review article received: 2015-08-07
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UDC: 796.015:613.2
AN OVERVIEW OF TRAINING METHODS THAT PROMOTE THE HIGHEST LIPID OXIDATION DURING AND AFTER A SINGLE EXERCISE SESSION
Barbara PURKART1, Boštjan ŠIMUNIČ2, Mitja GERŽEVIČ2
'Physiotherapy Centre Barbara Purkart k.d., Ulica Gradnikove brigade 8, 1000 Ljubljana,
Slovenia
2University of Primorska, Science and Research Centre, Institute for Kinesiology Research, Garibaldijeva 1, 6000 Koper, Slovenia
Corresponding author: Mitja GERŽEVIČ
University of Primorska, Science and Research Centre, Institute for Kinesiology Research, Garibaldijeva 1, 6000 Koper, Slovenia Tel.: +386 5 663 58 05, +386 5 663 77 31 e-mail: mitja.gerzevic@zrs.upr.si
ABSTRACT
Given that physical activity is the most effective way to increase lipid oxidation, its effects are influenced by several factors. The goal of this review was to identify the most effective methods that facilitate the highest lipid oxidation during and after a single exercise session. For this purpose, the available scientific literature was examined using Pu-bMed, Web of Science, Google Scholar and Cochrane Library databases up to June 2013 with the following keywords: excess post exercise oxygen consumption, exercise fatty acid, energy expenditure exercise and interval training. From the identified 48,583 potentially relevant references, 172 of them met all the required criteria. It was found out that prolonged (> 30 min) moderate intensity (55 - 70 % VO.max) exercise such as walking, jogging or cycling is the most effective way to increase lipid oxidation during and after a ssingle exercise session. Low-volume high-intensity interval exercise is supposed to be as effective as traditional exercise with continuous endurance, with the main effect on lipid oxidation after the session and similar long-term metabolic adaptations. However, more research is still needed to compare the effects of regular resistance exercise with traditional endurance and high-intensity interval exercise. Finally, nutrition is also a significant factor since food rich in fat and low in carbohydrates promotes greater lipid oxidation.
Keywords: endurance exercise, interval exercise, training, nutrition, fatty acid, tri-acylglycerol.
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PREGLED VADBENIH METOD, KI SPODBUDIJO NAJVEČJO OKSIDACIJO LIPIDOV MED IN PO POSAMEZNI VADBENI ENOTI
IZVLEČEK
Glede na to da je gibalna oz. telesna aktivnost najbolj učinkovit način povečanja oksidacije maščob, pa na njihovo porabo vpliva še vrsta drugih dejavnikov. Cilj tega preglednega članka je bil ugotoviti vplive in najbolj učinkovite metode za spodbujanje oksidacije maščobnih kislin med vadbeno enoto in po njej. Pregledali smo razpoložljive članke, ki so bili objavljeni do junija 2013 v sledečih bazah: PubMed, Web of Science, Google scholar in Cochrane Library. Pri iskanju smo uporabili naslednje ključne besede: poraba kisika po vadbi, poraba maščobnih kislin med telesno aktivnostjo, poraba energije med telesno aktivnostjo in intervalni trening. Tako smo dobili 48.583 člankov, od katerih je našim kriterijem ustrezalo 172 člankov. Ugotovili smo, da je dolgotrajna telesna aktivnost srednje intenzivnosti, kot sta hoja in lahkoten tek, najbolj učinkovit način za povečevanje oksidacije maščobnih kislin. Visokointenzivna intervalna vadba je bolj učinkovita s stališča porabe energije, vendar pri enaki porabi maščobnih kislin. Potrebnih bo še nekaj nadaljnjih raziskav, ki bodo primerjale učinke redne vadbe za moč ter redne klasične aerobne in intervalne vadbe za razvoj vzdržljivosti. K večji oksi-daciji maščobnih kislin pomembno vpliva tudi prehrana: hrana, bogata z maščobami in z nizko vsebnostjo ogljikovih hidratov, najbolj vzpodbuja oksidacijo maščobnih kislin.
Ključne besede: vadba vzdržljivosti, intervalna vadba, trening, prehrana, maščob-ne kisline, triglicerol
INTRODUCTION
Two of the greatest health threats in modern lifestyle are imbalanced nutrition and a sedentary lifestyle. Excessive diet and an increased sedentary lifestyle lead to obesity and metabolic syndrome which are both associated with numerous comorbidities (Poirier et al., 2006). An excessive carbohydrate intake, especially fructose, leads to an increase in body weight, visceral adipose tissue, muscle fat, as well as liver fat; furthermore, sugar enhances lipogenesis and the production of uric acid including an increase in plasma triacylglycerols (TG) concentrations (Bray, 2013). Lipids are implicated in the pathogenesis of several common human diseases, including: metabolic syndrome, cardiovascular disease and type 2 diabetes (Kiens, 2006). Enhanced lipid oxidation might be beneficial for counteracting lipid accumulation. Physical activity (PA) is the most effective way to increase lipid oxidation, due to the fact that it increases the metabolic rate (Kiens, Alsted, & Jeppesen, 2011). During PA the body has a higher energy demand. The body provides energy for PA converting chemical energy
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to mechanical energy and heat. This chemical energy is derived from macronutrients (carbohydrates, proteins and lipids) in the body and converted to adenosine triphosphate (ATP) energy molecules, which are used for work. Depending on the intensity and the duration of PA, different metabolic pathways provide energy: ATP-phosphocreatine (PCr) system, anaerobic glycolysis and aerobic glycolysis with carbohydrate, protein and lipid oxidation (Frayn, 2010; McArdle, Katch, & Katch, 2010). Normally, during prolonged low- to moderate- PA intensities (33 - 65 % of maximal oxygen consumption - VO2max), lipids metabolised at the highest rate, reaching their maximum at ~64 ± 4 % VO2max, whereas, at higher intensities, carbohydrates become the primary energy source (Achten, Gleeson, & Jeukendrup, 2002; Perez-Martin et al., 2001). The type of energy source used depends on several factors, not just intensity, but also duration and the type of PA (Antonutto & di Prampero, 1995), gender, aerobic fitness, nutrition (Kiens, 2006), substrate availability within skeletal muscles (Jeppesen & Kiens, 2012; Kiens et al., 2011), amount of fatty tissue and the neuro-hormonal influence on the oxidation (Astrup et al., 1992; Mittendorfer, Fields, & Klein, 2004). However, during PA, the lipid used for energy turnover is derived from different sources (Kiens, 2006; Kiens et al., 2011): blood fatty acids bound to albumin, fatty acids liberated from the hydrolysis of circulating TG and fatty acids from lipolysis of TG located in lipid droplets in skeletal muscles - muscle TG.
Given that endurance PA is the most effective way to increase lipid oxidation (Kiens et al., 2011), its effects are influenced by several factors, and because different types of interval training and resistance exercise are used and promoted in sport and kinesiology practice, it will be the goal of this review to identify what are the influences and which are the most effective methods for facilitating the highest lipid oxidation during and after a single workout.
METODHS
For the purposes of this review, the available articles in PubMed, Web of Science, Google Scholar and Cochrane Library were analysed up to June 2013. The following keywords were used for searching: excess post exercise oxygen consumption, exercise fatty acid, energy expenditure exercise and interval training. This search strategy identified 48,583 potentially relevant references, while only 172 articles met all the search topic requirements.
LIPID OXIDATION DURING ENDURANCE PHYSICAL ACTIVITY
The factors influencing lipid oxidation during endurance physical activity are: intensity, duration and type of PA, food intake, amount of fatty tissue, gender and physical fitness.
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Effect of Intensity on Lipid Oxidation during Activity
PA can be divided into low-, moderate-, and high- intensity activities. In literature, boundaries between these levels are not strictly defined and they range from up to 55 % VO_ for low-intensity, from 55 % to 70 % VO_ for moderate-intensity, and excee-
2max	J 7	2max	J 7
ding 75 % VO2max for high-intensity PA. During low and moderate-intensity endurance PA, the predominant energy sources are lipids (Pillard et al., 2010). Lipid oxidation during high-intensity PA is lower than during moderate-intensity (Jeppesen & Kiens, 2012). At the beginning of the previous century, it was discovered that by measuring the respiratory exchange ratio (RER), which is the ratio between eliminated CO2 and utilized O2 during respiration, it is possible to determine also the type of energy source used (Scott, 2005). If RER is around 1, the body uses carbohydrates, while if it is between 0.7 and 0.8, the body uses more lipids (Walsch, 2003) for energy transfer. By measuring RER, it was discovered that lipid oxidation increases from rest to an intensity level of 65 % VO2max. Lipid oxidation during endurance PA that lasts from 60 to 90 min increases by 5 to 10 times (Krogh & Lindhard, 1920, in Jeppesen & Kiens, 2012; Cristensen & Hansen, 1939, in Jeppesen & Kiens, 2012). Further studies using RER measurements and monitoring of isotopes have confirmed the highest oxidation of lipids during moderate-intensity endurance PA, namely, at the intensity level of 65 % VO2max, compared to low-intensity (25 % VO2max) and high-intensity (85 % VO2max) (Romijnet al., 1993). With the increased intensity of PA, lipid oxidation decreases. During 30 minutes of cycling, for example, at the intensity level of 75%, lipid oxidation is lower than at the intensity level of 55 % VO2max (van Loon et al., 2001). Even though, it has been known for almost a century that a total amount of oxidised fatty acids during high-intensity PA is lower than during moderate-intensity PA, the mechanisms behind this are still not clear. The limiting factor of fatty acid oxidation during the transition from rest to low or moderate-intensity PA is most probably the transport of fatty acid through the sarcolem-ma (Bonen, Luiken, Arumugam, Glatz, & Tandon, 2000; Jepessen et al., 2011). When considering transition from moderate to high intensity PA, some earlier authors argue that oxidation of plasma fatty acids, lipoprotein derived TGs and muscular TGs probably decrease due to unavailability of free carnitine and / or decrease in the intracellular pH, but not as a consequence of a decrease in plasma free fatty acids availability (van Loon, Greenhaff, Constantin Teodosiu, Saris, & Wagenmakers, 2001). Modern studies prefer the notion that the availability of free carnitine in blood is the sole factor limiting the transport of fatty acids to the mitochondria in the muscle (Roepstorff et al., 2005; Kiens et al., 2011; Jeppensen & Kiens, 2012). When considering lipid oxidation during endurance PA, moderate intensity is shown as the most effective from the point of highest lipid oxidation during PA.
