Abstract and Introduction

Abstract

Children recover from physical exertion faster than adults, especially, from high-intensity exercise. It is argued that, qualitatively, this is due mainly to dimensional differences but that, predominantly, it is a quantitative difference, stemming from the lower relative power children can generate and from which they need to recover. Children's lesser power capacity is, in turn, likely due to maturation-dependent neuromotor differences.

Introduction

Children appear to recover from physical exertion faster than adults. This notion is widely accepted among professionals and laymen alike. However, data demonstrating this difference are surprisingly limited,^[6,7,11,14] while attempts to explain it are even more scarce.

Children have long been shown to possess anaerobic power capacity that is lower compared with adults (e.g.,^[8]). In fact, even after correcting for differences in body mass, children's peak torque and peak power output reach only 60—80% that of adults.^[7,14] Using 31P magnetic resonance spectroscopy (MRS), Zanconato et al.^[15] indirectly found a lower rate of lactate (La) production during maximal exercise in children compared with adults. Lower La production can directly explain children's observed lower La accumulation and their lower peak blood La concentration ([La]). Assuming [La] to be inversely related to subsequent performance capacity would entail that lower [La] after a given exercise bout would facilitate faster recovery. Zafeiridis et al.^[14] recently demonstrated that muscle power decline, within 4 × 30-s and 2 × 60-s sets of maximal knee extensions-flexions, was smaller in boys compared with both adolescents and adults. Similar age-related differences were also reported within a series of 10-s bouts of cycling.^[11] Hebestreit et al.^[7] demonstrated that, after the 30-s Wingate Anaerobic Test (WAnT), prepubertal boys were able to duplicate their performance after a 2-min recovery, whereas adults were still unable to do so after 10 min (Fig. 1). Although a more limited fatigue could explain children's ability to repeat intense physical exercise in short succession,^[7] their faster performance recovery was also shown to be independent of fatigue.^[14]     

Children's faster recovery, therefore, appears to be predominantly due to lower power generation. This is a quantitative child-adult difference. In other words, it can be argued that children recover faster from high-intensity exercise because they have less to recover from.

Considering congruent evidence, notably children's lower muscular contraction velocity and relative force ( Table 1 ), we argue that children are more limited in their ability to recruit and use higher-hierarchy motor units. This, most likely, is due to neuromuscular immaturity-in either neuro-motor control or incomplete motor-unit differentiation.

True qualitative differences in recovery are largely traceable to dimensional differences between children and adults, affecting intramuscular and circulatory transit times. These differences can allow for a faster initial diffusion and initiation of metabolites breakdown.

Purpose

The purpose of this manuscript is to review child-adult differences in the recovery from high-intensity exercise and the factors responsible for them. In doing so, we want to reevaluate existing knowledge and establish a novel view of children's recovery and a new perspective of the factors involved in recovery.

Methodological Difficulties

Recovery Criteria

Intense exercise results in acute physiological responses of the metabolic, cardiovascular, respiratory, endocrine, immune, and neuromuscular systems. During the recovery from such exercise, numerous physiological processes take place, aimed at restoring homeostasis and functional capacity ( Table 2 ). These processes are not linear (e.g., see Ref. 3), and their kinetics are widely different (e.g., preexertion muscle glycogen stores take considerably longer to restore than ATP or plasma volume). The kinetics of these processes have mostly been studied in adults, although some comparative pediatric data do exist ( Table 2 ). As the recovery of performance capacity is clearly a function of physiological recovery, growth-or maturity-related differences in the rate of physiological processes could explain part of the faster performance recovery observed in children.^[7,11,14] However, the definition of recovery and its study are somewhat complicated by the fact that a complete return to homeostasis or to the physiological preexertion state is not necessary for a complete recovery of performance capacity. That is, residually elevated levels of factors such as heart rate (HR), core temperature, metabolic rate, or even [La] may not harm and often even benefit subsequent performance. This and the differential time axes of the various processes make it important to distinguish and clearly specify what kind of recovery is discussed, namely, physiological or that of the actual performance capacity.

