 & Iñigo MUJIKA2 1 Faculty of Sport Sciences, University of Poitiers, France Department of Physiology, Faculty of Medicine and Odontology, University of the Basque Country, Leioa, Basque Country

2

Introduction Endurance performance represents a complex interplay between several physiological factors, including maximal oxygen uptake (VO2max), aerobic endurance (AE) and the energy cost of running (Cr) (Di Prampero et al., 1986). Endurance training consists therefore in implementing exercise protocols that will enhance at least one of these determinants, in order to increase overall performance. According to the principle of reversibility, training induced physiological adaptations are transitory and may disappear when the training load is not sufficient. The reasons for such a scenario are numerous in an athlete’s life: illness, injury, post-season break or training load adaptation to recover from a state of overreaching. The consequences on endurance performance may vary according to the way training load is altered: training reduction, training cessation or bed rest confinement (Mujika & Padilla, 2000a). To avoid any confusion with the terminology, a glossary is given in Table 10.1. This chapter addresses the effect of training cessation on the physiological determinants of endurance performance and their underlying factors. Considering that detraining characteristics may differ according to the training background, we focus on studies dealing with well trained to highly trained athletes.

Maximal Oxygen Uptake Maximal oxygen uptake represents the maximal amount of oxygen that can be used at the cellular level for the entire body. It represents the upper limit of the cardiorespiratory system and has long been considered as an important determinant of endurance performance (Saltin & Astrand, 1967). According to the Fick principle, any alteration in VO2max is the consequence of a modification of maximal cardiac output (Qmax) and/or maximal arteriovenous difference in oxygen (a-vDO2max). It is generally accepted that the largest part of the training induced increase in VO2max results from an increase in blood volume, stroke volume and ultimately Qmax. Nevertheless, the increase in a-vDO2max, which results from a more effective distribution of arterial blood from inactive to active muscles together with a greater oxygen extraction and utilization capacity by these muscles, plays also an important role in cardiorespiratory adaptations to endurance training. Coyle et al. (1984) studied the effect of 12, 21, 56 and 84 days of training cessation on VO2max and its determinants in 7 well-trained cyclists. Main results are summarized in

Detraining

A partial or complete loss of training induced anatomical, physiological and performance adaptations, as a consequence of training reduction or cessation.

Training cessation

A temporary discontinuation or complete abandonment of a systematic program of physical conditioning.

Training reduction

A progressive or nonprogressive reduction of the training load during a variable period of time, in an attempt to reduce the physiological and psychological stress of daily training.

Table 10.1. Glossary.

101


Figure 10.1. They observed a ~15% decrease in VO2max that followed a roughly exponential kinetics. Very interestingly, there appeared to be a time sequence in the physiological mechanisms underlying this loss of adaptation. During a first phase lasting 21 to 28 days, a-vDO2max was maintained, suggesting that the decrease in VO2max was mainly a consequence of a decrease in oxygen delivery to the muscle. In fact, Coyle et al. (1985) reported a rapid decrease in Qmax (~8%) that reached a plateau after 21 to 28 days of training cessation. This loss of adaptation resulted from an important drop in maximal stroke volume (~11%), which was partly compensated for by a ~5% increase in maximal heart rate.

Figure 10.2. Effect of training cessation on the blood volume.

shown by a drop in Qmax, while it is peripheral (i.e. specific to the trained muscles) afterwards. This time sequence has many practical implications for athletes and coaches that are discussed at the end of this chapter.

Aerobic Endurance Aerobic endurance represents the capacity to sustain a high fraction of VO2max throughout the entire effort duration (Bosquet et al., 2002). Aerobic endurance is independent from VO2max, since two individuals with the same VO2max are not necessarily able to sustain the same fraction of VO2max for a given effort duration (Peronnet & Thibault, 1989). Both factors contribute to set exercise VO2, which is considered an important determinant of endurance performance, since the higher the exercise VO2, the higher the energy provision in the form of ATP resynthesis rate. Although physiological mechanisms involved in aerobic endurance are not fully understood, the capacity to sustain a high fraction of VO2max for a given duration has been associated with a combination of several factors, including a high percentage of type I muscle fibres, the capacity to store large amounts of muscle and/or liver glycogen, a high activity of mitochondrial enzymes and the capacity to spare carbohydrate by using more fatty acids as energy substrate (Bosquet et al., 2002).

