Medicine & Science in Sports & Exercise:
Basic Sciences: Symposium: New insights into the control of human muscle blood flow and metabolism in vivo Recent Advances
Quantification of anaerobic energy production during intense exercise
Section Editor(s): Richardson, Russell S. Chair
Copenhagen Muscle Research Centre, August Krogh Institute, University of Copenhagen, DENMARK
Submitted for publication March 1997.
Accepted for publication April 1997.
Anaerobic energy production during supramaximal exercise has been estimated from muscle metabolic changes. Based on such measurements the anaerobic energy production was determined to be 63 and 189 mmol ATP·kg-1 d.w. for 60 and 142 s of exhaustive cycling exercise, respectively. These estimations do not, however, include release of lactate from the exercising muscles. Furthermore, the anaerobic production cannot be related to the work performed since the muscle biopsy sample may not be representative for the muscles involved in the exercise, and the total anaerobic energy production during whole body exercise cannot be determined because the mass of the muscles used is unknown. When a single muscle is exercised, the problems are minimized. With a one-legged knee-extensor exercise model, which uses a defined muscle mass, the anaerobic energy production has been estimated to be 370 mmol ATP·kg-1 d.w. for a 192-s exhaustive exercise period. Estimated pulmonary oxygen deficit based on an energy demand extrapolated from a linear relationship between exercise intensity and oxygen uptake at submaximal exercise does not appear to represent the anaerobic energy production during whole body exercise.
Since Berzelius in 1841 (5) wrote to Lehman,“Dass ein muskel desto mehr Milchsaure enthalt, je mehr er vorher angestrengt worden is,” there has been great interest in the anaerobic energy system of the muscle. In the early 20th century, several researchers were dealing with the quantification of the anaerobic energy production. The terms “alactacid” and “lactacid anaerobic energy output” were coined (18). The energy of the alactacid was derived from the fast splitting of ATP (adenosine triphosphate) and creatine phosphate (CP) stored in the muscle and the lactacid part from glycolysis ending up with lactate formation. On the basis of these concepts and blood lactate determinations, anaerobic energy production during exercise was estimated in man (8,19). However, in 1937 Sacks and Sacks (23) were aware that it was difficult to conclude anything about muscle lactate formation from blood lactate data. The introduction of the needle biopsy technique (4) made it possible to determine local changes in the concentrations of certain metabolites such as lactate, ATP, and CP. This methodology has been used frequently, and in this brief review it will be considered to what extent such determinations of metabolites can be used to determine the anaerobic energy production. Since the oxygen deficit methodology is frequently used, how well the oxygen deficit expresses the anaerobic energy turnover will also be discussed. The review will deal with only human studies and will focus on the anaerobic energy turnover during supramaximally exercise intensities.
DIRECT DETERMINATIONS OF ANAEROBIC ENERGY PRODUCTION
To quantify the anaerobic energy production during intense dynamic exercise, muscle biopsies have been obtained before and after muscle contractions. Based on the decrease in muscle CP and ATP, as well as accumulation of metabolites like pyruvate and lactate, the anaerobic energy production of the biopsied muscle has been determined. Boobis(6) found that the anaerobic energy production during 6 and 30 s of maximal cycling was 63 and 189 mmol ATP·kg-1 d.w., respectively, of which glycolysis was estimated to contribute 53 and 64%, respectively. For exhaustive exercise bouts lasting 2-3 min Karlsson and Saltin (15) and Medbø and Tabata(21) estimated the anaerobic energy production to be 172 and 234 mmol ATP·kg-1 d.w., respectively. Similar values have been obtained in studies involving running and maximal isokinetic muscle contractions (Table 1).
From measurements on a muscle biopsy it is difficult to determine the total anaerobic energy turnover during whole body exercise such as cycling, since the mass and the activity of the muscles involved are unknown and the metabolic response of the biopsied muscle may not be representative of all of the muscles included in the exercise.
Another problem in the aforementioned studies is that the energy turnover related to the release of lactate to the blood from the exercising muscles is not taken into account. Therefore, the anaerobic energy production of the biopsied muscle is underestimated. The question is how much. It is difficult to estimate the release of lactate based on accumulation of lactate in the blood during intense exercise since it is unclear how large the dilution volume of lactate is. It may be as low as 80 mL·kg-1 body mass corresponding to blood volume or as high as 400 mL·kg-1 body mass corresponding to the total body fluid (7).Table 2 shows calculations of the total release of lactate based on lactate accumulation in the blood for various exercise durations in the study by Medbø and Tabata (21) with a minimal and maximal dilution volume of 6 and 30 L (body mass of subjects: 75 kg). The estimated energy release related to lactate release ranged between 5 and 38% of the total anaerobic energy production. It should be noted that these calculations underestimate the true release from the active muscles since the metabolization of lactate in various tissues, such as the heart and inactive muscles, during the exercise is not taken into account. Thus, these calculations suggest that the lactate release may represent a substantial anaerobic energy production and cannot be ignored, as is often done.