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Effects of Duration and Type of Activity on Lipid Oxidation during Activity
The type of energy source used during PA is not determined only by intensity level (as described above), but also by duration and type of PA. Phosphagens (adenosine triphosphate and creatine phosphate) are used during the first 5 to 10 seconds of maximum PA, followed by (rapid) anaerobic glycolysis, if maximum effort continues beyond 10 seconds (obviously the intensity decreases). At this stage, glycolysis maintains the energy transfer up to 2 or 3 minutes, with the glycogen in the muscle as the main energy source (McArdle et al., 2010). When intense exercise continues beyond several minutes, aerobic metabolism provides nearly all of the energy transfer. At this point, fat becomes the primary energy fuel and lipid oxidation the primary process of energy transfer for exercise and recovery when high-intensity, long-duration exercise depletes glycogen (McArdle et al., 2010) or when carbohydrates sparing and promotion of fat utilization occur as a training adaptation (Ástrand, Rodahl, Dahl, & Stromme, 2003; Fox & Mathews, 1981).
There are various lipids sources. During moderate-intensity PA, less than a half of lipids is derived from upper-body subcutaneous adipose tissue, a quarter comes from muscular TGs, and the rest is distributed among fatty acids from lower-body subcutaneous adipose tissue, intra-abdominal adipose tissue, plasma TGs and other (Horowitz, 2003). If PA is so intense or long that glycogen stores are exhausted, the energy derived from glycogen breakdown is supplemented by the breakdown of proteins (Kis-ner & Colby, 2007). Nonetheless, the total energy expenditure of jogging exceeds that of walking (Wilkin, Cheryl, & Haddock, 2012), fractional lipid oxidation remains at comparable levels, since the respiratory exchange ratio does not demonstrate a discernible pattern between walking and running (Stamford, 1975), meaning that carbohydrate and lipid oxidation increase simultaneously. At same relative intensity, expressed in per cent of VO2max, lipid oxidation is significantly higher while running compared to cycling (Capostagno & Bosch, 2010), also, more energy is being utilised (Zeni, Hoffman, & Clifford, 1996; Kravitz, Robergs, Heyward, Wagner, & Powers, 1997). When considering lipid oxidation, moderate intensity activity has to last at least 20 minutes to begin utilising lipids. The upper limit is dependable on individual body's glycogen storage capacity, to avoid undesirable protein depletion. Jogging and walking are shown to be more effective at lipid oxidation than cycling.
Effects of Food Ingestion on Lipid Oxidation during Activity
The ingested food has also an effect on lipid oxidation as muscles adjust the levels of muscle enzymes depending on the food ingested (Spriet, 2011). In addition, most liver enzymes, which regulate glycolysis and fatty acid oxidation, are also regulated by nutrient availability (Rui, 2014). A 7-week diet, rich in fats, increases muscles' ability to metabolized lipids, by increasing activity of enzymes and binding proteins, involved in the process of fatty acid oxidation in the muscle (Helge & Kiens, 1997; Kiens,
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2006). When untrained men were consuming fat rich diet for three days leading up to a moderate-intensity PA (cycling at an intensity of 70 % VO2max), lipid oxidation was significantly higher, compared to when they consumed a diet rich in carbohydrates (Christensen & Hansen, 1939, in Kiens et al., 2011). In the study performed by Galbo, Holst, and Christensen (1979), seven untrained men ran on a treadmill at 70 % VO2max intensity until exhaustion. Four days prior to the PA they were consuming carbohydrate and fat rich diets respectively. When they consumed fats, their glucagon, epinephrine, cortisol and growth hormone levels rose significantly compared to the carbohydrate diet. Food consumption in the days leading up to the PA affected not only their bodies' energy stores, but also their hormone reaction, directly affecting their oxidation during PA. Food rich in carbohydrates, on the other hand, promotes oxidation of glucose, production of lactate and inhibits oxidation of lipids (Galbo et al., 1979). A more recent study by Helge found once again a significantly greater lipid oxidation in the group that consumed fat rich diet (Helge, Richter, & Kiens, 1996; Helge, Wulff, & Kiens, 1998). Measuring exhaustion time parameters at the same absolute workload showed that endurance performance was enhanced similarly after both two and four weeks of adaptation to training and a fat-rich or a carbohydrate-rich diet (Helge et al., 1998). Helge, Watt, Richter, Rennie, and Kiens (2001) also demonstrated that circulating TG made a significant contribution to fuel utilization during endurance training after adaptation to a fat-rich diet. The increased lipid oxidation observed after training (cycling 60 to 75 minutes per session at 65 to 85 % VO2max, four times per week, seven weeks) and fat diet adaptation originated from both a higher plasma fatty acid oxidation and utilization of circulating TG. In contrast, the carbohydrate sparing observed after fat diet adaptation was due to muscle glycogen sparing and not to a diminished plasma glucose uptake (Helge et al., 2001). A longer-term adaptation to a fat-rich diet also leads to measurable changes in the capacity to recruit, transport and oxidize lipids (Helge & Kiens, 1997).
Another physiological process that increases lipid oxidation is starvation (Cahill, 2006). In the fasted state, fatty acids are oxidized mainly in the mitochondria to generate energy supply as well as ketone bodies (Rui, 2014). Free fatty acid levels were increased approximately 9-fold after 60 h of fasting in healthy male subjects, leading to elevated muscular TG levels and decreased muscular insulin sensitivity (Hoeks et al., 2010). Despite an increase in whole-body lipid oxidation, Hoeks et al. (2010) observed a reduction in mitochondrial capacity. Van Proeyen, Szlufcik, Nielens, Ramaekers, and Hespel (2011) investigated the effect of endurance training in the fasted state vs. training in the fed state on muscle oxidation and substrate utilization. They found out that moderate-intensity endurance training on an empty stomach significantly stimulates muscle cells to increase lipid oxidation and facilitate utilizing muscular TGs, compared to the group that consumed carbohydrates prior to, and during PA (untrained men, cycling 60 to 90 minutes daily for 6 weeks at intensity level of 70 % VO2max) (Van Proeyen et al., 2011). Availability of endogenous fuels in muscles affects lipid oxidation in muscles as well as on the level of entire body. The amount of muscular TGs in muscles before the activity also influences lipid oxidation, in addition to intensity, duration and type of activity as well as gender, fitness level and ingested food (Kiens, 2006). Mode-
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rately trained boys showed 2.5 times local lipid oxidation in their muscles when they consumed fat rich diet, compared to carbohydrate rich diet (which replenished glycogen stores in muscles), at same workload (60 minutes of cycling at 65 % VO2max intensity). Since it is spent for acetyl-carnitine formation, free carnitine availability significantly decreases, reducing lipid oxidation capability during endurance PA (Roepstorff et al., 2005). When muscle glycogen stores are low, a two times higher concentration of fatty acids can be observed in the plasma, as well as a significantly increased concentration of enzymes and binding proteins that participate in lipid oxidation (Wojtaszewski et al., 2003). It has been shown that glycogen stores are inversely proportional to the levels of free carnitine. When glycogen stores in muscles are high, there is very little free carnitine in the cells; this limits fatty acid transport into mitochondria, which consequently limits lipid oxidation in the muscles (Jeppesen & Kiens, 2012). The intake of carnitine dietary supplement increased ability to metabolise lipids during low-intensity endurance PA (untrained healthy men cycled for 30 minutes at 50 % VO2max intensity), a 44 % decrease in Lactate concentration in the blood during high-intensity PA (30 minutes of cycling at 80 % VO2max intensity) was also observed (Wall et al., 2011). This may indicate increased lipid oxidation while taking carnitine dietary supplement at higher intensities as well (Jeppesen & Kiens, 2012). When considering lipid oxidation, after adaptation to a high-fat diet due to an increased uptake of lipids originating from the bloodstream and only a minor extent to an increased muscle TG utilization, greater lipid oxidation is observed during PA. The intake of carnitine dietary supplement might also stimulate lipid oxidation. Training on an empty stomach stimulates muscle cells to increase lipid oxidation and facilitate utilizing muscular TGs.
Effects of Adipose Tissue Amounts on Lipid Oxidation during Activity
The amount of fat tissue also affects the capability of lipid oxidation. Chronic imbalances between energy intake and oxidation ultimately result in excess intracellular lipid accumulation, both at the whole body level and in individual organs or tissues. Obese and overweight people have a higher concentration of plasma fatty acids, most likely due to increased fatty acid release from an expanded fat mass; providing a link between obesity and ectopic lipid accumulation (Savage, Petersen, & Schulman, 2007). "Sedentary overweight subjects, compared to controls at the same exercise intensities, exhibit an alteration of the balance of substrate oxidation, reflected by lower rates of lipid oxidation and a shift of quantitative parameters to lower intensities" (Perez-Martin et al., 2001). The amount of fatty acids increases as a reaction to low-intensity PA (untrained men cycling for 90 minutes at 50 % VO2max intensity). The increase in fatty acids oxidation during exercise is ~ 50 % lower in obese and ~ 35 % lower in overweight people when compared to lean controls (Scheen, Pirnay, Luyckx, & Lefebvre, 1983; Mittendorfer et al., 2004). The obese have four times higher transport of fatty acids through sarcolemma (Bonen et al., 2004) and fatty acids penetrate into muscles, where they accumulate as muscular TGs (Goodpaster, Theriault, Watkins, & Kelley, 2000).
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The accumulation of muscular TGs in muscles may result in insulin resistance and the development of diabetes (Kelley & Goodpaster, 2001). The rate of total fat oxidation, assessed by indirect calorimetry during the last 30 minutes of exercise, was not significantly different between groups: lean, overweight and obese (Mittendorfer et al., 2004). That is why comparable RER levels were measured in overweight and lean untrained men (30 minutes cycling at anaerobic threshold) (Wong & Harber, 2006). Fat oxidation provided ~30 % of total energy requirements during the exercise in lean, overweight, and obese men. However, the source of fatty acids used as fuel during the exercise varied between groups. In lean subjects about one-half of the fatty acids oxidized during the exercise, having derived from systemic plasma fatty acids and the other half from non-systemic fatty acids. The relative contribution of systemic plasma fatty acids to total fat oxidation decreased and the relative contribution of non-systemic fatty acid to total fat oxidation increased with increasing adiposity. Presumably, the predominant source of non-systemic fatty acids was the fatty acids that were released during lipolysis of intramuscular TG (Mittendorfer et al., 2004).