Exercise Intensity

As pointed out earlier, maximal short-term performance is not comparable between children and adults. That is, although the exertion can be of maximal subjective intensity, the body mass-relative power output will still be considerably lower in children.^[7,8,11] The same will be true for any exertion at a given percentage of maximal power. Due to the considerable age-related size differences, the use of identical power outputs is not a methodological option. A realistic alternative is to normalize power output to total body, lean body, or muscle mass. However, in such a case, children's power output will constitute a considerably higher percentage of their maximal power capacity. Another possible approach is to use allometric scaling. However, because different body mass and height exponents have been suggested in the literature with no apparent consistency, this possibility remains ambivalent at the moment. Most studies have used maximal performance for comparison. The disadvantages of this approach are the significant differences in the deviation from homeostasis after that exertion and hence different states from which children and adults would have to recover. In addition, the prerequisite of maximal motivation is a crucial factor that cannot be a priori presumed identical in children and adults. This can normally be overcome by sufficient familiarization and habituation to the exercise tests and by proper encouragement and incentive to exercise at maximal effort.

Resting Values

Resting values of many physiological variables (e.g., HR and oxygen consumption, O₂) are higher in children compared with adults. Therefore, even if both groups attain similar values at maximal effort, the difference between resting and peak values will be smaller for the children. For example, if both groups reach a postexercise HR of 190 beats · min^-1, children's full recovery would be a return to 80—90 beats · min^-1, whereas the corresponding adult value could be some 15 beats · min^-1 lower than that.

"Peak" Values

Peak physiological values attained by children in response to maximal exercise are typically different from the corresponding adult values. Notable examples are peak [La] which has consistently been shown to be much lower in children^[3,7,11,14] or peak HR after maximal exhausting exertions (e.g.,^[3,7]). Again, this means that children may not start their recovery from a point identical or readily comparable with that of adults. This complicates any attempt of comparing recovery on common grounds.

A possible approach of managing the different resting and peak HR values is to define deviations from homeostasis as net change or as percentages of HR reserve (peak HR - resting HR), as has already been done in some studies.^[3,7]

Still, it is both practically and methodologically impossible to simultaneously control for all exercise and recovery variables, and it is normally necessary to equate groups by a single process or variable.

Recovery Processes — Differences Between Children and Adults

Cardiorespiratory Function

Hebestreit et al.^[7] demonstrated a faster recovery of ventilatory rate, HR, and O₂ in prepubertal boys, compared with men, after the 30-s WAnT. These findings agree with other studies^[3,11,14] that compared HR and O₂ kinetics between children and adults, after different exercise intensities as well as different exercise and recovery durations. To circumvent the difficulties associated with the child-adult cardiorespiratory differences, some of those studies normalized HR and O₂ responses to their respective resting values and presented them as "net" responses.^[3,7]

Lactate Clearance

Exercise La production is related to exercise intensity and duration, as well as to the magnitude, composition, and fitness level of the involved muscle mass. Also, La production should be significantly affected by the motor-unit recruitment pattern—mainly, the glycolytic versus oxidative motor-unit involvement, in performing a given task.

Muscle and blood [La] after intense exercise is a negative correlate of subsequent performance capacity, whether independently or secondary to its close association with high hydrogen ion concentration ([H⁺]) during and immediately after exercise. Indeed, [La] can be seen simply as a component of the strong ion difference portion of acid-base balance. Despite some controversy in the literature, it is widely accepted that, whether directly or indirectly, a faster reduction of [La] will hasten recovery from exercise and enhance closely subsequent performance.

In a recent study, we examined the question of whether children's faster recovery is due to their inferior power output, lesser La production, and subsequent lower blood [La], or to a higher La-disappearance rate and faster [La] decline toward preexercise levels.^[3] After a 30-s WAnT, [La] was monitored for 60 min in men and in prepubertal boys. On a subsequent session, the men performed a shortened version of WAnT to match the [La] peak attained earlier by the boys. Boys and men were thus equated by their respective exercise intensity (maximal) as well as by their peak postexercise [La]. In accordance with previous reports,^[6,12] after the 30-s WAnT, peak [La] was markedly lower in the boys (Fig. 2a) but was reached considerably earlier (5.0 vs 7.6 min after exercise in the boys and men, respectively). When peak postexercise [La]'s were equated and temporally aligned, their disappearance curves merged into a statistically single line with practically identical La-disappearance half-times that were, in turn, identical to those observed after the men's 30-s WAnT (~20 min, measured from peak [La]). It thus appears that although children may differ from adults in the production and accumulation of La, they do not differ in the rate of its elimination.