One way to determine the release of lactate is to measure the a-vdiff lactate over, and blood flow to, the exercising muscles. From measurements of arterial and femoral venous blood lactate, Katz et al.(16) estimated the mean lactate release to be 7 mmol·min-1 at the end of an intense cycle exercise bout, which can be compared with 15 mmol·min-1 during knee-extensor exercise(14). The difference is partly related to the higher arterial lactate concentrations during whole body exercise compared with knee-extensor exercise (2). In both studies an almost linear relationship between the muscle lactate gradient and lactate release has been observed (Fig. 1). However, the a-vdiff lactate for a given muscle lactate gradient appeared to be lower during cycling than during knee-extensor exercise (Fig. 2). One explanation is that lactate to a significant extent is taken up by inactive and low intensity exercising muscles/muscle fibers in the legs during cycling. Thus, the estimated lactate release, based on measurements of femoral a-vdiff lactate, will markedly underestimate the release from the active muscles during cycling. This problem also exists in the knee-extensor exercise model (see example in Fig. 3), but it is minimized as blood flow from the lower leg is occluded. To evaluate the magnitude of the lactate uptake by the inactive hamstrings and adductor muscles during knee-extensor exercise, femoral venous blood from the contralateral resting leg was collected during intense knee-extensor exercise. At the end of exercise the mean uptake of lactate, in the approximately 7.8 kg of inactive muscles, was 1.0 mmol·min-1 corresponding to an uptake of lactate by the hamstrings and adductor muscles of about 0.4 mmol·min-1 at the end of the knee-extensor exercise. This represents an underestimation of lactate release from the quadriceps muscle of about 3%.
It appears that it is difficult to quantify the anaerobic energy production during whole body dynamic exercise such as cycling and running. Therefore, we used the knee-extensor model in which the exercise is confined to an isolated muscle, namely, the quadriceps muscle. Subjects performed exhaustive exercise(approximately 3 min) at a work rate corresponding to an energy production of about 130% of peak ˙VO2 for the exercising muscles(1). Leg blood flow was measured and arterial and femoral venous blood samples were collected frequently during the exercise. In addition, a muscle biopsy was taken before and immediately after the exercise. Lactate efflux was estimated to contribute with as much as one-third of the lactate production. The net lactate production by the quadriceps muscle, determined as the total lactate release from the quadriceps muscles (taken into account that lactate is taken up by the hamstrings/adductor muscles) and lactate accumulation, corresponded to an energy production of 280 mmol·kg-1 d.w. With the addition of the energy released from muscle CP breakdown, changes in nucleotides, and accumulation of glycolytic intermediates, the total anaerobic energy production was estimated to be 370 mmol·kg-1 d.w. (Fig. 4). This was slightly higher than the anaerobic ATP provision of about 305 mmol·kg-1 d.w. by a quadriceps muscle after 200 s of intermittent electrical stimulation(24). The difference was probably caused by the occlusion of the circulation in the latter study. The finding that the lactate released to the blood during the one-legged dynamic exercise corresponded to an anaerobic energy production of 90 mmol·kg-1 d.w.(1) supports this concept.
Figure 4-Anaerobic e...Image Tools
The one-legged knee extensor model seems to allow for reasonably accurate quantification of the anaerobic energy production during dynamic exercise in an isolated muscle. During knee-extensor exercise muscle blood flow is higher and arterial lactate levels are lower than during whole body exercise. However, conditions that are similar to those occurring during whole body exercise can be obtained in the knee-extensor model by combining the one-legged knee-extensor exercise with contralateral leg and upper body exercise.
INDIRECT DETERMINATION OF ANAEROBIC ENERGY PRODUCTION
Since Krogh and Lindhard (17) introduced the oxygen deficit concept in the early part of this century, the oxygen deficit has frequently been used as a determination of the anaerobic energy production. In the one-legged knee-extensor study, the anaerobic energy production determined from changes in metabolites was close to the anaerobic energy production estimated from the leg O2 deficit, which was determined as the difference between estimated energy demand and total leg oxygen uptake(Fig. 4; 1). The close relationship between the two estimations for a single muscle group speaks in favor of using the oxygen deficit also as a measure of the anaerobic energy production during whole body exercise. However, there appear to be some problems.
