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J Appl Physiol 99: 499-504, 2005; doi:10.1152/japplphysiol.00062.2005
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Modeling the blood lactate kinetics at maximal short-term exercise conditions in children, adolescents, and adults

Ralph Beneke,1,3 Matthias Hütler,2,3 Marcus Jung,3 and Renate M. Leithäuser1

1Centre for Sports and Exercise Science, Department of Biological Sciences, University of Essex, Colchester, United Kingdom; 2Department of Physical Medicine and Rehabilitation, Haukeland University Hospital, Bergen, Norway; and 3Institute of Sports Medicine, Free University, Berlin, Germany

Submitted 18 January 2005 ; accepted in final form 22 March 2005


   ABSTRACT
TOP
 ABSTRACT
MATERIAL AND METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 
Whether age-related differences in blood lactate concentrations (BLC) reflect specific BLC kinetics was analyzed in 15 prepubescent boys (age 12.0 ± 0.6 yr, height 1.54 ± 0.06 m, body mass 40.0 ± 5.2 kg), 12 adolescents (16.3 ± 0.7 yr, 1.83 ± 0.07 m, 68.2 ± 7.5 kg), and 12 adults (27.2 ± 4.5 yr, 1.83 ± 0.06 m, 81.6 ± 6.9 kg) by use of a biexponential four-parameter kinetics model under Wingate Anaerobic Test conditions. The model predicts the lactate generated in the extravasal compartment (A), invasion (k1), and evasion (k2) of lactate into and out of the blood compartment, the BLC maximum (BLCmax), and corresponding time (TBLCmax). BLCmax and TBLCmax were lower (P < 0.05) in boys (BLCmax 10.2 ± 1.3 mmol/l, TBLCmax 4.1 ± 0.4 min) than in adolescents (12.7 ± 1.0 mmol/l, 5.5 ± 0.7 min) and adults (13.7 ± 1.4 mmol/l, 5.7 ± 1.1 min). No differences were found in A related to the muscle mass (AMM) and k1 between boys (AMM: 22.8 ± 2.7 mmol/l, k1: 0.865 ± 0.115 min–1), adolescents (22.7 ± 1.3 mmol/l, 0.692 ± 0.221 min–1), and adults (24.7 ± 2.8 mmol/l, 0.687 ± 0.287 min–1). The k2 was higher (P < 0.01) in boys (2.87 10–2 ± 0.75 10–2 min–1) than in adolescents (2.03 x 10–2 ± 0.89 x 10–2 min–1) and adults (1.99 x 10–2 ± 0.93 x 10–2 min–1). Age-related differences in the BLC kinetics are unlikely to reflect differences in muscular lactate or lactate invasion but partly faster elimination out of the blood compartment.

glycolysis; extravasal compartment; invasion; elimination

THE BLOOD LACTATE CONCENTRATION (BLC) after maximal short-term, high-intensity exercise has been frequently described to be lower in children than in adolescents and adults (2, 7, 50). However, because of methodological differences with respect to mode and duration of maximal short-term, high-intensity exercise, blood sampling site, and assay for the BLC analysis, many studies provide largely overlapping ranges of BLC values irrespective of age (1, 8, 11, 20, 21, 26, 30, 41, 48).

Lower values of BLC in children compared with older individuals have been used to support the hypothesis that the maximal muscular glycolytic rate increases with the progress in maturation (2, 22, 42). However, such cases should be considered with care because the BLC does reflect not only an increase in lactate in the muscle compartment but also a number of other processes modulating the transport of lactate into and its elimination out of the blood compartment. Direct measurement of the latter physiological processes requires either invasive experimental methods such as muscle biopsies and combined arterial and venous catheterization, or sophisticated methods like nuclear magnetic resonance spectroscopy. Rare studies that conducted muscle biopsies in children provided inconsistent data about muscular lactate concentrations and anaerobic enzymes (9, 18, 19, 25, 32). Recent results of 31P-nuclear magnetic resonance spectroscopy studies were also quite evasive (33, 43, 51). These inconsistent findings possibly indicate an impaired external validity of the test situation with respect to real-life conditions. Additionally, physiological acute responses measured in a specific muscle, such as intramuscular lactate, pH, and high-energy phosphates, do not necessarily reflect the temporal features of noninvasive integral physiological measures, attainable under applied testing conditions (44, 49). Furthermore, and in particular in children, invasive procedures such as muscle biopsies are not only ethically restricted but also have limitations with respect to repetitive sampling with short time intervals, which is essential for the analysis of the dynamic behavior of physiological measures. Therefore, there is rare if any evidence that differences in postexercise BLC levels between children and adults do reflect age- and/or maturity-related differences in the ability of the skeletal muscle to generate lactate.