In a noteworthy study, Beneke et al.^[1] compared the full spectrum of postexercise (WAnT) La kinetics between children, adolescents, and adults. For the first time, a biexponential model was used in children to reflect La production and peak concentration, as well as appearance and disappearance rates into and from the blood. The authors' interpretation of their finding was that children clear La from their blood faster than adults. However, in their model, the authors did not account for dimensionality differences, namely, children's smaller intramuscular perfusion distances and shorter circulation times (see later discussion). As is the case with the kinetics of variables such as O₂, these differences directly effect a hastening of La appearance in blood and shortening of the time lag to peak [La], as was also shown by Beneke et al..^[1] However, in their model, this unaccounted-for effect presented itself as an overestimate of the children's actual La production. Consequently, to allow for children's lower observed peak [La], the model produced a corresponding higher disappearance coefficient. The authors' conclusion stands in disagreement with our study that deliberately avoided the pitfalls of the La-appearance phase.^[3] Moreover, that conclusion contradicts the practically identical La-disappearance slopes evident in the La curves depicted by Beneke et al. (Fig. 2b).

Electrolytes and Acid-base Balance

After intense exercise, there is a transitional increase in plasma electrolytes in both children and adults.^[6] Hebestreit et al.^[6] could not show differences between boys and men in the increase of potassium ion concentrations in the blood during a 10-min recovery from a 30-s WAnT. Sodium and calcium ions concentrations increased to a lesser extent in boys, whereas chloride concentrations did not increase at all in the boys. Most of the electrolyte disparity between the two age groups could be explained by the smaller postexercise changes in plasma volume in children compared with adults. Thus, there does not seem to be a marked child-adult difference in the extent of electrolyte movement into the bloodstream, after exercise.

Using 31P MRS, Zanconato et al.^[15] showed higher muscle pH (lower acidity) in children, after maximal exercise. These findings correspond with those of Hebestreit et al.^[6] and Ratel et al.^[12] who showed a lesser plasma [H⁺] response in boys after a short exhaustive exercise. In their boys, Hebestreit et al.^[6] also found smaller changes in strong-ion difference and in plasma pCO₂. These changes appeared earlier and subsided faster compared with the men, reflecting not only a more limited perturbation of the acid-base balance but also its faster recovery. Again, these findings conform to the notion of children's more limited reliance on glycolytic motor units, lower power production, and having less to recover from.

Restoration of Energy Substrates

The restoration of short-term muscle power, such as that required in anaerobic-type activities, depends on the resynthesis of energy substrates. Only creatine phosphate (CrP) resynthesis has been studied in both children and adults. Using 31P MRS, Taylor et al.^[13] demonstrated faster intramuscular CrP resynthesis and recovery half-times, after graded exercise of the calf muscles in 6- to 12-yr-old children compared with adults. The faster CrP resynthesis has been attributed to children's greater reliance on oxidative metabolism and lower dependence on glycolytic metabolism. This explanation is consistent with our notion of differential motor-unit recruitment patterns. That is, children's more limited use of higher-hierarchy motor units would mean a higher relative reliance on lower-hierarchy motor units and would make for a more oxidative intramuscular milieu in which faster resynthesis of energy substrates is facilitated.

Neuromotor Function

The EMG is a reflection of motor-unit action potentials within the monitored muscle. EMG pattern changes normally stem from changes in recruited motor-unit numbers and/or excitation frequency, although changes in conduction velocity or level of motor-unit synchronization may also play a role. Although it is difficult to distinguish between all those factors, EMG pattern changes reflect changes in neuromotor function.