First, the finding that 14 well-trained runners had a higher oxygen uptake at high submaximal running speeds than the energy demand estimated from a linear relationship between oxygen uptake and lower speeds indicates that the relationship is not linear from low to high submaximal speeds(Fig. 5; 3). Thus, the energy demand during supramaximal intensities may be underestimated when extrapolated from a linear relationship between oxygen uptake and submaximal speeds. This means that the higher the intensity chosen for the supramaximal exercise the more pronounced the underestimation of the true oxygen deficit.
Figure 5-Relationshi...Image Tools
Second, it has been observed that the oxygen uptake progressively increases as exercise at high submaximal speeds is continued. Consequently, the relationship between oxygen uptake and speed is dependent upon when the oxygen uptake measurements are performed during the submaximal exercises. As an example, Figure 6 shows the estimated energy demands during the supramaximal exercise when oxygen uptake was measured after 4-6 min or after 8-10 min of each submaximal running bout. The estimated oxygen deficit was 33% higher when the longer exercise periods were used.
Figure 6-Individual ...Image Tools
Third, the anaerobic energy production during submaximal exercise is not taken into account in the calculation of the energy demand during supramaximal exercise. It is well known that blood lactate is elevated during high intensity submaximal exercise, reflecting lactate production in the exercising muscles and thus representing an anaerobic energy production. The energy production related to lactate production has been estimated to be at least 10% of the aerobic energy production at high intensity submaximal exercise(1).
These findings seem to suggest that the energy demand during supramaximal exercise cannot be estimated from a linear extrapolation from submaximally measurements. Nevertheless, the oxygen deficit method is frequently used, and it has been claimed that the oxygen deficit provides an accurate measure of the anaerobic energy production.
Medbø and Tabata (21) found a high correlation between the oxygen deficit and the anaerobic energy production determined from muscle metabolic measurements assuming that the mass of active muscle corresponded to 25% of body mass and that the metabolic response in the biopsied muscle was representative for all active muscles(Fig. 7). The high correlation between the two determinations is not surprising since subjects performed both exercise of short (30 s) and long (2-3 min) duration. The short exercise bouts give both a very high rate of anaerobic energy turnover and a high oxygen deficit per time unit since both determinations are related to the oxygen uptake, which is limited in the initial phase of exercise. Similarly, when longer exercise times are used, both the metabolically determined rate of anaerobic energy turnover and the oxygen deficit per time unit is low because of a more pronounced oxygen uptake than during the shorter exercise bouts. Therefore, the high correlation does not provide evidence that the oxygen deficit expresses the anaerobic energy production during whole body exercise. On the other hand, several findings in the study by Medbø and Tabata(21) suggest that the oxygen deficit cannot be used to quantify the anaerobic energy turnover. There was a lack of correlation between oxygen deficit and the metabolically determined anaerobic energy production for each exercise duration (Fig. 7). Furthermore, for the same anaerobic energy production (x-axis) an almost twofold difference in oxygen deficit was observed (see values in circles inFig. 7). In addition, the release of lactate to the blood was not taken into account in the study by Medbø and Tabata (1993). Thus, the estimated metabolic anaerobic energy production (x-axis) was underestimated and probably more so with longer exercise periods.
Figure 7-Individual ...Image Tools
It would be nice if a simple measure such as the oxygen deficit could be used to determine the anaerobic energy production during intense exercise. Unfortunately, it appears that the energy provided from anaerobic sources during intense whole body exercise cannot be quantified from oxygen deficit determinations when energy demand during supramaximal exercise is estimated from a linear relationship between work intensity and energy production during submaximal exercise. Clearly, further studies are needed to examine what the energy demand during intense exercise is.
Several problems arise when the total anaerobic energy production during intense whole body exercise, such as cycling and running, is estimated from measurements in biopsies obtained before and after the exercise. By using a model in which a single muscle is exercising and the mass of active muscles can be quantified, such as the knee-extensor exercise model, the problems are minimized and the anaerobic energy production can be determined more accurately. Estimated pulmonary oxygen deficit that is based on an energy demand extrapolated from a linear relationship between exercise intensity and oxygen uptake at submaximal exercise does not appear to represent the anaerobic energy production during exercise.
The experiments reported in this article were performed in collaboration with B. Saltin, T. Graham, L. Johansen, B. Kiens, and S. Strange. The studies were supported by grants from Team Danmark, the Danish Natural Science Foundation (11-0082), the Danish National Research Foundation (504-14), and Brandts Legat.
Address for correspondence: Jens Bangsbo, The August Krogh Institute, LHF, Universitetsparken 13, DK-2100 Copenhagen Ø, Denmark.
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ANAEROBIC ENERGY; SUPRAMAXIMAL EXERCISE; LACTATE; OXYGEN DEFICIT; CREATINE PHOSPHATE; ADENOSINE BIPHOSPHATE
©1998The American College of Sports Medicine
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