"Lipid accumulation in skeletal muscle and liver may be a result of increased delivery / synthesis of fatty acids to / in these tissues in those conditions in which energy intake exceeds adipose tissue storage capacity (as seen in obesity and lipodystrophy), or a consequence of either acquired or inherited mitochondrial dysfunction" (Savage et al., 2007). Obese people have a lower expression of the adipose tissue hormone adiponectin (Civitarese et al., 2006), which is one of the hormones (along with leptin and FGF21) that enhance mitochondrial proliferation in white adipose tissue and whole-body energy expenditure associated with the lipid burning in beige adipocytes (Un-ger, Scherer, & Holland, 2013). In addition to lower hormonal response to endurance PA, ineffective lipid oxidation can be observed with obese people. They have smaller mitochondria and / or impaired oxidation process within the mitochondria thus, being handicapped in their effort to lose fat (Colberg, Simoneau, Thaete, & Kelly, 1995; Borer, 2008). It is possible that "hyperinsulinemia" in overweight and obese compared with lean men contributed also to the blunted lipolytic response to exercise. Although the relative decrease in plasma insulin concentration was similar in lean, obese and overweight, the absolute plasma insulin concentrations were greater during exercise in overweight and obese than in lean subjects. It is also likely that the attenuated lipolytic response to exercise in overweight and obese men was caused by a blunted increase in epinephrine secretion and a concomitant reduction in adipose tissue lipolytic response to circulating catecholamines (Mittendorfer et al., 2004). "Adipocyte dysfunction due to either obesity or lipodystrophy is associated with excessive and untimely delivery of fatty acids to the liver and skeletal muscle and probably contributes to insulin resistance in both organs by altering the balance between fatty acids uptake / synthesis and the disposal leading to increases in intracellular lipid content." Also, an increasingly sedentary lifestyle and the associated relative increase in fat mass almost certainly contribute to aging induced insulin resistance. Muscle insulin resistance and accumulation of muscular TG precede the development of hepatic insulin resistance and type 2 diabetes (Savage et al., 2007). Exercise (insulin resistant boys; 45 minutes on elliptical
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trainer) resulted in a greater than threefold increase in postprandial net muscle glycogen synthesis, reflecting improved muscle insulin responsiveness, and a ~ 40 % reduction in net hepatic TG synthesis. The changes in the whole body energy storage were accompanied by a ~ 30 % decrease in hepatic lipogenesis and were independent of changes in fasting or postprandial plasma glucose and insulin concentrations (Rabol, Petersen, Dufour, Flannery, & Schulman, 2011). Exercise, as well as weight loss, reduced insulin resistance (Houmard et al., 2002). When considering lipid oxidation, it seems an inverse relationship between adiposity and the lipolytic response to exercise. The limited availability of systemic plasma fatty acids as a fuel in overweight and obese men was associated with a compensatory increase in the oxidation of non-systemic fatty acids.
Effects of Gender and Fitness Level on Lipid Oxidation during Activity
Women utilise more of lipids than men at the same relative activity intensity level (Kiens, 2006), Lipid oxidation remains the same during luteal and follicular phase of the menstrual cycle (Matsuo, Saitoh, & Suzuki, 1999). Due to adaptation mechanisms, regular endurance PA increases lipid utilisation during PA (Costill, Fink, Getchell, Ivy, & Witzmann, 1979; Koivisto, Hendler, Nadel, & Felig, 1982; Gollnick, 1977; Short & Sedlock, 1997; Jeppesen & Kiens, 2012). An increased lipid oxidation occurs due to increased capillary density (Kiens, Essen-Gustavsson, Christensen, & Saltin, 1993), increased lipid binding protein activity, an increase of fatty acid oxidation controlling enzymes (Kiens & Lithell, 1993; Alsted et al., 2009; Jeppesen et al., 2012), reduced insulin secretion and increased activation of adiponectin hormone in the adipose tissue (Civitarese et al., 2006). These adaptations to regular endurance PA increase the ability of mobilisation, transportation and oxidation of lipids in people with aerobic stamina (Henriksson, 1977; Kiens et al., 1993; Jeppesen et al., 2012). When considering lipid oxidation, women utilise more lipids than men, and after adaptation to training, greater lipid oxidation (recruit, transport and oxidize lipids) is observed during PA.
LIPID OXIDATION AFTER CONTINUOUS ACTIVITIY
Following PA, body immediately requires oxygen to regenerate its oxygen energy supplies (in myoglobin and haemoglobin), synthesis of phosphagens, removal of lac-tate from blood, increased need for oxygen in tissues due to increased temperature, an increase in catecholamine concentration and increased heart and respiratory muscles activity (Borsheim & Bahr, 2003). The period following the PA is known as the "excess post-exercise oxygen consumption" phase (EPOC) (Scott, 1997). Increased lipid oxidation and decreased carbohydrate oxidation can be observed during most of the EPOC period (Maehlum, Grandmontagne, Newsholme, & Sejersted, 1986; Bahr, Ingnes, Vaa-ge, Sejersted, & Newsholme, 1987; Bahr, Hansson, & Sejersted, 1990; Chad & Quigley, 1991; Short & Sedlock, 1997), thus, it was imperative to further study the literature on
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how it describes the EPOC amount and duration, and how lipids are utilised after PA. Amount and duration of EPOC are influenced by intensity and duration of PA (Sedlock, Fissinger, & Melby, 1989), the method of carrying out the PA (Almuzaini, Potteiger, & Green, 1998), the menstrual cycle (Matsuo et al., 1999), aerobic fitness level (Sedlock, Lee, Flynn, Park, & Kamimori, 2010) and amount of fatty tissue (Wong & Harber, 2006). Gender per se (Lamont, Romito, & Rossi, 2010), the amount of active muscles (Sedlock, 1991b) and nutrition (Bahr & Sejersted, 1991b) show no effect on EPOC.
Effect of Intensity and Duration of Activity on Lipid Oxidation after Activity
Intensity of PA is exponentially related to the EPOC level (Brehm & Gutin, 1986; Sedlock et al., 1989; Gore & Withers, 1990; Bahr & Sejersted, 1991a; Frey, Byrnes, & Mazzeo, 1993; Smith and Naughton, 1993; Hardman, 2001; Borsheim & Bahr, 2003), the duration of PA on the other hand is in linear relation to the EPOC level (Bahr et al., 1987; Chad & Wenger, 1988; Sedlock et al., 1989; Gore & Withers, 1990; Smith & Mc Naughton, 1993). Lipid oxidation following low-intensity long-term PA can be more than three times higher than during resting state (within three hours following 120 minutes of PA at 51 % VO2max intensity) (Bahr et al., 1990), low-intensity and / or short-term PA, however, does not lead to longer EPOC (B0rsheim & Bahr, 2003). When EPOC length was studied at constant intensity level and various durations of moderate-intensity PA (cycling at 70 % VO2max intensity), it was discovered that EPOC after 30, 45 and 60 minutes of moderate-intensity PA lasted ~ 2 hours, ~ 3 hours and ~ 7 hours, respectively (Chad & Wenger, 1988), after 80 minutes of cycling up to 12 hours (Maehlum et al., 1986; Bahr et al., 1987). When EPOC length was studied at constant duration (80 minutes of cycling) and various intensity levels of moderate-intensity PA (29 %, 50 % and 75 % VO2max), it was discovered that EPOC lasted respectively for ~ 20 minutes, ~ 3 hours and ~ 10 hours after the activity; respective EPOC amounts were ~ 10 kcal, ~ 30 kcal and ~ 150 kcal (Bahr & Sejersted, 1991b). EPOC amount studies on trained participants, 8 hours after a 20-, 50-, and 80-minute run at of 70% VO2max intensity, showed the values of ~ 25 kcal, ~ 50 kcal and ~ 75 kcal, respectively (Gore & Withers, 1990). Studying effect of intensity and duration on amount and duration of EPOC in trained men, showed that short term high-intensity PA brought about significantly higher EPOC (~ 30 kcal) than a low-intensity PA, regardless of its duration (~ 15 kcal). A short-term low-intensity PA resulted in significantly shorter EPOC (~ 20 minutes), compared to a long-term low-intensity PA (~ 30 minutes) and a short-term high-intensity PA (~ 35 minutes) (Sedlock et al., 1989).
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Effect of Dividing Activity into Sets and Amount of Working Muscles on Lipid
Oxidation after Activity
Studying whether dividing PA into sets has any effect, it was found that the EPOC amount after 2 sets separated by 6 hours of rest (15 minutes of cycling at 70 % VO2max intensity) was significantly greater than if same PA was done in a single set (30 minutes of cycling at 70 % VO2max intensity) (Almuzaini et al., 1998). Similar findings were reached in an earlier study where the EPOC amount after two sets (25 minutes of running at 70 % VO2max intensity) was significantly greater than if the PA was done in a single set (50 minutes of running at 70 % VO2max intensity) (Kaminsky, Padjen, & LaHam--Saeger, 1990).	^
EPOC amount and duration following PA for upper limbs (20 minutes, at 60 % VO2max intensity on upper limb cycle ergometer) and PA for lower limbs (20 minutes, 60 % VO2max intensity on lower limb cycle ergometer) are virtually the same (23 minutes and ~ 9 kcal for the upper limbs and 24 minutes and ~ 10 kcal for the lower limbs). It can be concluded that the amount of active muscles as well as absolute VO_ value
2max
do not affect the amount and the duration of EPOC (Sedlock, 1991b).
Effects of Gender on Lipid Oxidation after Activity
When comparing low-intensity PA (50 % VO2max, 500 kcal) and high-intensity PA (75 % VO2max, 500kcal) in women, three hours after a high-intensity PA (~ 40 kcal) EPOC amount was greater than after low-intensity PA (~ 20 kcal). During and after a low-intensity PA, more lipids were used (~ 37 g) than during and after a high-intensity PA (~ 28 g). This difference, however, was not statistically significant (p = 0.07) (Phelain, Reinke, Harris, & Melby, 1997). The study has two obvious shortcomings: lipid oxidation following a high-intensity PA was still increased, indicating EPOC after high-intensity PA lasts longer than three hours, which in turn indicates that the EPOC period was not measured in its entirety, and, secondly, the effect of menstrual cycle was not taken into account. EPOC and lipid oxidation after PA (60 minutes of cycling at 60 % VO2max intensity) are significantly greater in luteal than in follicular phase of the menstrual cycle (Matsuo et al., 1999). Not controlling the menstrual cycle could be the reason why no statistically significant differences were found in the amount and duration of EPOC (women cycling at various intensities) (Sedlock, 1991a). Normalising absolute EPOC value to lean mass results in disappearing gender differences (Tahara et al., 2008; Lamont et al., 2010).