There is limited information concerning age-related neuromuscular functional differences, in general, and on exercise-related differences, in particular. The available data focus on neuromotor function during exercise and not on the recovery therefrom. The data are mainly concerned with agonist/antagonist muscle activity during nonfatiguing conditions. To our knowledge, there are no published data on neuromotor function during recovery from exercise in children. Preliminary data^[5] demonstrate that, after 10 min of plantar flexion at 20% of maximal voluntary contraction, the recovery of both torque and EMG activity of the agonist muscles (plantar flexors) was faster in children than in their adult counterparts. These preliminary data suggest that recovery of neuromotor function, as reflected by EMG pattern, is faster in children compared with adults.

Consistent with our notion of maturation-differentiated motor-unit recruitment patterns, we believe that it is during the exercise itself, not during recovery, that the neuromotor system exerts its main differentiating effect on children compared with adults; that is, the neuromotor system determines the magnitude of power production and thereby affects the extent of fatigue and of the required consequent recovery.

Possible Reasons for Faster Recovery in Children

Children's observed faster recovery is, in our view, mainly due to children's lower maximal power output in the initial exercise bout and consequently having less to recover from. However, dimensional and possibly other maturation-related differences in muscle morphology and metabolic characteristics may also contribute to children's faster recovery (Fig. 3).

Dimensional Characteristics

Children are characterized by a smaller muscle fiber diameter,^[2] resulting in a shorter mean muscle-blood diffusion distance. In animals, a shorter diffusion distance has been shown to correlate with higher capillary density,^[10] suggesting that children, too, are characterized by a relatively greater functional capillarization. These anatomical differences would allow for a faster transition of metabolites (e.g., La, H⁺,and CO₂) from muscle to blood. In addition, children's smaller body dimensions translate into shorter cardiovascular circulation distances and shorter circulation times. These phenomena effectively explain children's faster O₂ and HR kinetics during and after exercise,^[3,7] as well as children's earlier peaking of [La] after exercise.^[1,3] Two points should be noted here.^[1] Those dimensional differences do not affect metabolism and therefore account only for [La]'s earlier peaking, not for any difference in actual La removal from the blood.^[2] Children's O₂ kinetics is affected by the dimensional differences via faster gas exchange at both the muscular and pulmonary end sites. Unlike oxygen, children's La kinetics do not benefit at the pulmonary end site as it cannot be expelled by the pulmonary system.

Earlier [La] peaking, in our view, is therefore the major qualitative recovery advantage that children have over adults (Fig. 4).

Aerobic-Anaerobic Metabolism

During short intense exercise, children rely relatively more on oxidative rather than anaerobic metabolism than do adults.^[7] Children have been shown to possess lower intramuscular glycogen and CrP stores, compared with adults, and to use them to a lesser extent during exercise ( Table 1 ). Findings of lower phosphofructokinase^[4] and lactate dehydrogenase activities^[9] and, on the other hand, of faster return to homeostasis after exertion (CrP resynthesis)^[13] and acid-base balance^[12] are consistent with children's lesser glycolytic capacity and lower peak [La] after exercise.^[3,11,14] True qualitative musculometabolic differences between children and adults cannot be excluded. However, we suggest that these observed differences are predominantly a reflection of children's relative disuse of higher-hierarchy glycolytic motor units and not peculiar characteristics of their muscular makeup. Although metabolic differences have hitherto been regarded as underlying causes of the observed age-related differences in performance or recovery capacity, we suggest that they are consequential reflections of a more fundamental neuromotor difference.

Conclusion

Children typically recover from short, high-intensity exercise considerably faster than adults. Most of this seeming advantage is likely a direct consequence of children's limited power capacity—a quantitative difference. Although requiring additional experimental support, this is likely due to children's inability to recruit higher-hierarchy motor units to the extent typically attained by adults. Most of the observed metabolic or compositional differences could be attributed to a differential motor-unit recruitment and usage. Qualitatively, children's true advantage lies in the shorter delay between the onset of exercise or its termination and the peaking of metabolites in the blood, allowing the recovery process to commence earlier. This qualitative difference, however, comprises only a small portion (few minutes) of the total recovery duration or of the apparent difference in that duration between children and adults.

Challenges for the Future