Figure 10.1. Effect of training cessation on the physiological determinants of maximal oxygen uptake (VO2max). Q: cardiac output; a-vDO2: arteriovenous difference in oxygen; SV: stroke volume; HR: heart rate. Adapted from the data reported by Coyle et al. (1984).

The rapid decrease in blood volume after the first days of training cessation observed in several studies is expected to play a key role in the cascade of events leading to the decrease in Qmax (Figure 10.2). Once this first “circulatory detraining” phase is completed, the ongoing decrease of VO2max is now the consequence of a continuous decrease in a-vDO2max (~9%; Figure 10.1). Considering that capillary density did not decline during the 84 days of training cessation, this alteration is likely to be the consequence of a decrease in muscle mitochondrial density or other factors such as a reduction in muscle blood flow or capillary transit time (Coyle et al., 1984).

It is well established that endurance training results in an increased percentage of type I muscle fibres (Pette, 1984). It is worth noting however that this progressive shift requires a significant period of time to take place and the magnitude of change is often small (Pette, 1984). As expected, the effect of training cessation on muscle fibre distribution depends on the duration of the period of inactivity (Mujika & Padilla, 2001b). While short-term training cessation (i.e. three weeks or less) is not enough to induce any changes

In summary, these results suggest the existence of two distinct phases in the physiological mechanisms underlying the continuous decrease in VO2max that is observed in welltrained endurance athletes once they stop training. During a first phase lasting 21 to 28 days, the decrease in VO2max is mainly the consequence of a loss of central adaptation, as

102

Detraining (Hortobagyi et al., 1993; Houston et al., 1979), long term inactivity periods (up to several years) have been associated with a progressive return to baseline (Coyle et al., 1984; Larsson & Ansved, 1985).

dehydrogenase and malate dehydrogenase followed the same pattern of disadaptation (Coyle et al., 1984; 1985). Similar results have been observed in runners (Houmard et al., 1992; Houston et al., 1979), triathletes (McCoy et al., 1994) or soccer players (Amigó et al., 1998). Simsolo et al. (1993) also observed a large reduction of muscle lipoprotein lipase activity after two weeks of training cessation in 16 endurance athletes, which undoubtedly altered the capacity to spare carbohydrate by using more fatty acids as energy substrate.

Non-proteic respiratory exchange ratio (RER) is commonly used to estimate the respective contribution of fatty acids and glucose to energy production (Péronnet & Massicotte, 1991). Endurance training has long been associated with a reduced RER at both maximal and submaximal exercise intensities, thus suggesting a reduced reliance on glucose for energy production. Training cessation results in a rapid increase in RER that appears to reach a plateau within 14 days (Figure 10.3), as well as a rapid decrease in muscle glycogen stores (up to 20% within 1 week of bed rest or training cessation) (Costill et al., 1985; Mikines et al., 1989). The rapid decrease in the glucose transporter protein GLUT-4 concentration reported after 6 to 10 days of training cessation (Vukovich et al., 1996), together with the important drop of glycogen synthase activity after just 5 days of training cessation (Mikines et al., 1989) is thought to play a major role in this process (Mujika & Padilla, 2000a; Mujika & Padilla, 2000b).

The lactate concentration to a given submaximal exercise intensity is one of the numerous methods used to determine aerobic endurance (Bosquet et al., 2002). The lower its concentration, the better the aerobic endurance. Considering the short and long term loss of adaptation that affect some of the physiological factors underlying aerobic endurance, it is expected that this important determinant of endurance performance is altered by training cessation. As shown in Figure 10.4, blood lactate concentration increases exponentially with training cessation duration, suggesting that aerobic endurance decreases rapidly when the training process is interrupted. Although a steady state value is reached around 21 to 28 days, one can expect a further decrease in aerobic endurance that results from the progressive decrease of type I muscle fibres.