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Effects of Amount of Fatty Tissue, Food Ingestion and Fitness Level on Lipid
Oxidation after Activity
EPOC in lean people lasts longer and is greater by one third than in overweight and obese people. Overweight and obese people have significantly higher RER value, which indicates that during the regeneration phase they use less lipids and that PA has a reduced effect on lipid oxidation increase during rest than in lean people (Wong & Harber, 2006). Similar conclusions were drawn in an earlier study; it was found that during rest neither low-intensity PA (40 % VO2max) nor moderate-intensity PA (70 % VO2max) resulted in fatty acid oxidation increase in obese people (van Baak, 1999). Ingesting food prior to moderate-intensity PA had no effect on the EPOC amount and duration (Bahr & Sejersted, 1991b).
Regular PA results in increased recovery effectiveness following PA (Hagberg, Hickson, Ehsani, & Holloszy, 1980): blood lactate level decreases, as does rectal temperature and hormonal response (Sedlock et al., 2010), thus reducing the EPOC duration (Frey et al., 1993; Sedlock, 1994; Short & Sedlock, 1997). The amount of EPOC when comparing relative values is identical (Kaminsky et al., 1986; Sedlock, 1994; Short & Sedlock, 1997; Borsheim & Bahr, 2003; Sedlock et al., 2010). If we compare absolute values, EPOC amount following a regular PA is significantly reduced (Sedlock et al., 2010), while the ability to metabolise fatty acids increases (Kaminsky, Knowlton, Perkins, & Hetzler, 1986; Short & Sedlock, 1997; Borsheim & Bahr, 2003; Gill et al., 2006; Ferreira et al. 2011).
Energy expenditure was significantly higher during rest even up to 48 hours after moderate-intensity PA (60 minutes running at 70 to 75 % VO2max intensity) (Jamurtas et al., 2004). In spite of all this, we must be aware that EPOC represents only up to 10 % of energy expended during PA (LeCheminant et al., 2008) or, depending on PA duration (from 20 to 80 minutes) and intensity (30, 50 or 70 % VO2max) only 1 to 8.9 % of energy expended during PA (Gore & Withers, 1990). When considering lipid oxidation in recovery phase after PA, the increased lipid oxidation can be observed during most of the EPOC period. Intensity of PA is exponentially related to the EPOC level, the duration of PA on the other hand is in linear relation to the EPOC. Dividing PA into sets causes greater EPOC than if the PA is in a single set. EPOC in lean people lasts longer and is greater. Normalising absolute EPOC value to lean mass results in disappearing gender differences, however, lipid oxidation after PA is significantly greater in luteal than in follicular phase of the menstrual cycle. If we compare absolute values, EPOC amount following regular PA is significantly reduced when comparing relative values is identical, while the ability to metabolise lipids increases. The amount of active muscles as well as ingested food prior to PA has no effect on the amount and duration of EPOC.
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INTERVAL TRAINING AND LIPID OXIDATION
During a high intensity PA, oxidation of plasma fatty acids, muscle and plasma TGs are lower than during a moderate intensity PA, despite greater energy expenditure (van Loon et al., 2001; Jeppesen & Kiens, 2012). Plasma glucose and muscle glycogen utilization is directly proportional to PA intensity (Romijn et al., 1993; van Loon et al., 2001), while the mechanism balancing lipid oxidation has yet to be explained (Jeppesen et al., 2011). "Carnitine could act as an acceptor of acetyl groups from acetyl-CoA, by forming acetylcarnitine, a reaction catalyzed by the mitochondrial enzyme carnitine acetyltransferase, when acetyl-CoA is generated faster than utilized by the Krebs cycle" (Jeppesen & Kiens, 2012). With increasing exercise intensities, muscle acetylcarnitine content is increased concomitantly with a decrease in the free carnitine content (Je-ppesen & Kiens, 2012). On the other hand, a low muscle content of free carnitine is supposed to lead to a diminished supply of the long chain fatty acid CoA to p-oxidation, limiting long chain fatty acid oxidation during high intensity exercise. Thus, an increased availability of pyruvate, acetyl-CoA formation, and 'binding' of the free carnitine during high intensity exercise also provide a potential mechanism, whereby fatty acid oxidation is down-regulated" (Jeppesen & Kiens, 2012). A comparison was made between lipid oxidation in untrained boys (aged 8 to 12), during and two hours after PA (30 minutes of cycling at intensity that maximises lipid oxidation determined for individual boy) and during and two hours after PA to which high-intensity short-term burst was added (cycling at intensity that utilized maximum lipids and every two minutes four seconds of maximum intensity). It was found that the amount of lipids metabolised and the EPOC amount were the same, for the same work performed (Crisp, Fournier, Licari, Braham, & Guelfi, 2012). The same EPOC amount and the duration was found in adult men as well following interval PA (three minutes of cycling at 30 % VO2max intensity and two minutes at 90 % VO2max intensity, seven repetitions) and continuous moderate-intensity PA (~ 30 minutes of cycling at 65 % VO2max intensity) for the same work performed. RER values were significantly lower in the 2-hour period following interval PA (McGarvey, Jones, & Petersen, 2005). Absolute values of metabolised fatty acids during and following the exercise were, unfortunately, not measured, so we still do not know whether lipid oxidation during and following a continuous PA is lower, equal or higher than during and after an interval PA for the same work performed. However, Hazell, Olver, Hamilton, and Lemon (2012) have recently demonstrated a similar total VO2 over 24 hours after sprint (high-intensity) interval exercise (four times 30-second maximal cycling at resistance of 10 % body mass with four-minutes rests) and continuous endurance exercise (30 minutes cycling at ~ 70 % VO2max) session (SIE = 498.0 ± 29.4 L; CEE = 500.2 ± 49.2 L; CTRL = 400.2 ± 44.6 L), indicating that the significant body-fat losses observed previously with sprint interval trainings are partially due to increases in oxidation post exercise.
Comparing the two hours following the high-intensity short-term burst of activity (four repetitions of 30-second intervals of sprinting on a cycle ergometer and 4.5 minutes of rest) to resting, a 75 % lipid oxidation increase was found (Chan & Burns,
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2013). The EPOC duration and the amount following the interval PA depends on a number of high-intensity short-term burst (Bahr, Grennered, & Sejersted, 1992) and work to rest ratio (Gosselin, Kozlowski Devinney-Boymel, & Hambridge, 2012). After two minutes of cycling at 108 % VO2max intensity, EPOC amount is ~ 30 kcal and lasts 30 minutes; after 2 series with a 3-minute break, EPOC amount is ~ 35 kcal and lasts 60 minutes; after 3 sets with two 3-minute breaks EPOC amount is ~ 80 kcal and lasts 4 hours (Bahr et al., 1992). The highest energy expenditure and the lowest blood lactate values are found when using 30 seconds of moderate-intensity PA and 30 seconds of high-intensity short-term activity (Gosselin et al., 2012; Zuniga et al., 2011). In a recent study (Kelly, King, Goerlach, & Nimmo, 2013), two commonly used high-intensity short-term activity protocols (10 times 1 minute of high-intensity cycling followed by a one-minute rest and 10 times 4-minute high-intensity cycling followed by a 2-min-ute rest), supposedly suitable for untrained people and people suffering from chronic diseases, were compared. It was discovered that during the 60 minutes after interval exercises, RER was lower in both protocols. But during the slow phase of EPOC period (from 1.25 to 9.25 hours) there were no significant differences between RER values or energy expenditure. They conclude that the effect on post-exercise metabolic rate was transient and relatively minor (Kelly et al., 2013).
Interval training causes both central (cardiovascular) and peripheral (skeletal muscle) body adaptations (Gibala, Little, MacDonald, & Hawley, 2012). High-intensity short-term training (10 x 2 minutes 105 % VO2max with 2 minutes breaks) increased the anaerobic threshold significantly more than endurance training (50 % VO2max 55 minutes or 70 % VO2max 35 minutes) in the same time period (Poole & Gaesser, 1985). Modern studies have come to similar conclusions. Just two-week high-intensity intermittent training (7 sessions every second day, each session consisted of 10 4-min cycling bouts at 90 % VO2max separated by 2 minutes of rest), increased post-training whole body lipid oxidation during the 60 minutes of cycling at 60 % VO2max in moderate trained women (menstrual cycle was not monitored) (Talanian, Galloway, Heigenhauser, Bonen, & Spriet, 2007). Studies show that low-volume high-intensity interval training increases a body's capability of lipid oxidation just as effectively as higher-volume moderate-intensity endurance training (Gibala et al., 2006; Gibala & McGee, 2008). However, considering time, interval training is a more time efficient strategy than continuous training (Burgomaster et al., 2008). Interval training is safe for healthy people as well as people "at risk" (Shiraev & Barclay, 2012). Studies on obese and metabolic syndrome patients report a similar or a greater effect of high-intensity interval training compared to endurance training on life quality, cardio-metabolic risk factors, aerobic fitness and cardio-vascular function, as well as blood glucose reduction, insulin signalling in adipose tissue and skeletal muscles, lowering the mean arterial blood pressure, and finally, on adipose tissue lipogenesis reduction, body weight and adipose tissue reduction (Earnest, 2008; Guiraud et al., 2012; Hansen, Dendale, van Loon, & Meeuseen, 2010; Kessler, Sisson, & Short, 2012; Tjenna et al., 2008). In practice, this translates to similar or greater effect, for at least 60 % less time spent doing high-intensity interval training compared to endurance training. This is a very significant aspect considering
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that "a lack of time" is the most commonly cited obstacle for participating in regular PA (Stutts, 2002; Kimm et al., 2006). When considering lipid oxidation, interval training is at least as effective as endurance training, with less time invested. Some people also find it more interesting.