Comparison of selected studies all using 30-s cycling exercise, blood samples collected from the earlobe, and the same method for the analysis of the BLC does provide equivocal results due to differences in the time of blood sampling (20, 21, 48). However, highest BLC values were found if the BLC maximum was determined from blood samples subsequently collected every minute up to the seventh minute postexercise (48). This seems to indicate that differences in the BLC kinetics may have not been sufficiently considered in most of the previous studies. Consequently, the latter may indicate that differences in BLC levels observed at given time points postexercise possibly reflect variations in the kinetics of the BLC rather than dramatic divergences in the muscular metabolic profile between children and adults.

For the analysis of the BLC kinetics, we have fallen back on a common approach in clinical pharmacology. There, dynamic appearance and disappearance of a substance in the blood compartment after paravascular application is a frequent scenario, which is often managed on the basis of minimally invasive measurements and analyses by using various mathematical models such as the biexponential four-parameter kinetics model previously applied on numerous drugs (15). The present study, therefore, aimed to analyze the response of the BLC to the Wingate Anaerobic Test (WAnT) in prepubescent boys, adolescents, and adults using a biexponential four-parameter kinetics model based on BLC measurements pre- and up to 20 min postexercise. This analysis intends to provide indicators of the invasion and evasion of the BLC and of the lactate generated in the extravascular compartment. Furthermore, it allows the calculation of the maximum of the postexercise BLC (BLCmax), the corresponding time (TBLCmax), and the dynamics of the subsequent decrease of the BLC postexercise.


   MATERIAL AND METHODS
TOP
 ABSTRACT
 MATERIAL AND METHODS
RESULTS
 DISCUSSION
 REFERENCES
 
Subjects.   Fifteen prepubescent boys, 12 male adolescents, and 12 men participated in the present study (Table 1). All subjects were physically active, healthy nonsmokers, and no one was under pharmacological or specific dietetic treatment. Informed consent was obtained from all subjects or their guardians after explanation of the nature and risks involved in participation in the experiments, which conformed to internationally accepted policy statements regarding the use of human subjects as approved by the local ethic committee.


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  		Table 1. Anthropometric data

 
Procedures.   The subjects started with an incremental load test on an electrodynamically braked cycle ergometer (Excalibur Sport, Lode). The test started with a workload of 1.0 W/kg, which was increased by 0.5 W/kg after every second minute. The incremental load test was finished at individual maximal power output indicated by volitional fatigue after strong vocal encouragement. The incremental load test served for the determination of peak power (Ppeak), peak oxygen uptake (O2 peak) and peak BLC (BLCpeak). If the test was terminated at the end of a 2-min stage, then Ppeak was equivalent to this stage. If the test was terminated before the last stage had been completed, Ppeak was calculated as power of previous stage (W) plus power increment times duration of exercise at the final stage (s) divided by 120 s. O2 peak was defined as the highest oxygen uptake (O2) averaged throughout a 30-s time segment of the final minute of the test. Capillary blood samples were drawn from the hyperemic ear lobe during the final 15 s of each stage and every minute up to the fifth minute after test termination, and the BLC was immediately analyzed by the enzymatic amperometric method (Ebio Plus, Eppendorf). BLCpeak was determined as the highest BLC measured during the posttest period.

On a separate day, each subject performed a 30-s WAnT on a mechanically braked cycle ergometer (834 E, Monark). According to generally accepted recommendations for anaerobic performance testing (29), the WAnT sessions started with a standardized warming up of 5-min cycling at 0.5 W/kg, including two sprints lasting 3 s performed at the end of the third and the fourth minute as coordinative preparation for the subsequent high-intensity workload. After a subsequent 10-min rest, the subjects were instructed to pedal as fast as possible. A resistance corresponding to 7.5% of the body weight was applied after an acceleration phase of 3 s. After termination of the test, the subjects were supervised during a 20-min rest in seated position. Capillary blood was drawn immediately before and after the test, minute by minute up to the 10th, and every second minute up to the 20th minute of rest, and immediately analyzed.

All tests were carried out at similar times in the morning on separate days at least 2 h after a previous light meal. Time intervals between separated testing sessions were 1 wk. The subjects were instructed not to engage in strenuous activity during the day before an exercise test.