Figure 10.3. Effect of training cessation on the respiratory exchange ratio during exercise. RER: respiratory exchange ratio. Figure 10.4. Effect of training cessation on the blood lactate concentration during exercise.

Endurance training increases the number and size of the muscle fibre mitochondria, as well as the activity of oxidative enzymes (Abernethy et al., 1990). One of the main characteristics of muscular detraining is an important decrease of this activity (Mujika & Padilla, 2001b). Coyle et al. (1984, 1985) reported that citrate synthase activity declined by 23% during the first 3 weeks of training cessation in endurance trained athletes, by 23% again from the 4th to the 8th week and stabilized thereafter. Succinate

In summary, aerobic endurance decreases very rapidly once training ceases, most probably for metabolic reasons. An additional and delayed decrease remains possible when the duration of training cessation is long enough to alter muscle fibre distribution.

103


Energy Cost of Locomotion

In summary, the oxygen uptake required to run at a given speed does not appear to be altered by training cessation. However the concomitant increase in RER and decrease in VO2max result in a decreased exercise tolerance at a given speed, since it corresponds to a higher relative intensity and more glucose is needed for ATP resynthesis while the glycogen stores are markedly decreased.

The energy cost of locomotion (Cr) represents the energy demand to move at a given submaximal power output or speed. The lower the Cr, especially when body mass is accounted for such as in running, the lower the energy expenditure to move at a given velocity and the better the endurance performance. Factors affecting Cr are numerous and have been thoroughly reviewed by Saunders et al. (2004). Some of them are not changeable (e.g. height), while others can be manipulated (e.g. stride biomechanics, strength, elastic store-recoil capacity). Numerous interventions such as plyometric (Berryman et al., 2010) or high intensity interval training (Saunders et al., 2004) are effective to decrease Cr and improve performance.

Practical Implications Previous sections described the consequences of training cessation on the physiological determinants of endurance performance. It is important for coaches to know whether an alternative training strategy is efficient to limit these consequences, particularly when the athlete is injured.

In addition to VO2max and its determinants, Coyle et al. (1985) also examined the response to submaximal intensity exercise after 12, 21, 56 and 84 days of training cessation. Interestingly, the VO2 response for the same absolute intensity remained stable during this period, suggesting that the energy required to develop this power output was not affected by the lack of training. This is in agreement with the finding by Houmard et al. (1992) that Cr was not altered by a 14-day training cessation period in 12 distance runners. As already mentioned, the ability to store and recoil elastic energy as well as maximal strength are recognized as important determinants of Cr (Saunders et al., 2004). We recently performed a meta analysis to examine the effect of training cessation on maximal force and maximal power and found that both neuromuscular qualities could be maintained for up to 3-4 weeks before declining. This ability to maintain strength performance is probably related with the ability to maintain Cr.

As already discussed, the factors underpinning the continuous decrease of VO2max depend on the duration of training cessation. They are mainly central Qmax during the first 3-4 weeks, and mainly peripheral a-vDO2max afterwards. Considering that central adaptations and disadaptations are not specific to the trained muscles, an alternative training can be implemented to avoid or limit detraining while an athlete is injured. Deep water running has been shown to be effective for this purpose (Chu & Rhodes, 2001). For example, Bushman et al. (1997) found that VO2max, Cr, aerobic endurance and ultimately 5 km performance could be maintained in 11 well-trained runners who substituted their usual on-land training by deep water running for a period of 4 weeks. One leg cycling represents another exercise modality that can be used to limit the central effect of training cessation in injured athletes. Olivier et al. (2010) randomized 24 soccer players with anterior cruciate ligament reconstruction in a control group that followed a classic rehabilitation program and an experimental group that added aerobic training of the untreated leg to the rehabilitation program. Stroke volume and VO2max were maintained in the experimental group while they decreased by ~20 and 10% respectively in the control group. Arm cranking represents an alternative modality of cardiovascular training that is commonly used in the conditioning of spinal cord injury patients (Figoni, 1990). Considering that arm VO2max represents roughly 70 to 80% of leg VO2max (Secher & Volianitis, 2006), arm cranking allows to reach exercise intensities that should be high enough to maintain (or limit the decrease of) Qmax. Pogliaghi et al. (2006) provided data that tended to confirm this hypothesis, since they found in 12 healthy men aged 67 ± 5 years that arm cranking and leg cycling were equally effective in improving maximal and submaximal exercise capacity, and that roughly 50% of this improvement was due to central adaptations. It should be noted however