RESISTANCE TRAINING AND LIPID OXIDATION
Muscles do not utilize lipids during resistance exercises (Melby, Scholl, Edwards, & Bullough, 1993). Resistance exercises are first ensued by anaerobic regeneration, the so-called "delayed glycolysis", a glycolytic process at the start of regeneration. It is significantly faster and more effective at phosphagens re-synthesis than at aerobic processes. It ensures re-synthesis of depleted phosphagens, up to the levels allowing oxidative processes to allow sufficient regeneration (Margaria et al., 1933, in di Prampero & Feretti, 1999). An increase in lipid oxidation has been found during EPOC period 30 to 120 minutes after finishing a resistance exercise (Binzen, Swan, & Manore, 2001). Intensity has been identified as a significant factor in EPOC amount following resistance exercise (Thornton & Potteiger, 2002) as well as the speed of execution (Scott, 2012) and the size of active muscle groups, a slight dependency on breaks between sets was also observed (Farinatti & Castinheiras, 2011; Haltom et al., 1999). No dependency was found towards the order in which the resistance exercise is carried out (Da Silva, Brentano, & Kruel, 2010), or the type of muscle contraction (Scott, 2012). During the first two hours following resistance exercise (2 sets, 8 repetitions at 85 % 8 RM), the EPOC amount was significantly higher than after the activities for strength endurance (2 sets, 15 repetitions 45 % 8 RM) at equal work carried out. No difference in RER was found following the resistance exercise or the activities for strength endurance (Thornton & Potteiger, 2002). Absolute lipid oxidation values were not measured, so we cannot conclude whether lipid oxidation after resistance exercise differs from those following activities for strength endurance. EPOC amount is dependent on execution speed of resistance exercises; it is significantly greater during slower execution (4s lift / 1s release or 1s lift / 4s release) in comparison to faster execution (1.5 second lift / 1.5 second release) (Scott, 2012). The EPOC amount following the resistance exercise of larger muscle groups is significantly greater than following resistance exercise of smaller muscle groups at equal repetitions and unequal work performed. Duration of rest between sets (1 or 3 minutes) had no effect on EPOC in larger muscle groups (Farinatti & Castinheiras, 2011). A shorter break between sets (20 seconds; 2 circular exercises for the upper and lower part, 20 repetitions 75 % 20 RM) resulted in significantly greater EPOC amount compared to same resistance exercise with a 1-minute break (Haltom et al., 1999). EPOC amount during the first 2 hours following resistance exercise was ~ 30 kcal (Binzen et al., 2001). Part of these calories is used for delayed glycolysis and part for lipid oxidation.
Regular resistance training, however, increases muscle mass, therefore increasing oxidation rate during rest as well as absolute lipid utilisation (Dolezal, Potteiger, Jacob-
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sen, & Benedict, 2000). Significantly, increased oxidation was found even 38 hours after the resistance training (31 minutes, 10 repetitions, maximum until exhaustion, for the entire body) (Schuenke, Mikat, & McBride, 2002), and 24 hours following the resistance training (60 minutes, 70 - 75 %, 1 repetition maximum, for the entire body) (Jamurtas et al., 2004). Heden (2011) found that in overweight people, there was a ~ 5 % increase in oxidation rate up to 72 hours during rest after the resistance training, following the recommendations of the American Society for Sport Medicine (Haskell et al., 2007; Heden, 2011).
Measuring local fatty acid oxidation during resistance exercise for the individual muscle groups (Dean et al., 2000) and (Helge, Stallknecht, Richter, Galbo, & Kiens, 2007) concluded that resistance exercise caused no noticeable hormonal changes and enabled exceptionally good circulation and oxygen supply to active muscles. By monitoring isotopes, muscle biopsies, oxygen consumption and RER during unilateral extension of the knee against resistance intensity ranging from 25 % to 85 % of maximum power - Pmax), the total fatty acid oxidation in the thigh increased 15 times (at 25 % Pmax intensity) compared to rest, and remained the same regardless of the intensity. Free fatty acid oxidation in the thigh increased with resistance exercise intensity, reducing oxidation of plasma TG and muscular TG. At 100 % Pmax intensity fatty acid oxidation capability decreased by a third compared to 85 % Pmax intensity. These results contradict activities that incorporate the muscles of entire body, such as cycling, where maximum lipid utilisation is at 65 % VO2max. The reason may lie in significantly greater blood circulation in the active muscles, when we perform resistance exercise for individual muscle groups than when we perform PA that includes greater muscle mass. This "super fusion" creates muscle environment that retains free carnitine and promotes lipid oxidation processes even at 80 % Pmax intensity. At intensities exceeding 80 % Pmax, the availability of free carnitine decreases, heavily diminishing the ability of lipid oxidation (Jeppeson & Kiens, 2012).
When combining endurance PA with resistance exercise it was found that the order of PA and the resistance exercise execution had no effect on the size and the duration of EPOC (Drummond, Vehrs, Schaalje, & Parcell, 2005; Oliveira & Oliveira, 2011). The order, however, did have an effect on RER. Execution of endurance PA prior to resistance exercise resulted in significantly lower RER, resulting in higher lipid oxidation, compared to the reverse order of endurance PA following resistance exercise (Oliveira & Oliveira, 2011). Resistance exercise (3 series at 70 % 1 repetition maximum, 10 repetitions, 105-second break between series or exercises, 7 exercises for upper and lower body), moderate-intensity PA (25 minutes of running at 70 % VO2max intensity), combination of moderate-intensity PA and resistance exercise (there was a 5-minute break in between) or resistance exercise and moderate-intensity PA, resulted in the same EPOC duration (~ 40 minutes) following the session (Drummond et al., 2005). When considering lipid oxidation, the total amount of lipids utilized during and following resistance exercise is negligible compared to lipid oxidation during and following the endurance PA or interval training, but regular resistance training increases muscle mass, therefore increasing oxidation rate and lipid utilisation during rest.
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CONCLUSIONS
Prolonged (> 30 minutes) moderate intensity (55 - 70 % VO2max) PA, such as walking, jogging or cycling, are the most effective way to increase lipid oxidation during and after a single exercise session. Studies also suggest no difference in lipid oxidation between periods following low-volume high-intensity interval exercise and traditional continuous endurance PA. However, time benefit of low-volume, high-intensity interval exercise compared to traditional endurance PA is significant. Further research is required to confirm whether adding just a few seconds of sprints during moderate-intensity endurance PA every so often would result in the same lipid oxidation as during a continuous PA without sprint intervals.
Regularity of PA seems most important. Regular continuous and regular interval exercise or activity triggers the same adaptation mechanisms, and increases one's fatty acid mobility, transport and oxidation capability. Further research is necessary to compare the effects of regular resistance, regular endurance and regular interval training on lipid oxidation effectiveness. Both regular endurance and regular interval training increase a certain amount of muscle mass, therefore increasing resting oxidation. It may also be of interest to compare the effects of Nordic walking, which additionally activates upper limb muscles in the movements and, thus, more muscle mass, as well as resistance exercise of the entire body on the effect of lipid oxidation.
Nutrition also significantly affects lipid oxidation. Food rich in fat and low in carbohydrates encourages lipid oxidation. It is essential not to exceed body's daily energy requirements, which leads to increased body weight and obesity. Obese and overweight people are recommended to take part in regular endurance or interval training. However, from the standpoint of relieving lower limbs joints, it may be better to participate in cycling or swimming, despite lower lipid oxidation potential.
REFERENCES
Achten, J., Gleeson, M., & Jeukendrup, A. E. (2002). Determination of the exercise intensity that elicits maximal fat oxidation. Medicine & Science in Sports & Exercise, 34(1), 92-97. VIEW ITEM Almuzaini, K. S., Potteiger, J. A., & Green, S. B. (1998). Effects of split exercise sessions on excess postexercise oxygen consumption and resting metabolic rate. Canadian Journal of Applied Physiology, 23(5), 433-443. VIEW ITEM Alsted, T. J., Nybe, L., Schweiger, M., Fledelius, C., Jacobsen, P., Zimmermann, R., et al. (2009). Adipose triglyceride lipase in human skeletal muscle is upregulated by exercise training. American Journal of Physiology, Endocrinology and Metabolism, 296(3), 445-453. VIEW ITEM Antonutto, G., & di Prampero, P. E. (1995). The concept of lactate threshold. The Journal
of Sports Medicine and Physical Fitness, 35(1), 6-12. Astrand, P. O., Rodahl, K., Dahl, H., & Stramme, S. B. (2003). Textbook of work physiology - 4th edition. Champaign: Human Kinetics.
109
ANNALES KINESIOLOGIAE • 6 • 2015 • 2
Barbara PURKART, Boštjan ŠIMUNIČ, Mitja GERŽEVIČ: AN OVERVIEW OF TRAINING METHODS THAT PROMOTE THE ..., 93-118
Astrup, A., Buemann, B., Christensen, N. J., Madsen, J., Gluud, C., Bennett, P., et al. (1992). The contribution of body composition, substrates and hormones to the variability in energy expenditure and substrate utilization in premenopausal woman. The Journal of Clinical Endocrinology and Metabolism, 74(2), 279-286. VIEW ITEM Bahr, R., Grannerad, O., & Sejersted, O. M. (1992). Effect of supramaximal exercise on excess postexercise O2 consumption. Medicine and Science in Sports and Exercise, 24(1), 66-71. VIEW ITEM Bahr, R., Hansson, P., & Sejersted, O. M. (1990). Triglyceride/fatty acid cycling is increased after exercise. Metabolism, 39(9), 993-999. VIEW ITEM Bahr, R., & Sejersted, O. M. (1991a). Effect of feeding and fasting on excess postexercise oxygen consumption. Journal of Applied Physiology, 71(6), 2088-2093. VIEW ITEM Bahr, R., Ingnes, I., Vaage, O., Sejersted, O. M., & Newsholme, E. A. (1987). Effect of duration of exercise on excess postexercise O2 consumption. Journal of Applied Physiology, 62(2), 485-490. VIEW ITEM Bahr, R., & Sejersted, O. M. (1991b). Effect of intensity of exercise on excess postexercise O2 consumption. Metabolism, 40(8), 836-841. VIEW ITEM Binzen, C. A., Swan, P. D., & Manore, M. M. (2001). Postexercise oxygen consumption and substrate use after resistance exercise in women. Medicine and Science in Sports and Exercise, 33(6), 932-938. VIEW ITEM Bonen, A., Luiken, J. J., Arumugam, Y., Glatz, J. F., & Tandon, N. N. (2000). Acute regulation of fatty acid uptake involves the cellular redistribution of fatty acid translocase. Journal for Biology and Chemistry, 275, 14501-14508. VIEW ITEM Bonen, A., Parolin, M. L., Steinberg, G. R., Calles-Escandon, J., Tandon, N. N., Glatz, J. F., et al. (2004). Triacylglycerol accumulation in human obesity and type 2 diabetes is associated with increased rates of skeletal muscle fatty acid transport and increased sarcolemmal FAT/CD36. FASEB Journal, 18, 1144-1146. VIEW ITEM Borer, K. T. (2008). How effective is exercise in producing fat loss? Kinesiology, 40(2),
126-137. VIEW ITEM Barsheim, E., & Bahr, R. (2003). Effect of exercise intensity, duration, and mode on postexercise oxygen consumption. Sports Medicine, 33(14), 1037-1060. VIEW ITEM Bray, G. A. (2013). Energy and fructose from beverages sweetened with sugar or high-fructose corn syrup pose a health risk for some people. Advances in nutrition, 4(2), 220-225. VIEW ITEM Brehm, B. A., & Gutin, B. (1986). Recovery energy expenditure for steady state exercise in runners and nonexercisers. Medicine and Science in Sports and Exercise, 18(2), 205-210. VIEW ITEM Burgomaster, K. A., Howarth, K. R., Phillips, S. M., Rakobowchuk, M., Macdonald, M. J., McGee, S. L., et al. (2008). Similar metabolic adaptations during exercise after low volume sprint interval and traditional endurance training in humans. The Journal of Physiology, 586(1), 151-160. VIEW ITEM Cahill, G. F. Jr. (2006). Fuel metabolism in starvation. Annual review of Nutrition, 26, 1-22. VIEW ITEM
Capostagno, B., & Bosch, A. (2010). Higher fat oxidation in running than cycling at the same exercise intensities. International Journal of Sport Nutrition and Exercise Metabolism, 20(1), 44-45.