Data processing and statistical analysis.   WAnT performance expressed as peak power (PP) and minimum power (MP) were calculated as the highest and the lowest mechanical power elicited from the test taken as the average power over a 5-s period. The mean power output sustained throughout the six 5-s segments is defined as average power (AP). The power drop (PD) is the difference between PP and MP, whereas the fatigue index is the degree of PD during the test expressed as percentage of PP (29). All performance measures were calculated as related to body mass and estimated muscle mass (MM).

For the estimation of MM, the lean leg volume was calculated according to Dore et al. (14) in the boys and adolescents. The relative MM was predicted by assuming that lean leg volume represents the pattern of the development of the total mass of skeletal muscle and that the relative muscle mass in male subjects at an average age corresponding to the group of the adolescents is 42% of the body mass (10, 38, 40). In the adults, the relative MM was set at 42%, which is within the range of physically active male subjects aged 20–30 yr (27). Absolute MM was calculated from body mass and relative MM.

The BLC response to each single WAnT was individually analyzed by use of a four-parameter biexponential model. This model requires a BLC value at the start of exercise (BLC0), and a series of BLC values for as little as 20 min postexercise. It approximates an extravascular increase (A) in lactate generated by exercise metabolism, and two constants describing the kinetics of appearance (k1) and disappearance (k2) of lactate in the blood compartment (Eq. 1).

(1)
where t is time. Rearrangement of Eq. 1 enables for the calculation of BLCmax (Eq. 2), the TBLCmax (Eq. 3), and the turn point (TP), the time after that the decrease ({Delta}) of the posttest BLC can be described monoexponentially (Eq. 4).

(2)

(3)

(4)
The change of the extravascular lactate concentration related to MM (AMM) was estimated based on the assumption that the total lactate water space of the body represents ~62.5% and 60% of the body mass in the boys and in the adolescents and adults, respectively (3, 12, 13, 38).

Descriptive results are reported as mean values and standard deviations (SD). A multiple nonlinear regression analysis was used to test whether the biexponential four-parameter model sufficiently describes the behavior of the BLC over time and to determine the constants A, k1, and k2. Differences between subjects were analyzed by using a one-way ANOVA model with Tukey post hoc analyses. The interrelationships between selected variables were examined by simple linear and nonlinear regression analyses. For all statistics, the significance level was set at P < 0.05.


   RESULTS
TOP
 ABSTRACT
 MATERIAL AND METHODS
 RESULTS
DISCUSSION
 REFERENCES
 
In the incremental load test, BLCpeak was lower (P < 0.05) in the boys than in adolescents and adults. Ppeak was higher (P < 0.05) in adolescents than in boys and adults, whereas Ppeak related to muscle mass was lower in the adults than in boys and adolescents. No difference in O2 peak was found between the three groups but O2 peak related to muscle mass was lower (P < 0.05) in adults than in boys and adolescents (Table 2).


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  		Table 2. Incremental load test

 
Under WAnT conditions, the BLC was higher (P < 0.05) in adolescents and adults than in boys from the second postexercise minute on, but no difference in the BLC could be proven between adolescents and adults (Fig. 1). The test-by-test analysis of the kinetics of each single WAnT using the four-parameter biexponential model revealed relative explanations of the variance of the BLC over time of 98.7 ± 0.7, 98.3 ± 1.3, and 97.2 ± 2.6%, which were not different between boys, adolescents, and adults, respectively. Further analysis of residuals provided Durbin-Watson coefficients of 1.71, 1.56, and 1.12 in boys, adolescents, and adults, respectively, and showed that in the adults the four-parameter biexponential model slightly overestimated the BLC response during the initial 4 min combined with a slight underestimation of the BLC between the 9th and 16th minute post-WAnT, which was not the case in the adolescents and boys (Fig. 1). A and BLCmax were lower (P < 0.05) and TBLCmax and TP were shorter (P < 0.05) in boys than in adolescents and adults with no difference between the latter groups. The k2 was higher (P < 0.05) in boys than in adolescents and adults. A (Fig. 2), BLCmax (Fig. 3), and k2 (r = –0.38, y = –0.001x + 0.033, P < 0.05) were interrelated with age; k2 was also correlated with BLCmax (Fig. 4). No differences between the groups were found in k1 and AMM (Table 3). BLCmax was higher (P < 0.05) than BLCpeak in all groups. The latter difference, 1.5 ± 1.1, 0.7 ± 0.8, and 1.1 ± 1.0 mmol/l, was higher (P < 0.05) in boys than in adolescents and adults, respectively (Tables 2 and 3).