However, it is important to keep in mind that although the oxygen demand remains stable, the strategy used by the subjects to match this energy demand changed significantly over time, since the RER increased linearly with the duration of training cessation (from 0.93 ± 0.01 at baseline to 1.00 ± 0.01 at day 84, corresponding to a ~8% difference). Considering the decrease in VO2max we already discussed, the relative intensity of this power output increased with the duration of training cessation from 74 ± 2% at baseline to 90 ± 3% at day 84 (~22% difference). Perceived exertion logically increased from 12.3 ± 0.4 at baseline to 17.1 ± 0.4 at day 84 (~39% difference). In view of the increase in RER and likely concomitant decrease in glycogen stores (see the preceding section), one can easily hypothesize that although Cr is not affected, time to exhaustion at a given intensity is significantly altered.

104

Detraining that arm cranking appears to be less well tolerated by athletes than one leg cycling (Olivier et al., 2008). While other modes of locomotion than the sport-specific one can also be used as alternative exercises, it is worth noting that transfer effects between modes are sometimes limited, particularly when cycling or running are substituted by swimming (Tanaka, 1994).

the physiological consequences of implementing no alternative training. t $IPPTF UIF NPTU BQQSPQSJBUF BMUFSOBUJWF USBJOJOH according to the cause of training cessation and its anticipated duration. t 3FTVNF OPSNBM USBJOJOH QSPHSFTTJWFMZ FWFO XIFO UIF duration of training cessation is short. t 8IFOUSBJOJOHDFTTBUJPOFYDFFETUPXFFLT TUSVDUVSBM disadaptations will occur which require the training program to go back to the preceding cycle.

Metabolic consequences of training cessation occur rapidly and affect both substrate utilization and glycogen stores (Mujika & Padilla 2001a). These adaptations are peripheral (i.e. specific to the trained muscles). If it is possible to implement an alternative training including exercises that involve the same muscle groups than the competitive activity, for example deep water running for an athlete who suffers an ankle sprain or an Achilles tendinosis, then metabolic adaptations should be maintained. Otherwise, athletes can eventually maintain their VO2max if an alternative training including exercises that are not specific to their sport specific muscle groups is implemented, but their aerobic endurance will dramatically decrease. Consequently, care should be taken to increase the training load progressively when athletes resume training, since they may eventually be able to maintain the same intensity than before their injury, but not the same volume at this intensity. Finally, when it is not possible to mobilize trained muscles for a period longer than 3 to 4 weeks, peripheral disadaptations will occur and require going through previous training cycles to restore initial adaptations.

Summary t .PTU PG UIF QIZTJPMPHJDBM EFUFSNJOBOUT PG FOEVSBODF performance decline rapidly once the training process is interrupted, leading to detraining and impaired performance capacity. t ,OPXJOH UIF LJOFUJDT PG UIFTF EJTBEBQUBUJPOT BMMPXT athletes and coaches to implement alternative strategies limiting the effect of training cessation. t 702max decreases exponentially with the duration of training cessation. t 2max is altered before a-vDO2max, with a cut off duration of 3-4 weeks. t .FUBCPMJD EJTBEBQUBUJPOT PDDVS WFSZ SBQJEMZ BOE negatively affect aerobic endurance. t ćF FOFSHZ DPTU PG SVOOJOH JT MFTT BČFDUFE CZ USBJOJOH cessation than other determinants of endurance performance. t &OEVSBODFQFSGPSNBODFJTEFDSFBTFECZUPEVSJOH periods of training cessation lasting 3-4 weeks or longer. t 8IFO UIF USBJOJOH QSPDFTT JT JOUFSSVQUFE NPTU PęFO because of an injury, athletes and coaches should estimate