110
ANNALES KINESIOLOGIAE • 6 • 2015 • 2
Barbara PURKART, Boštjan ŠIMUNIČ, Mitja GERŽEVIČ: AN OVERVIEW OF TRAINING METHODS THAT PROMOTE THE ..., 93-118
Chad, K. E., & Quingley, B. M. (1991). Exercise intensity: effect on postexercise O2 uptake in trained and untrained women. Journal of Applied Physiology, 70(4), 1713-1719. VIEW ITEM
Chad, K. E., & Wenger, H. A. (1988). The effect of exercise duration on the exercise and
post-exercise oxygen consumption. Canadian Journal of Sport Science, 13, 204-207. Chan, H. H., & Burns, S. F. (2013). Oxygen consumption, substrate oxidation, and blood pressure following sprint interval exercise. Applied Physiology, Nutrition and Metabolism, 38(2), 182-187. VIEW ITEM Civitarese, A. E., Ukropcova, B., Carling, S., Hulver, M., DeFrionzo, R. A., Mandarino, L., et al. (2006). Role of adiponectin in human skeletal muscle bioenergetics. Cell Metabolism, 4(1), 75-87. VIEW ITEM Colberg, S. R., Simoneau, J. A., Thaete, F. L., & Kelly, D. E. (1995). Skeletal muscle utilization of free fatty acids in women with visceral obesity. The Journal of Clinical Investigation, 95(4), 1846-1853. VIEW ITEM Costill, D. L., Fink, W. J., Getchell, L. H., Ivy, J. L., & Witzmann, F. A. (1979). Lipid metabolism in skeletal muscles of endurance trained males and females. Journal of Apllied Physiology, 47(4), 787-791. VIEW ITEM Crisp, N. A., Fournier, P. A., Licari, M. K., Braham, R., & Guelfi. K. J. (2012). Adding sprints to continuous exercise at the intensity that maximises fat oxidation: Implications for acute energy balance and enjoyment. Metabolism, 61(9), 1280-1288. VIEW ITEM Da Silva, R. L., Brentano, M. A., & Kruel, L. F. (2010). Effects of different strength training methods on postexercise energetic expenditure. Journal of Strength and Conditioning Research, 24(8), 2255-2260. VIEW ITEM Dean, D., Daugaard, J. R., Young, M. E., Saha, A., Vavvas, D., Asp, S., et al. (2000). Exercise diminishes the activity of acetyl-CoA carboxylase in human muscle. Diabetes, 49(8), 1295-1300. VIEW ITEM di Prampero, P. E., & Ferretti, G. (1999). The energetics of anaerobic muscle metabolism: a reappraisal of older and recent concepts. Respiration Physiology, 118(2-3), 103-115. VIEW ITEM
Dolezal, B. A., Potteiger, J. A., Jacobsen, D. J., & Benedict, S. H. (2000). Muscle damage and resting metabolic rate after acute resistance exercise with an eccentric overload. Medicine & Science in Sports & Exercise, 32(7), 1202-1207. VIEW ITEM Drummond, M. J., Vehrs, P. R., Schaalje, G. B., & Parcell, A. C. (2005). Aerobic and resistance exercise sequence affects excess postexercise oxygen consumption. Journal of Strength and Conditioning Research, 19(2), 332-337. VIEW ITEM Earnest, C. P. (2008). Exercise interval training: an improved stimulus for improving the
physiology of pre-diabetes. Medical Hypothesis, 71(5), 752-761. VIEW ITEM Farinatti, P. T., & Castinheiras Neto, A. G. (2011). The effect of between-set rest intervals on the oxygen uptake during and after resistance exercise sessions performed with large- and small-muscle mass. Journal of Strength and Conditioning Research, 25(11), 3181-3190. VIEW ITEM Ferreira, A. P., Ferreira, C. B., de Souza, V. C., de Almeida Cordova, C. O., Branco Silva, G. C., Nobrega, O. T., & de Fran?a, N. M. (2011). The influence of intense intermittent versus moderate continuous exercise on postprandial lipemia. Clinics (Sao Paulo), 66(4), 535-541. VIEW ITEM Fox, E. L., & Mathews, D. K. (1981). The physiological basis of physical education and athletics. Philadelphia: Saunders College Pub.
111
ANNALES KINESIOLOGIAE • 6 • 2015 • 2
Barbara PURKART, Boštjan ŠIMUNIČ, Mitja GERŽEVIČ: AN OVERVIEW OF TRAINING METHODS THAT PROMOTE THE ..., 93-118
Frayn, K. (2010). Metabolic regulation. Oxford: John Wiley & Sons. Frey, G. C., Byrnes, W. C., & Mazzeo, R. S. (1993). Factors influencing excess postexercise oxygen consumption in trained and untrained women. Metabolism, 42(7), 822-828. VIEW ITEM
Galbo, H., Holst, J., & Christensen, N. J. (1979). The effect of different diets and of insulin on the hormonal response to prolonged exercise. Acta Physiologica Scandinavica, 107(1), 19-32. VIEW ITEM Gibala, M. J., Little, J. P., MacDonald, M. J., & Hawley, J. A. (2012). Physiological adaptations to low-volume, high-intensity interval training in health and disease. The Journal of Physiology, 590(5), 1077-1084. VIEW ITEM Gibala, M. J., Little, J. P., van Essen, M., Wilkin, G. P., Burgomaster, K. A., Safdar, A., et al. (2006). Short-term sprint interval versus traditional endurance training: similar initial adaptations in human skeletal muscle and exercise performance. The Journal of Physiology, 575(3), 901-911. VIEW ITEM Gibala, M. J., & McGee, S. L. (2008). Metabolic adaptations to short-term high-intensity interval training: a little pain for a lot of gain? Exercise and Sport Sciences Reviews, 36(2), 58-63. VIEW ITEM Gill, J., Al-Mamari, A., Ferrell, W., Cleland, S., Sattar, N., Packard, C., et al. (2006). Effects of a moderate exercise session on postprandial lipoproteins, apolipoproteins and lipoprotein remnants in middle-aged men. Atherosclerosis, 185(1), 87-96. VIEW ITEM Gollnick, P. D. (1977). Free fatty acid turnover and the availibility of substrates as a limiting factor in prolonged exercise. Annals of the New York Academy of Science, 301, 64-71. VIEW ITEM
Goodpaster, B. H., Theriault, R., Watkins, S. C., & Kelley, D. E. (2000). Intramuscular lipid content is increased in obesity and decreased by weight loss. Metabolism, 49(4), 467-472. VIEW ITEM Gore, C. J., & Withers, R. T. (1990). Effect of exercise intensity and duration on postexercise metabolism. Journal of Applied Physiology, 68(6), 2362-2368. VIEW ITEM Gosselin, L. E., Kozlowski, K. F., Devinney-Boymel, L., & Hambridge, C. (2012). Metabolic Response of Different High Intensity Aerobic Interval Exercise Protocols. Journal of Strength and Conditioning Research, 26(10), 2866-2871. VIEW ITEM Guiraud, T., Nigam, A., Gremeaux, V., Meyer, P., Juneau, M., & Bosquet L. (2012). High-intensity interval training in cardiac rehabilitation. Sports Medicine, 42(7), 587-605. VIEW ITEM
Hagberg, J. M., Hickson, R. C., Ehsani, A. A., & Holloszy, J. O. (1980). Faster adjustment to and recovery from submaximal exercise in the trained state. Journal of Applied Physiology, 48(2), 218-224. VIEW ITEM Haltom, R. W., Kraemer, R. R., Sloan, R. A., Hebert, E. P., Frank, K., & Tryniecki, J. L. (1999). Circuit weight training and its effects on excess postexercise oxygen consumption. Medicine and Science in Sports and Exercise, 31(11), 1613-1618. VIEW ITEM
Hansen, D., Dendale, P., van Loon, L. J. C., & Meeuseen, R. (2010). The impact of training modalities on the clinical benefits of exercise intervention in patients with cardiovascular disease risk or type 2 diabetes mellitus. Sports Medicine, 40(11), 921-940. VIEW ITEM
112
ANNALES KINESIOLOGIAE • 6 • 2015 • 2
Barbara PURKART, Boštjan ŠIMUNIČ, Mitja GERŽEVIČ: AN OVERVIEW OF TRAINING METHODS THAT PROMOTE THE ..., 93-118
Hardman, A. E. (2001). Issues of fractionization of exercise (short vs long bouts). Medicine and Science in Sports and Exercise, 33(Supp. 6), 421-427. VIEW ITEM Haskell, W. L., Lee, I. M., Pate, R. R., Powell, K. E., Blair, S. N., Franklin, B. A., et al. (2007). Physical activity and public health: updated recommendation for adults from the American College of Sports Medicine and the American Heart Association. Medicine and Science in Sports and Exercise, 39(8), 1423-1434. VIEW ITEM Hazell, T. J., Olver, T. D., Hamilton, C. D., & Lemon, P. W. R. (2012). Two minutes of sprint-interval exercise elicits 24-hr oxygen consumption similar to that of 30 min of continuous endurance exercise. International Journal of Sport Nutrition and Exercise Metabolism, 22(4), 276-283. VIEW ITEM Heden, T. (2011). One-set resistance training elevates energy expenditure for 72 h similar
to three sets. European Journal of Applied Physiology, 111(3), 477-484. VIEW ITEM Helge, J. W., & Kiens, B. (1997). Muscle enzyme activity in man: Role of substrate availability and training. The American Journal of Physiology, 272(5), 1620-1624. VIEW ITEM
Helge, J. W., Richter, E. A., & Kiens, B. (1996). Interaction of training and diet on metabolism and endurance during exercise in man. The Journal of Physiology, 492(1), 293-306. VIEW ITEM Helge, J. W., Stallknecht, B., Richter, E. A., Galbo, H., & Kiens, B. (2007). Muscle metabolism during graded quadriceps exercise in man. The Journal of Physiology, 581(3), 1247-1258. VIEW ITEM Helge, J. W., Wulff, B., & Kiens, B. (1998). Impact of a fat rich diet on endurance in man: role of dietary period. Medicine and Science in Sports and Exercise, 30(3), 456-461. VIEW ITEM
Helge, J. W., Watt, P. W., Richter, E. A., Rennie, M. J., & Kiens, B. (2001). Fat utilization during exercise: adaptation to a fat-rich diet increases utilization of plasma fatty acids and very low density lipoprotein-triacylglycerol in humans. The Journal of Physiology, 537(3), 1009-1020. VIEW ITEM Henriksson, J. (1977). Training induced adaptations of skeletal muscle and metabolism during submaximal exercise. The Journal of Physiology, 270(3), 661-675. VIEW ITEM Hoeks, J., Van Herpen, N. A., Mensink, M., Moonen-Kornips, E., Van Beurden, D., Hesselink, M. K., et al. (2010). Prolonged fasting identifies skeletal muscle mitochondrial dysfunction as a consequence rather than cause of human insulin resistance. Diabetes, 59(9), 2117-2125. VIEW ITEM Horowitz, J. F. (2003). Fatty acid mobilization from adipose tissue during exercise. Trends