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  		Fig. 1. Measured blood lactate concentration (BLC) response to a Wingate Anaerobic Test (WAnT) was lower (*P < 0.05) in boys ({blacktriangleup}) than in adolescents ({blacklozenge}) and adults ({blacksquare}); the dynamics of the BLC (solid curve line) shown as average of all individual curve approximations in each group was faster (P < 0.05) in boys, than adolescents and adults.

 


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  		Fig. 2. Lactate generated in the extravascular compartment (A) shows a maximum during the third decade of life.

 


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  		Fig. 3. Maximum of the post-WAnT BLC (BLCmax) shows a maximum during the third decade of life.

 


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  		Fig. 4. Velocity constant of lactate elimination from the blood compartment (k2) decreases with an increase in the BLCmax.

 

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  		Table 3. Lactate response to the WAnT

 
In boys AP was lower (P < 0.05) than in adolescents and adults, whereas PP was only lower (P < 0.05) in boys than in adults, but there were no differences between adults and adolescents and boys and adolescents, respectively. MP was lower (P < 0.05) in boys than in adolescents, but no differences between adolescents and adults and boys and adults were found. Adults had a higher (P < 0.05) PD than adolescents, but there was no difference between boys and adolescents or boys and adults. However, if the latter measures of WAnT performance were related to MM, no difference between any of the age groups was found (Table 4).


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  		Table 4. WAnT performance

 

   DISCUSSION
TOP
 ABSTRACT
 MATERIAL AND METHODS
 RESULTS
 DISCUSSION
REFERENCES
 
The present study is the first approach to analyze age-related differences in the dynamic response of the BLC to high-intensity, short-term exercise based on a model comprising parameters for the extravascular increase in lactate generated by exercise metabolism, and the kinetics of appearance and disappearance of lactate into and out of the blood compartment. Previous, more complex system models that allow an objective analysis of theories on the regulation of ATP production in muscle cells, partly combined with the consideration of theories about limiting factors of oxygen transport to the muscle cell (3, 4, 35, 36, 37) have not been applied on age-related changes in the BLC response to exercise. Furthermore, and particularly when applied to maximal short-term exercise, they strongly rely on assumptions concerning the dynamics of the onset of the glycolytic system during the initial seconds of exercise and are therefore highly speculative.

The applied biexponential four-parameter model well described the behavior of the BLC under WAnT conditions as a cumulative effect of all related factors, irrespective of whether their specific behavior may be described adequately by using exponential models as well. The present results confirm previous results that both incremental load tests and also the WAnT generate lower (P < 0.05) levels of BLC in children compared with adolescents and adults (26, 47). Differences in the BLC response to exercise are more likely to be seen between children and adults or adolescents than between adolescents and adults (18, 26, 32). Differences in model parameters between boys, adolescents, and adults give support to the hypothesis that the difference in BLCmax is a result of a lower (P < 0.05) extravascular increase in lactate generated by the exercise metabolism during physical activity combined with faster elimination of the BLC from the intravascular compartment in boys compared with adolescents and adults, respectively. The latter also seems to explain differences (P < 0.05) in TBLCmax and TP.

However, the present results of lower (P < 0.05) levels of BLCmax as result of a lower (P < 0.05) extravascular increase in lactate generated by exercise do not support the idea of a reduced muscular glycolytic rate at younger age (18, 19, 23, 24). It seems that A has a maximum during the third decade of life. However, the finding that AMM and k1 are almost identical in all three age groups of the present study seems to be more in line with studies that could not confirm age-related divergences in anaerobic muscular metabolism (9, 25). The latter appears to get further support by similar measures of WAnT performance if expressed related to MM combined with good to excellent levels of performance under WAnT and incremental load conditions (5, 6, 8, 28, 30). Furthermore, AMM values of ~23 mmol/kg, which is equivalent to an intramuscular rate of lactate increase of ~0.77 mmol·kg–1·s–1, are well in the range of the magnitude of intramuscular lactates and energetic equivalents of anaerobic lactic energy production of previous studies using maximal cycling or electrical stimulation of comparable duration in adults (30, 31, 46). Such levels of intramuscular lactate increase are higher than corresponding levels found after O2 peak tests, which also showed age-related differences based on muscle biopsies (18, 32). However, in the present study the higher difference between BLCmax and BLCpeak in boys compared with adolescents and adults may support the idea of age-related differences in intramuscular lactate levels at O2 peak if determined by an incremental load test. Under the assumption that BLCpeak is found when lactate attained equilibrium in its total dilution space, in line with previous findings (18, 32), the present values of BLCpeak indicate a lower increase in muscle lactate in the magnitude of ~2–3 mmol/kg in the boys compared with the adolescents and adults at the incremental test. The latter differences in the lactate response to incremental load and WAnT combined with lower (P < 0.05) levels of O2 peak and Ppeak related to muscle mass in adults than in boys may indirectly provide further evidence for consistent findings of higher activities of aerobic muscular enzymes in children (9, 19, 25) and faster O2 kinetics in children compared with adults (34, 45).