105


References Abernethy, P.J., Thayer, R. & Taylor, A.W. (1990). Acute and chronic responses of skeletal muscle to endurance and sprint exercise. A review. Sports Medicine, 10, 365-389. Amigó, N., Cadefau, J.A., Ferrer, I., Terrados, N. & Cusso, R. (1998). Effect of summer intermission on skeletal muscle of adolescent soccer players. Journal of Sports Medicine and Physical Fitness, 38, 298-304. Berryman, N., Maurel, D. & Bosquet, L. (2010). Effect of plyometric vs. dynamic weight training on the energy cost of running. Journal of Strength and Conditioning Research, 24, 1818-1825. Bosquet, L., Léger, L. & Legros, P. (2002). Methods to determine aerobic endurance. Sports Medicine, 32, 675-700. Bushman, B.A., Flynn, M.G., Andres, F.F., Lambert, C.P., Taylor, M.S. & Braun, W.A. (1997). Effect of 4 wk of deep water run training on running performance. Medicine and Science in Sports and Exercise, 29, 694-699. Chu, K.S. & Rhodes, E.C. (2001). Physiological and cardiovascular changes associated with deep water running in the young: possible implications for the elderly. Sports Medicine, 31, 33-46. Costill, D.L., Fink, W.J., Hargreaves, M., King, D.S., Thomas, R. & Fielding, R. (1985). Metabolic characteristics of skeletal muscle during detraining from competitive swimming. Medicine and Science in Sports and Exercise, 17, 339-343. Coyle, E.F., Hemmert, M.K. & Coggan, A.R. (1986). Effects of detraining on cardiovascular responses to exercise: role of blood volume. Journal of Applied Physiology, 60, 95-99. Coyle, E.F., Martin, W.H., Bloomfield, S.A., Lowry, O.H. & Holloszy, J.O. (1985). Effects of detraining on responses to submaximal exercise. Journal of Applied Physiology, 59, 853-859. Coyle, E.F., Martin, W.H., Sinacore, D.R., Joyner, M.J., Hagberg, J.M. & Holloszy, J.O. (1984). Time course of loss of adaptations after stopping prolonged intense endurance training. Journal of Applied Physiology, 57, 1857-1864. Cullinane, E.M., Sady, S.P., Vadeboncoeur, L., Burke, M. & Thompson, P.D. (1986). Cardiac size and O2max do not decrease after short-term exercise cessation. Medicine and Science in Sports and Exercise, 18, 420424. Di Prampero, P.E., Atchou, G., Bruckner, J.C. & Moia, C. (1986). The energetics of endurance running. European Journal of Applied Physiology, 55, 259-266. Drinkwater, B.L. & Horvath, S.M. (1972). Detraining effects on young women. Medicine and Science in Sports, 4, 91-95. Figoni, S.F. (1990). Perspectives on cardiovascular fitness and SCI. Journal of the American Paraplegia Society, 13, 63-71. Hortobagyi, T., Houmard, J.A., Stevenson, J.R., Fraser, D.D., Johns, R.A. & Israel, R.G. (1993). The effects of detraining on power athletes. Medicine and Science in Sports and Exercise, 25, 929-935. Houmard, J.A., Hortobagyi, T., Johns, R.A., Bruno, N.J., Nutte, C.C., Shinebarger, M.H. & Welborn, J.W. (1992). Effect of short term training cessation on performance meausres in distance runners. International Journal of Sports Medicine, 13, 572-576. Houston, M.E., Bentzen, H. & Larsen, H. (1979). Interrelationships between skeletal muscle adaptations and performance as studied by detraining and retraining. Acta Physiologica Scandinavica, 105, 163-170. Larsson, L. & Ansved, T. (1985). Effects of long-term physical training and detraining on enzyme histochemical and functional skeletal muscle characteristic in man. Muscle Nerve, 8, 714-722. Madsen, K., Pedersen, P.K., Djurhuus, M.S. & Klitgaard, N.A. (1993). Effects of detraining on endurance capacity and metabolic changes during prolonged exhaustive exercise. Journal of Applied Physiology, 75, 1444-1451. McCoy, M., Proietto, J. & Hargreaves, M. (1994). Effect of detraining on GLUT-4 protein in human skeletal muscle. Journal of Applied Physiology, 77, 1532-1536. Mikines, K.J., Sonne, B., Tronier, B. & Galbo, H. (1989). Effects of acute exercise and detraining on insulin action in trained men. Journal of Applied Physiology, 66, 704-711.