in Endocrinology and Metabolism, 14(8), 386-392. VIEW ITEM Houmard, J. A., Tanner, C. Y., Cunningham, P. G., Pories, W. J., MacDonald, K. G., & Schulman, G. I. (2002). Effect of weight loss on insulin sensitivity and intramuscular long-chain fatty acyl-CoAs in morbidly obese subjects. Diabetes, 51(10), 2959-2963. VIEW ITEM
Jamurtas, A. Z., Koutedakis, Y., Paschalis, V., Tofas, T., Yfanti, C., Tsiokanos, A., et al. (2004). The effects of a single bout of exercise on resting energy expenditure and respiratory exchange ratio. European Journal of Applied Physiology, 92(4-5), 393-398. VIEW ITEM
Jeppesen. J., Albers, P. H., Rose, A. J., Birk, J. B., Schjerling, P., Dzamko, N., et al. (2011). Contraction induced skeletal muscle FAT/CD36 trafficking and fatty acid uptake is AMPK independent. Journal of Lipid Research, 52, 699-711. VIEW ITEM
113
ANNALES KINESIOLOGIAE • 6 • 2015 • 2
Barbara PURKART, Boštjan ŠIMUNIČ, Mitja GERŽEVIČ: AN OVERVIEW OF TRAINING METHODS THAT PROMOTE THE ..., 93-118
Jeppesen, J., & Kiens, B. (2012). Regulation and limitations to fatty acid oxidation during
exercise. The Journal of Physiology, 590(5), 1059-1068. VIEW ITEM Jeppesen, J., Jordy, A. B., Sjaberg, K. A., Fullekrug, J., Stahl, A., Nybo, L., et al. (2012).
Enhanced Fatty Acid Oxidation and FATP4 Protein Expression after Endurance Exercise Training in Human Skeletal Muscle. PLoS One, 7(1). VIEW ITEM Kaminsky, L. A., Padjen, S., & LaHam-Saeger, J. (1990). Effect of split exercise sessions on excess postexercise oxygen consumption. British Journal of Sports Medicine, 24(2), 95-98. VIEW ITEM
Kaminsky, L. A., Knowlton, R G., Perkins, R. M., & Hetzler, R K. (1986). Relationships of aerobic capacity and percent body fat with plasma free fatty acid following walking. The American Journal of Clinical Nutrition, 44(5), 603-609. VIEW ITEM Kelley, D. E., & Goodpaster, B. H. (2001). Skeletal muscle triglyceride: an aspect of regional adiposity and insulin resistance. Diabetes Care, 24(5), 933-941. VIEW ITEM Kelly, B., King, J. A., Goerlach, J., & Nimmo, M. A. (2013). The impact of high-intensity intermittent exercise on resting metabolic rate in healthy males. European Journal of Applied Physiology, 113(12), 3039-3047. VIEW ITEM Kessler, H. S., Sisson, S. B., & Short, K. R (2012). The potential for high-intensity interval training to reduce cardiometabolic disease risk. Sports Medicine, 42(6), 489-509. VIEW ITEM
Kiens, B. (2006). Skeletal musle lipid metabolism in exercise and insulin resistance. Physiological Reviews, 86(1), 205-243. VIEW ITEM Kiens, B., Alsted, T. J., & Jeppesen, J. (2011). Factors regulating fat oxidation in human
skeletal muscle. Obesity Reviews, 12(10), 852-858. VIEW ITEM Kiens, B., Essen Gustavsson, B., Christensen, N. J., & Saltin, B. (1993). Skeletal muscle substrate utilization during submaximal exercise in man: Effect of endurance training. The Journal of Physiology, 469(1), 459-478. VIEW ITEM Kiens, B., & Lithell, H. (1993). Lipoprotein metabolism influenced by training induced changes in human skeletal muscle. The Journal of Clinical Investigation, 83(2), 558564. VIEW ITEM
Kimm, S. Y., Glynn, N. W., McMahon, R. P., Voorhees, C. C., Striegel-Moore, R. H., & Daniels, S. R. (2006). Self-perceived barriers to activity participation among sedentary adolescent girls. Medicine & Science in Sports & Exercise, 38(3), 534-540. VIEW ITEM
Kisner, C., & Colby, L. A. (2007). Therapeutic exercise. F. A. Davis Company, Philadelphia.
Koivisto, V., Hendler, R., Nadel, E., & Felig, P. (1982). Influence of physical training on the fuel-hormone response to prolonged low-intensity exercise. Metabolism, 31(2), 192-197. VIEW ITEM Kravitz, L., Robergs, R A., Heyward, V. H., Wagner, D. R., & Powers, K. (1997). Exercise mode and gender comparisons of energy expenditure at self-selected intensities. Medicine and Science in Sports and Exercise, 29(8), 1028-1035. VIEW ITEM Lamont, L. S., Romito, R., & Rossi, K. (2010). Fat-free mass and gender influences the rapid-phase excess postexercise oxygen consumption. Applied Physiology, Nutrition and Metabolism, 35(1), 23-26. VIEW ITEM LeCheminant, J. D., Jacobsen, D. J., Bailey, B. W., Mayo, M. S., Hill, J. O., Smith, B. K., et al. (2008). Effects of long-term aerobic exercise on EPOC. International Journal of Sports Medicine, 29(1), 53-58. VIEW ITEM
114
ANNALES KINESIOLOGIAE • 6 • 2015 • 2
Barbara PURKART, Boštjan ŠIMUNIČ, Mitja GERŽEVIČ: AN OVERVIEW OF TRAINING METHODS THAT PROMOTE THE ..., 93-118
Maehlum, S., Grandmontagne, M., Newsholme, E. A., & Sejersted, O. M. (1986). Magnitude and duration of excess postexercise oxygen consumption in healthy young subjects. Metabolism, 35(5), 425-429. VIEW ITEM Matsuo, T., Saitoh, S., & Suzuki, M. (1999). Effects of the menstrual cycle on excess postexercise oxygen consumption in healthy young women. Metabolism, 48(3), 275-277. VIEW ITEM
McArdle, W. D., Katch, F. I., & Katch, V. L. (2010). Exercise physiology: Nutrition,
energy and human performance (7th ed.). Philadephia: Lippincott Wilkins & Wilkins. McGarvey, W., Jones, R., & Petersen, S. (2005). Excess post-exercise oxygen consumption following continuous and interval cycling exercise. International Journal of Sport Nutrition and Exercise Metabolism, 15(1), 28-37. VIEW ITEM Melby, C., Scholl, C., Edwards, G., & Bullough, R. (1993). Effect of acute resistance exercise on postexercise energy expenditure and resting metabolic rate. Journal of Applied Physiology, 75(4), 1847-1853. VIEW ITEM Melby, C. L., Tincknell, T., & Schmidt, W. D. (1992). Energy expenditure following a bout of non-steady state resistance exercise. The Journal of Sports Medicine and Physical Fitness, 32(2), 128-135. VIEW ITEM Mittendorfer, B., Fields, D. A., & Klein, S. (2004). Excess body fat in man decreases plasma fatty acid availability and oxidation during endurance exercise. American Journal of Physiology, Endocrinology and Metabolism, 286(3), 354-362. VIEW ITEM Oliveira, N. L., & Oliveira, J. (2011). Excess postexercise oxygen consumption is unaffected by the resistance and aerobic exercise order in an exercise session. Journal of Strength and Conditioning Research, 25(10), 2843-2850. VIEW ITEM Pérez-Martin, A., Dumortier, M., Raynaud, E., Brun, J. F., Fédou, C., Bringer, J., et al. (2001). Balance of substrate oxidation during submaximal exercise in lean and obese people. Diabetes & Metabolism (Paris), 27(4), 466-474. VIEW ITEM Phelain, J. F., Reinke, E., Harris, M. A., & Melby, C. L. (1997). Postexercise energy expenditure and substrate oxidation in young women resulting from exercise bouts of different intensity. Journal of American College Nutrition, 16(2), 140-146. VIEW ITEM Pillard, F., van Wymelbeke, V., Garrigue, E., Moro, C., Crampes, F., Guilland, J. C., Berlan, M., de Glisezinski, I., Harant, I., Rivière, D., & Brondel, L. (2010). Lipid oxidation in overweight men after exercise and food intake. Metabolism: clinical and experimental, 59(2), 267-274. VIEW ITEM Poirier, P., Giles, T. D., Bray, G. A., Hong, Y., Stern, J. S., Pi-Sunyer, F. X., et al. (2006). Obesity and cardiovascular disease: pathophysiology, evaluation, and effect of weight loss: an update of the 1997 American Heart Association Scientific Statement on Obesity and Heart Disease from the Obesity Committee of the Council on Nutrition, Physical Activity, and Metabolism. Circulation, 113(6), 898-918. VIEW ITEM Poole, D. C., & Gaesser, G. A. (1985). Response of ventilatory and lactate thresholds to continuous and interval training. Journal of Applied Physiology, 58(4), 1115-1121. VIEW ITEM
Rabol, R., Petersen, K. F., Dufour, S., Flannery, C., & Schulman, G. L. (2011). Reversal of muscle insulin resistance with exercise reduces postprandial hepatic de novo lipogen-esis in insulin resistant individuals. Proceedings of National Academy of Science USA, 108(33), 13705-13709. VIEW ITEM Roepstorff, C., Halberg, N., Hillig, T., Saha, A. K., Ruderman, N. B., Wojtaszewski, J. F., et al. (2005). Malonyl-CoA and carnitine in regulation of fat oxidation in human
115
ANNALES KINESIOLOGIAE • 6 • 2015 • 2
Barbara PURKART, Boštjan ŠIMUNIČ, Mitja GERŽEVIČ: AN OVERVIEW OF TRAINING METHODS THAT PROMOTE THE ..., 93-118
skeletal muscle during exercise. American Journal of Physiology, Endocrinology and Metabolism, 288(1), 133-142. VIEW ITEM Romijn, J. A., Coyle, E. F., Sidossis, L. S., Gastaldelli, A., Horowitz, J. F., Enderte, E., et al. (1993). Regulation of endogenous fat and carbohydrate metabolism in relation to exercise intensity and duration. American Journal of Physiology, Endocrinology and Metabolism, 265(3), 380-391. VIEW ITEM Rui, L. (2014). Energy metabolism in the liver. Comprehensive physiology, 4(1), 177-197. VIEW ITEM
Savage, D. B., Petersen, K. F., & Schulman, G. L. (2007). Disordered Lipid Metabolism and the Pathogenesis of Insulin Resistance. Physiological reviews, 87(2), 507-520. VIEW ITEM
Scheen, A. J., Pirnay, F., Luyckx, A. S., & Lefebvre, P. J. (1983). Metabolic adaptation to prolonged exercise in severely obese subjects. International Journal of Obesity, 7(3), 221-229.