The result that the elimination of BLC was almost 30% faster (P < 0.05) in the boys compared with adolescents and adults gives further evidence to the hypothesis that, compared with adults, children are superior in the decrease of BLC even under resting conditions (6). On the one hand, the latter may be attributed to higher resting metabolic rates in children compared with adolescents and adults (2); on the other hand, it may be also an effect of lower BLCmax (Fig. 3), an interrelationship described earlier (39). Both of the latter are accelerators of the BLC kinetics shortening TBLCmax in the boys compared with adolescents and adults.

The negative correlation between k2 and BLCmax (Fig. 4) supports previous reports that k2 decreases and the time constant ({tau}) or the half-time of the BLC during recovery (T1/2) increases, if the postexercise maximum of the BLC is higher (39). The present data also clearly indicate that most approaches based on the difference in the BLC between selected time points during the recovery period may be significantly flawed by the dynamics of the lactate invasion. The k1 values determined in the present study are more or less equivalent to a {tau} of 1.3 min, indicating that 5–6 min are required for a sufficient completion of the invasion of lactate into the blood compartment. Furthermore, if monoexponential models are applied, the inclusion of data before the TP of the postexercise BLC curve, e.g., data close to the highest level of the postexercise BLC leads to a systematic underestimation of k2 and corresponding overestimations of {tau} and T1/2 of between 10 and 25%, respectively.

Consequently the findings of no difference in k1 combined with age-related differences in k2 and a negative correlation between k2 and BLCmax does not support the conclusion of a most recent study that in boys the disappearance dynamics of the BLC after maximal short-term exercise are not different from those of men (17), although almost identical levels of BLC had been measured and equally to the present results BLCmax values of ~10.5 mmol/l were combined with a value of T1/2 of ~20 min. However, in the latter study similar levels of BLCmax had been achieved by using shorter tests in adults compared with children (17). In a within-subject design, BLCmax and A are a function not only of exercise intensity but also of the duration of exercise, whereas k2 decreases if the test duration is increased from 10 to 30 s (Beneke R, Masen DJ, Leithäuser RM, unpublished data). Consequently, similar rates in the decrease of the BLC after short-term exercise of different duration resulting in similar levels of BLCmax in children and adults (17) are more likely the effect of test duration rather than similar kinetics of the disappearance of the BLC.

In conclusion, after maximal short-term exercise the BLCmax is lower and earlier reached in boys than adolescents and adults. There are almost no differences in the BLC response between the latter two groups. The difference in the kinetics of the BLC between boys, adolescents, and adults appears to reflect a lower extravascular increase in lactate generated by the maximal short-term exercise combined with a faster elimination of the BLC. The extravascular increase of lactate seems to have a maximum during the third decade of life. Nevertheless, the latter does not support the hypothesis of a reduced muscular glycolytic rate, but it is consistent with lower relative muscle mass, higher relative total lactate water space, and favorable conditions for the aerobic metabolic system in boys than in adolescents and adults, respectively.


   FOOTNOTES
 

Address for reprint requests and other correspondence: R. Beneke, Dept. of Biological Sciences, Univ. of Essex, Wivenhoe Park, Colchester CO4 3SQ, United Kingdom (E-mail: rbeneke{at}essex.ac.uk)

The costs of publication of this article were defrayed in part by the payment of page charges. The article must therefore be hereby marked "advertisement" in accordance with 18 U.S.C. Section 1734 solely to indicate this fact.


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 DISCUSSION
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B. A. Keller
State of the Art Reviews: Development of Fitness in Children: The Influence of Gender and Physical Activity
American Journal of Lifestyle Medicine, February 1, 2008; 2(1): 58 - 74.
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