Moore, R.L., Thacker, E.M., Kelley, G.A., Musch, T.I., Sinoway, L.I., Foster, V.L. & Dickinson, A.L. (1987). Effect of training/detraining on submaximal exercise responses in humans. Journal of Applied Physiology, 63, 1719-1724. Mujika, I. & Padilla, S. (2000a). Detraining: loss of a training induced physiological and performance adaptations. Part I. Sports Medicine, 30, 79-87. Mujika, I. & Padilla, S. (2000b). Detraining: loss of training-induced physiological and performance adaptations. Part II. Sports Medicine, 30, 145-154. Mujika, I. & Padilla, S. (2001a). Cardiorespiratory and metabolic characteristics of detraining in humans. Medicine and Science in Sports and Exercise, 33, 413-421. Mujika, I. & Padilla, S. (2001b). Muscular charateristics of detraining in humans. Medicine and Science in Sports and Exercise, 33, 1297-1303. Neufer, P.D., Costill, D.L., Fielding, R.A., Flynn, M.G. & Kirwan, J.P. (1987). Effect of reduced training on muscular strength and endurance in competitive swimmers. Medicine and Science in Sports and Exercise, 19, 486-490. Olivier, N., Legrand, R., Rogez, J., Berthoin, S., Prieur, F. & Weissland, T. (2008). One-leg cycling versus arm cranking: which is most appropriate for physical conditioning after knee surgery? Archives of Physical Medicine and Rehabilitation, 89, 508-512. Olivier, N., Weissland, T., Legrand, R., Berthoin, S., Rogez, J., Thevenon, A. & Prieur, F. (2010). The effect of a one-leg cycling aerobic training program during the rehabilitation period in soccer players with anterior cruciate ligament reconstruction. Clinical Journal of Sport Medicine, 20, 28-33. Péronnet, F. & Massicotte, D. (1991). Table of nonprotein respiratory quotient: an update. Canadian Journal of Applied Physiology, 16, 23-29. Péronnet, F. & Thibault, G. (1989). Mathematical analysis of running performance and world running records. Journal of Applied Physiology, 67, 453-465. Pette, D. (1984). J.B. Wolffe memorial lecture. Activity-induced fast to slow transitions in mammalian muscle. Medicine and Science in Sports and Exercise, 16, 517-528. Pogliaghi, S., Terziotti, P., Cevese, A., Balestreri, F. & Schena, F. (2006). Adaptations to endurance training in the healthy elderly: arm cranking versus leg cycling. European Journal of Applied Physiology, 97, 723-731. Raven, P.B., Welch-O’Connor, R.M. & Shi, X. (1998). Cardiovascular function following reduced aerobic activity. Medicine and Science in Sports and Exercise, 30, 1041-1052. Saltin, B. & Astrand, P.O. (1967). Maximal oxygen uptake in athletes. Journal of Applied Physiology, 23, 353-358. Saunders, P.U., Pyne, D.B., Telford, R.D. & Hawley, J.A. (2004). Factors affecting running economy in trained distance runners. Sports Medicine, 34, 465-485. Secher, N.H. & Volianitis, S. (2006). Are the arms and legs in competition for cardiac output? Medicine and Science in Sports and Exercise, 38, 17971803. Simsolo, R.B., Ong, J.M. & Kern, P.A. (1993). The regulation of adipose tissue and muscle lipoprotein lipase in runners by detraining. Journal of Clinical Investigation, 92, 2124-2130. Tanaka, H. (1994). Effects of cross training. Sports Medicine, 18, 330-339. Vukovich, M.D., Arciero, P.J., Kohrt, W.M., Racette, S.B., Hansen, P.A. & Holloszy, J.O. (1996). Changes in insulin action and GLUT-4 with 6 days of inactivity in endurance runners. Journal of Applied Physiology, 80, 240-244.

106