Schuenke, M. D., Mikat, R. P., & McBride, J. M. (2002). Effect of an acute period of resistance exercise on excess post-exercise oxygen consumption: implications for body mass management. European Journal of Applied Physiology, 86(5), 411-417. VIEW ITEM
Scott, C. B. (1997). Interpreting energy expenditure for anaerobic exercise and recovery: an anaerobic hypothesis. The Journal of Sports Medicine and Physical Fitness, 37(1), 18-23. VIEW ITEM
Scott, C. B. (2005). Contributions of anaerobic energy expenditure to whole-body thermo-
genesis. Nutrition & Metabolism, 2(1), 14. VIEW ITEM Scott, C. B. (2012). The effect of time-under-tension and weight lifting cadence on aerobic, anaerobic, and recovery energy expenditures: 3 submaximal sets. Applied Physiology, Nutrition and Metabolism, 37(2), 252-256. VIEW ITEM Scott, C. B., Leighton, B. H., Ahearn, K. J., & McManus, J. J. (2011a). Aerobic, anaerobic, and excess postexercise oxygen consumption energy expenditure of muscular endurance and strength: 1-set of bench presses to muscular fatigue. Journal of Strength and Conditioning Research, 25(4), 903-908. VIEW ITEM Sedlock, D. A. (1991a) Effect of exercise intensity on postexercise energy expenditure in
woman. British Journal of Sports Medicine, 25(1), 38-40. VIEW ITEM Sedlock, D. A. (1991b). Postexercise energy expenditure following upper body exercise.
Research Quarterly for Exercise and Sport, 62(2), 213-216. VIEW ITEM Sedlock, D. A. (1994). Fitness level and postexercise energy expenditure. The Journal of
Sports Medicine and Physical Fitness, 34(4), 336-342. VIEW ITEM Sedlock, D. A., Fissinger, J. A., & Melby, C. L. (1989). Effect of exercise intensity and duration on postexercise energy expenditure. Medicine and Science in Sports and Exercise, 21(6), 662-666. VIEW ITEM Sedlock, D. A., Lee, M. G., Flynn, M. G., Park, K. S., & Kamimori, G. H. (2010). Excess postexercise oxygen consumption after aerobic exercise training. International Journal of Sport Nutrition and Exercise Metabolism, 20(4), 336-349. Shiraev, T., & Barclay, G. (2012). Evidence based exercise - clinical benefits of high intensity interval training. Australian Family Physician, 41(12), 960-962. Short, K. R., & Sedlock, D. A. (1997). Excess postexercise oxygen consumption and recovery rate in trained and untrained subjects. Journal of Applied Physiology, 83(1), 153-159. VIEW ITEM
116
ANNALES KINESIOLOGIAE • 6 • 2015 • 2
Barbara PURKART, Boštjan ŠIMUNIČ, Mitja GERŽEVIČ: AN OVERVIEW OF TRAINING METHODS THAT PROMOTE THE ..., 93-118
Smith, J., & Mc Naughton, L. (1993). The effects of intensity of exercise on excess postexercise oxygen consumption and energy expenditure in moderately trained men and women. European Journal of Applied Physiology and Occupational Physiology, 67(5), 420-425. VIEW ITEM Spriet, L. L. (2011). Metabolic regulation of fat use during exercise and in recovery. Nestle
Nutrition Institute Workshop Series, 69, 39-53. VIEW ITEM Stamford, B. A. (1975). Maximal oxygen uptake during treadmill walking and running at
various speeds. Journal of Applied Physiology, 39(3), 386-389. VIEW ITEM Stutts, W. C. (2002). Physical activity determinants in adults. Perceived benefits, barriers, and self-efficacy. American Association of Occupational Health Nurses, 50(11), 499507. VIEW ITEM
Tahara, Y., Moji, K., Honda, S., Nakao, R., Tsunawake, N., Fukuda, R., et al. (2008).
Fat-free mass and excess post-exercise oxygen consumption in the 40 minutes after short-duration exhaustive exercise in young male Japanese athletes. The Journal of Physiological Anthropology, 27(3), 139-143. VIEW ITEM Talanian, J. L., Galloway, S. D., Heigenhauser, G. J., Bonen, A., & Spriet, L. L. (2007).
Two weeks of high-intensity aerobic interval training increases the capacity for fat oxidation during exercise in women. Journal of Applied Physiology, 102(4), 1439-1447. VIEW ITEM
Thornton, M. K., & Potteiger, J. A. (2002). Effects of resistance exercise bouts of different intensities but equal work on EPOC. Medicine and Science in Sports and Exercise, 34(4), 715-722. VIEW ITEM Tjanna, A. E., Lee, S. J., Rognmo, 0., Stolen, T. O., Bye, A., Haram, P. M., et al. (2008). Aerobic interval training versus continuous moderate exercise as a treatment for the metabolic syndrome: A pilot study. Circulation, 118(4), 346-354. VIEW ITEM Unger, R. H., Scherer, P. E., & Holland, W. L. (2013). Dichotomous roles of leptin and adiponectin as enforcers against lipotoxicity during feast and famine. Molecular biology of the cell, 24(19), 3011-3015. VIEW ITEM van Baak, M. A. (1999). Exercise training and substrate utilization in obesity. International
Journal of Obesity, 23(Suppl. 3), 11-17. VIEW ITEM van Loon, L. J., Greenhaff, P. L., Constantin Teodosiu, D., Saris, W. H., & Wagenma-kers, A. J. (2001). The effects of increasing exercise intensity on muscle fuel utilisation in humans. The Journal of Physiology, 536(1), 295-304. VIEW ITEM Van Proeyen, K., Szlufcik, K., Nielens, H., Ramaekers, M., & Hespel, P. (2011). Beneficial metabolic adaptations due to endurance exercise training in the fasted state. Journal of Applied Physiology, 110(1), 236-245. VIEW ITEM Wall, B. T., Stephens, F. B., Constantin Teodosiu, D., Marimuthu, K., Macdonald, I.
A.,	& Greenhaff, P. L. (2011). Chronic oral ingestion of L-carnitine and carbohydrate increases muscle carnitine content and alters muscle fuel metabolism during exercise in humans. The Journal of Physiology, 589(4), 963-973. VIEW ITEM
Walsh, T. S. (2003). Recent advances in gas exchange measurement in intensive care patients. British journal of Anaesthesia, 91(1), 120-131. VIEW ITEM Wilkin, L. D., Cheryl, A., & Haddock, B. L. (2012). Energy expenditure comparison between walking and running in average fitness individuals. Journal of Strength and Conditioning Research, 26(4), 1039-1044. VIEW ITEM Wojtaszewski, J. F., MacDonald, C., Nielsen, J. N., Hellsten, Y., Hardie, D. G., Kemp,
B.	E., et al. (2003). Regulation of 5'AMP-activated protein kinase activity and substrate
117
ANNALES KINESIOLOGIAE • 6 • 2015 • 2
Barbara PURKART, Boštjan ŠIMUNIČ, Mitja GERŽEVIČ: AN OVERVIEW OF TRAINING METHODS THAT PROMOTE THE ..., 93-118
utilization in exercising human skeletal muscle. American Journal of Physiology, Endocrinology and Metabolism, 284(4), 813-822. VIEW ITEM Wong, T., & Harber, V. (2006). Lower Excese Postexercise Oxygen Consumption and Altered Growth Hormone and Responses to Exercise in Obese Men. The Journal of Clinical Endocrinology and Metabolism, 91(2), 678-686. VIEW ITEM Zeni, A. I., Hoffman, M. D., & Clifford, P. S. (1996). Energy expenditure with indoor exercise machines. The Journal of the American Medical Association, 275(18), 14241427. VIEW ITEM
Zuniga, J. M., Berg, K., Noble, J., Harder, J., Chaffin, M. E., & Hanumanthu, V. S. (2011). Physiological responses during interval training with different intensities and durations of exercise. Journal of Strength and Conditioning Research, 25(5), 12791284. VIEW ITEM
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